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Mixotrophy and the toxicity of Ochromonas in a pelagic food web
Abstract
1. Toxic compounds produced by many phytoplankton taxa are known to have negative effects on competitors (allelopathy), anti-predatory effects on grazers (mortality or impaired reproduction) or both. Although mixotrophs of the genus Ochromonas are known to be toxic to zooplankton, it has often been assumed in studies of plankton community processes that all flagellates in the size range of this taxon are edible to typical zooplankton grazers (i.e. cells ≤30 μm for Daphnia, ≤6 μm for rotifers).
2. We explored the toxicity of a species of Ochromonas to other planktonic taxa, including its competitors (two species of phytoplankton and protists) and consumers (two species of zooplankton). To test if mode of nutrition by this mixotroph influences its toxicity to other taxa, we exposed each test species to Ochromonas cultured in chemostats under four different nutritional regimes: osmotrophy (labile dissolved organic carbon) and phagotrophy (bacterial prey) in both light and dark conditions (i.e. with or without photosynthesis).
3. Filtrate from osmotrophically fed Ochromonas had a significant negative effect on the population growth rate of two obligate phototrophic phytoplankton, Cryptomonasozolini and Chlamydomonas reinhardtii. The protists Tetrahymena tetrahymena and Paramecium aurelia were also negatively affected by Ochromonas filtrate. Ochromonas cells were toxic to both the rotifer Brachionus calicyflorus and the cladoceran Daphnia pulicaria, with the toxic effects significantly more severe when fed at high cell densities (75 000 cells mL−1) than at low densities (7500 cells mL−1). Ochromonas cultured osmotrophically in the light was more toxic to the Daphnia than cells cultured under other conditions. In contrast, Ochromonas from all nutritional conditions was equally highly toxic to Brachionus.
4. Our findings support the view that Ochromonas can be toxic to other components of the food web with which it interacts. It is especially toxic to zooplankton that directly consume it, although the effect depends upon Ochromonas cell density and whether or not a good food source is simultaneously present. Our results call into question the common practice of pooling flagellates into a single ‘functional group’ included in an ‘edible phytoplankton’ category of cells <30 μm in diameter.
... Those taxa belong to the group of mixotrophic chrysophyceans. Several studies indicate that multiple species of this group show toxic activity at which negatively impacting zooplankton feeding (Nielsen et al., 1990;Boenigk and Stadler, 2004;Barreiro et al., 2005;Hiltunen et al., 2012;Vad et al., 2020). It seems that those observations also apply to the presently studied zooplankter E. gracilis. ...
... Erkenia subaequiciliata, Ochromonas spp.; c.f. Boenigk and Stadler, 2004;Hiltunen et al., 2012), small, chain-forming diatoms (Cyclotella spp. 7 -20 µm; Stephanodiscus hantzschii), and colony-forming, partly gelatinous chlorophytes (e.g. ...
... However, nutritional mode can modulate dietary quality, and existing studies suggest that osmotrophic nutrition may enhance deleterious effects (Hiltunen et al., 2012;Leeper & Porter, 1995) and modulate fatty acid profiles (Boëchat et al., 2007). Altogether, these suggest that dietary quality of mixotrophs may dynamically vary through space and time. ...
... Firstly, toxicity seems to be a common trait in chrysophytes (Table 1), however, it may depend on physiological strategies, e.g., direct (osmotrophy) and indirect (phagotrophy) use of DOC can result in different consequences on consumers (Hiltunen et al., 2012;Leeper & Porter, 1995). Notably, the two species (O. ...
• The importance of mixotrophic algae as key bacterivores in microbial food webs is increasingly acknowledged, but their effects on the next trophic level remain poorly understood. Their high stoichiometric food quality is contrasted by anti-grazing strategies.
• We tested the quality of freshwater mixotrophs as prey for zooplankton, using four non-colonial chrysophyte species and a cryptophyte as a high quality reference food. We (1) analyzed the stoichiometric and biochemical (fatty acid) composition of the mixotrophs, and (2) quantified their dietary effects on Daphnia longispina survival.
• Survival of D. longispina significantly depended on the identity of species provided as food, ranging from higher to lower as compared to starvation. This was not reflected in differences in cellular stoichiometry or fatty acid profiles of the mixotrophs. We suggest that toxicity may be the driver for the observed differences.
• Generalization of the dietary effects of mixotrophic chrysophytes does not appear straightforward. Besides fundamental species-specific differences, potential toxic effects may vary depending on environmental cues or physiological strategies. Notably in our study, Ochromonas tuberculata, a species previously reported to be deleterious, turned out to be a beneficial food source in terms of enabling high survival of D. longispina.
• We challenge the generality of the assumption that chrysophytes are of low value as food for zooplankton. We recommend that future studies test how environmental conditions and physiological strategies shape the quality of mixotrophs as food for consumers at higher trophic levels, specifically focusing on effects of dietary toxicity.
... In freshwater ecosystems, chrysophytes (Chrysophyceae) represent a major mixotrophic group accounting for a considerable share of phytoplankton in oligo-and mesotrophic lakes that also frequently form blooms (Watson et al. 1997;Ptacnik et al. 2008). Their expected increase in dominance urges for a better understanding about their role in pelagic trophic relationships, such as their contribution for secondary production, especially as some species are potentially toxin-producing (Boenigk and Stadler 2004;Hiltunen et al. 2012;Watson et al. 2015). We particularly lack information on the bottom-up role of colonial taxa among genera like Uroglenopsis and Dinobryon. ...
... Here we provided evidence that it represents low-quality food for zooplankton and therefore its dominance may have serious consequences for pelagic carbon flow by altering secondary production with possible species-specific differences in consumers. Our findings, together with deleterious effects on zooplankton reported for other species of chrysophytes (Boenigk and Stadler 2004;Hiltunen et al. 2012), highlight the need for considering taxonomic differences (e.g., cryptophytes are high-quality food) and taxon-specific traits (e.g., grazing resistance, toxins) when assessing the food quality of mixotrophic protists. Such information is critical to resolve uncertainties and refine global models on the importance of mixotrophy in trophic webs. ...
Growing evidence suggests that global climate change promotes the dominance of mixotrophic algae especially in oligotrophic aquatic ecosystems. While theory predicts that mixotrophy increases trophic transfer efficiency in aquatic food webs, deleterious effects of some mixotrophs on consumers have also been reported. Here, using a widespread mixotrophic algal genus Dinobryon, we aimed to quantify how colonial taxa contribute to secondary production in lakes. We therefore studied the dietary effects of Dinobryon divergens on Cladocera (Daphnia longispina) and Copepoda (Eudiaptomus gracilis), representing two main taxonomic and functional groups of zooplankton. In feeding experiments, we showed that Dinobryon was largely grazing resistant and even inhibited the uptake of the high-quality reference food in Daphnia. Eudiaptomus could to some extent compensate with selective feeding, but a negative long-term food quality effect was also evident. Besides, Eudiaptomus was more sensitive to the pure diet of Dinobryon than Daphnia. Low lipid content and high C:P elemental ratio further supported the low nutritional value of the mixotroph. In a stable isotope approach analysing a natural plankton community, we found further evidence that carbon of Dinobryon was not conveyed efficiently to zooplankton. Our results show that the increasing dominance of colonial mixotrophs can result in reduced dietary energy transfer to consumers at higher trophic levels. In a wider perspective, global climate change favours the dominance of some detrimental mixotrophic algae which may constrain pelagic trophic transfer efficiency in oligotrophic systems, similarly to cyanobacteria in eutrophic lakes.
... We used a three-species, intraguild predation, marine planktonic food web as our study system. (Hiltunen et al., 2012). We eventually chose a marine system because salinity provided, along with temperature and chemostat dilution rate, an additional controllable parameter. ...
... Because the analysis was based on Taylor-series approximations for nearequilibrium dynamics, the qualitative predictions are robust to model details such predator functional responses. For numerical simulations in this paper, we used a model very similar to that in Hiltunen et al. (2012), except that multiple prey genotypes can be present. For the case of two prey genotypes, the model equations are as follows: ...
We explore the role of rapid evolution in the community dynamics of a three-species planktonic food web with intraguild predation. Previous studies of a two-species predator-prey system showed that rapid evolution of an anti-predator defence trait in the prey results in long-period antiphase predator-prey cycles (predator maximacoinciding with prey minima and vice versa) that are virtually diagnostic of eco-evolutionary dynamics. Here, we ask if there exist diagnostic population dynamics for a food web where algae are consumed by two predators (flagellates and rotifers), while rotifers also consume flagellates. With genetically homogeneous non-evolving prey, we previously predicted theoretically, and confirmed experimentally, that population cycles exhibit short-period oscillations with peaks in prey density followed by peaks in flagellates and then rotifers. In contrast, when prey defence can evolve, theory predicts a wide diversity of possible dynamics depending upon the trade-off between defences against the two predators. When defence against one predator implies vulnerability to the other, the predicted pattern is that predators "take turns": one predator peaks at each prey minimum, while the other remains rare because prey are defended against it. There is strong selection for prey to evolve defence against the abundant predator (losing defence against the rare one); once this happens, predator dominance reverses rapidly. This pattern is what we generally observed in seven separate microcosms (sampled daily for 130-330 days). Cycles in which predator abundances alternate between stasis and rapid change may be explained using the concept of canards from dynamical systems theory. Nevertheless, details differed among experimental runs, making patterns diagnostic of eco-evolutionary dynamics difficult to identify.
... We used a three-species, intraguild predation, marine planktonic food web as our study system. (Hiltunen et al., 2012). We eventually chose a marine system because salinity provided, along with temperature and chemostat dilution rate, an additional controllable parameter. ...
... Because the analysis was based on Taylor-series approximations for nearequilibrium dynamics, the qualitative predictions are robust to model details such predator functional responses. For numerical simulations in this paper, we used a model very similar to that in Hiltunen et al. (2012), except that multiple prey genotypes can be present. For the case of two prey genotypes, the model equations are as follows: ...
Consumer–resource interactions are fundamental components of ecological communities. Classic features of consumer–resource models are that temporal dynamics are often cyclic, with a ¼-period lag between resource and consumer population peaks. However, there are few published empirical examples of this pattern. Here, we show that many published examples of consumer–resource cycling show instead patterns indicating eco-evolutionary dynamics. When prey evolve along a trade-off between defence and competitive ability, two-species consumer–resource cycles become longer and antiphase (half-period lag, so consumer maxima coincide with minima of the resource species). Using stringent criteria, we identified 21 two-species consumer–resource time series, published between 1934 and 1997, suitable to investigate for eco-evolutionary dynamics. We developed a statistical method to probe for a transition from classic to eco-evolutionary cycles, and find evidence for eco-evolutionary type cycles in about half of the studies. We show that rapid prey evolution is the most likely explanation for the observed patterns.
... egg production, hatching success) and growth efficiency of zooplankton predators in conjunction with a single prey species in monoculture reared in conditions along the mixotrophic spectrum or varying proportions of phagotrophy and photoautotrophy ratios (Traboni et al., 2021). Given the potential for toxicity (Hiltunen et al., 2012;Tang et al., 2020) or inedibility (Vad et al., 2020) among mixoplankton, we also see a need for prey-preference assays (as in Castellani et al., 2008;Parrish et al., 2012), but focused on mixoplankton and their varying nutritional value as prey. Advances in flow cytometric sorting and imaging allow for discrimination between potential mixotrophic prey items in situ, which could allow for studies of prey selection in spectrometry) could be used to quantify carbon and nitrogen fluxes in mixoplankton. ...
Protist plankton can be divided into three main groups: phytoplankton, zooplankton, and mixoplankton. In situ methods for studying phytoplankton and zooplankton are relatively straightforward since they generally target chlorophyll/photosynthesis or grazing activity, while the integration of both processes within a single cell makes mixoplankton inherently challenging to study. As a result, we understand less about mixoplankton physiology and their role in food webs, biogeochemical cycling, and ecosystems compared to phytoplankton and zooplankton. In this paper, we posit that by merging conventional techniques, such as microscopy and physiological data, with innovative methods like in situ single-cell sorting and omics datasets, in conjunction with a diverse array of modeling approaches ranging from single-cell modeling to comprehensive Earth system models, we can propel mixoplankton research into the forefront of aquatic ecology. We present eight crucial research questions pertaining to mixoplankton and mixotrophy, and briefly outline a combination of existing methods and models that can be used to address each question. Our intent is to encourage more interdisciplinary research on mixoplankton, thereby expanding the scope of data acquisition and knowledge accumulation for this understudied yet critical component of aquatic ecosystems.
... mismatch of the preferred prey C:N:P ratio), copepod gross growth efficiency is lower (Mitra and Flynn, 2005;Bi and Sommer, 2020). Alternatively, toxicity has been documented in several mixoplankton flagellates (Boenigk and Stadler, 2004;Adolf et al., 2006;Hiltunen et al., 2012), which has implications for zooplankton prey quality, especially at times when mixoplankton are abundant. ...
Phago-mixotrophy, the combination of photoautotrophy and phagotrophy in mixoplankton, organisms that can combine both trophic strategies, have gained increasing attention over the past decade. It is now recognized that a substantial number of protistan plankton species engage in phago-mixotrophy to obtain nutrients for growth and reproduction under a range of environmental conditions. Unfortunately, our current understanding of mixoplankton in aquatic systems significantly lags behind our understanding of zooplankton and phytoplankton, limiting our ability to fully comprehend the role of mixoplankton (and phago-mixotrophy) in the plankton food web and biogeochemical cycling. Here, we put forward five research directions that we believe will lead to major advancement in the field: (i) evolution: understanding mixotrophy in the context of the evolutionary transition from phagotrophy to photoautotrophy; (ii) traits and trade-offs: identifying the key traits and trade-offs constraining mixotrophic metabolisms; (iii) biogeography: large-scale patterns of mixoplankton distribution; (iv) biogeochemistry and trophic transfer: understanding mixoplankton as conduits of nutrients and energy; and (v) in situ methods: improving the identification of in situ mixoplankton and their phago-mixotrophic activity.
... The interest in cyanobacteria is understandable, because they can produce toxic blooms which have negative impacts on water quality, and hence are highly relevant in lake management (Chorus and Bartram 1999, Meriluoto et al 2017, Huisman et al 2018. However, in addition to cyanobacteria, other freshwater phytoplankton taxa, such as chrysophytes (Hiltunen et al 2012) and euglenophytes (Zimba et al 2017), are also capable of toxin production. Moreover, other phytoplankton groups may play key roles in biogeochemical cycles, such as silica drawdown by diatoms (Smol and Stoermer 2010), or may have unexpected impacts on food web structure such as mixotrophic taxa capable of both photoautotrophic and heterotrophic growth (Flynn et al 2013, Hansson et al 2019. ...
Although environmental impacts on the biodiversity and species composition of lakes have been studied in great detail at local and regional scales, unraveling the big picture of how lake communities respond to environmental variation across large spatial scales has received less attention. We performed a comprehensive analysis to assess how the phytoplankton community composition varies among >1,000 lakes across the conterminous United States of America. Our results show that lake-to-lake similarity in species composition was low even at the local scale, and slightly decreased with geographical distance. Analysis of the compositional data by Dirichlet regression revealed that the geographical variation in phytoplankton community composition was best explained by total phosphorus, water temperature, pH, and lake size. High total phosphorus concentrations were associated with high relative abundances of cyanobacteria and euglenophytes at the expense of other phytoplankton groups. High lake temperatures stimulated cyanobacteria, dinoflagellates, desmids and euglenophytes, whereas cryptophytes, golden algae and diatoms were relatively more abundant in colder lakes. Low lake pH correlated with high dissolved CO 2 concentrations, which may explain why it benefitted phytoplankton groups with inefficient carbon concentrating mechanisms such as golden algae and euglenophytes. Conversely, the relative abundance of cyanobacteria showed a pronounced increase with lake pH. Large lakes showed higher relative abundances of cyanobacteria and diatoms, whereas small lakes showed higher relative abundances of chlorophytes, desmids, dinoflagellates and euglenophytes. Biodiversity increased with lake temperature, but decreased at high total phosphorus concentrations and pH. The key environmental variables identified by our study (high phosphorus loads, warm temperature, low pH) are associated with anthropogenic pressures such as eutrophication, global warming and rising atmospheric CO 2 concentration. Hence, our results provide a comprehensive illustration of the major impact of these anthropogenic pressures on the biodiversity and taxonomic composition of lake phytoplankton communities.
... In contrast to mineral and biochemical content, there seems to be no toxicity gradient along the bacteriaphytoplankton size range. Toxic constituents are known from bacteria (Matz et al., 2004), cyanobacteria (Wilson et al., 2006), as well as mixotrophic and heterotrophic flagellates (Hiltunen et al., 2012). ...
Aims: This chapter covers main and recent findings in the study of zooplankton nutritional constraints. We will present detailed laboratory studies on the physiological needs of zooplankton regarding food quantity and single elements or biochemicals. In addition, we aim to summarize the findings on the degree and type of nutritional constraints experienced by zooplankton in different seasons and lakes.
Main concepts covered: Nutritional constraints are studied via linking zooplankton growth to various concentrations of food of different quality via functional response curves. This work has quantified the role of food quantity limitation for zooplankton growth, as well as identified important food components constraining the quality of zooplankton food such as elements, long-chain poly-unsaturated fatty acids, sterols and amino acids. Further work has shown that zooplankton might be constrained by several food components simultaneously, and that water temperature strongly influences the strength of both quantity and quality constraints.
Main methods covered: We explore how controlled laboratory experiments aim at separating the roles of food quantity versus quality constraints in zooplankton, and compare the various approaches on identifying the strength and type of nutritional constraining zooplankton growth in situ. While correlative studies suggest limitation of zooplankton growth by the availability and quality of food, experimental supplementation of laboratory-cultured algae or of lake seston with specific dietary compounds provided strong evidence for both quantity and quality limitation of zooplankton growth.
Conclusions: Laboratory studies show that there is a strong potential for both food quantity and quality limitation of zooplankton as well as co-limitation by different quality compounds. Likewise, field studies suggest that limitation of zooplankton growth by both food quantity and food quality occurs frequently in lakes. However, the relative importance of food quantity versus food quality, and especially of the various food quality components has been difficult to identify in situ. Available studies suggest that during the spring season, zooplankton is strongly constrained by temperature and less by food quantity and quality, whereas during summer, zooplankton populations are constrained by both food quantity and quality.
... The demonstrated ability to significantly inhibit the growth of the Anabaena strain in a Microcystis cell-free medium further confirms this hypothesis. The release of secondary metabolites and biologically active substances into the growth medium by Microcystis likely inhibits the Anabaena strain, and it is consistent with observations of their impact on plankton [31,32,[36][37][38][39]. Activities such as catalase, peroxidase, or superoxide dismutase are likely to be enhanced by the increase in the production of oxidative stress species due to allelochemicals from Microcystis, thereby inhibiting the growth of Anabaena [32]. ...
In recent decades, harmful algal blooms (HABs) have been significantly affecting environments, aquatic ecosystems, and human health, as well as damaging economies, especially near rivers and lakes, and in coastal regions. Microcystis and Anabaena are two genera of harmful cyanobacteria that will often predominate during toxic microalgal blooms. In this study, we employ a method for control and mitigation of HABs by microalgal cell instability using different types of aminoclays (ACs). Allelopathic interactions between the two strains of algae are studied in mono-culture, co-culture, and filtrated cell-free medium in the presence of the ACs. The growth of the Anabaena strain is significantly reduced by the cyanobacterial strains in the co-culture media, and both are significantly affected by the Acs’-enhanced algicidal activity. Anabaena sp. KVSF7 shows higher sensitivity against the ACs than does Microcystis sp. KW. In this way, the algicidal activity of ACs is harnessed, the effects of which are in the order of aluminum aminoclay (AlAC) > magnesium aminoclay (MgAC) > calcium aminoclay (CaAC). The ammonium sites in the ACs carry positive charges to induce instability of HABs along with the electrostatic attraction between algal cells and AC. Therefore, the utilization of the algicidal activity of the ACs can effectively reduce HABs, especially on cyanobacterial blooms.
... Boxhorn et al. (1998) reported the quicker death of the rotifer Brachionus angularis by higher doses of P. malhamensis. Hiltunen et al. (2012) claimed that Ochromonas is toxic to the components of the food web with which it interacts, especially toxic to zooplankton that directly consume its cells. Nonetheless, based on the similar life history responses between starved and Poterioochromonas-fed individuals, Zhang et al. (2009Zhang et al. ( , 2011 studied that Poterioochromonas is neither acutely toxic nor a nutritious food for D. magna. ...
Mixotrophs account for a high proportion (occasionally up to 80%) of the phytoplankton biomass. Chrysophyte is one major component of mixotrophs. Because of their possible toxicity and linkage between microbial community and higher trophic levels, the effect of mixotrophic golden algae on potential grazers received much attention. The present study investigated the effect of Ochromonas gloeopara at different proportions in diet (combined with Scenedesmus obliquus) on the life history of Daphnia similoides sinensis. Results showed that osmotrophically grown O. gloeopara in light produced fish toxins and hemolysins, and negatively influenced the survival and reproduction of D. similoides sinensis. The mortality of the cladoceran increased as the proportion of O. gloeopara in food increased. The D. similoides sinensis could not reproduce throughout the life when Ochromonas comprised above 35%. When fed foods containing 15% of Ochromonas, the time to first brood of D. similoides sinensis was prolonged, together with the reduced number of offspring in first brood and total number of broods. Replacement by 100% S. obliquus delayed the time to death, but did not improve the reproduction of Daphnia. The present study indicated the strong inhibitory effect of O. gloeopara on D. similoides sinensis, and underlined the importance of evaluating its ecological role in aquatic ecosystems.
... The same holds also for some species of aquatic snails eaten by mallards ). Such digestion resistance may promote coexistence and stabilize the dynamics even more than post-attack defended prey (see Appendix A.1). Furthermore, toxicity of a prey may differ in the consequences on prey coexistence from the defence mechanisms considered here, especially when it interferes not only with the predator but also with the competitor (Hiltunen et al. 2012). However, for a large variety of defence strategies, e.g., aposematism, weaponry or mimicry, the used classification regarding the phase at which the defence interrupts the predation sequence is adequate. ...
Predation drives coexistence, evolution and population dynamics of species in food webs, and has strong impacts on related ecosystem functions (e.g. primary production). The effect of predation on these processes largely depends on the trade-offs between functional traits in the predator and prey community. Trade-offs between defence against predation and competitive ability, for example, allow for prey speciation and predator-mediated coexistence of prey species with different strategies (defended or competitive), which may stabilize the overall food web dynamics. While the importance of such trade-offs for coexistence is widely known, we lack an understanding and the empirical evidence of how the variety of differently shaped trade-offs at multiple trophic levels affect biodiversity, trait adaptation and biomass dynamics in food webs. Such mechanistic understanding is crucial for predictions and management decisions that aim to maintain biodiversity and the capability of communities to adapt to environmental change ensuring their persistence. In this dissertation, after a general introduction to predator-prey interactions and tradeoffs, I first focus on trade-offs in the prey between qualitatively different types of defence (e.g. camouflage or escape behaviour) and their costs. I show that these different types lead to different patterns of predator-mediated coexistence and population dynamics, by using a simple predator-prey model. In a second step, I elaborate quantitative aspects of trade-offs and demonstrates that the shape of the trade-off curve in combination with trait-fitness relationships strongly affects competition among different prey types: Either specialized species with extreme trait combinations (undefended or completely defended) coexist, or a species with an intermediate defence level dominates. The developed theory on trade-off shapes and coexistence is kept general, allowing for applications apart from defence-competitiveness trade-offs. Thirdly, I tested the theory on trade-off shapes on a long-term field data set of phytoplankton from Lake Constance. The measured concave trade-off between defence and growth governs seasonal trait changes of phytoplankton in response to an altering grazing pressure by zooplankton, and affects the maintenance of trait variation in the community. In a fourth step, I analyse the interplay of different tradeoffs at multiple trophic levels with plankton data of Lake Constance and a corresponding tritrophic food web model. The results show that the trait and biomass dynamics of the different three trophic levels are interrelated in a trophic biomass-trait cascade, leading to unintuitive patterns of trait changes that are reversed in comparison to predictions from bitrophic systems. Finally, in the general discussion, I extract main ideas on trade-offs in multitrophic systems, develop a graphical theory on trade-off-based coexistence, discuss the interplay of intra- and interspecific trade-offs, and end with a management-oriented view on the results of the dissertation, describing how food webs may respond to future global changes, given their trade-offs.
... Potential reasons why Nodularia alone cannot sustain rotifer growth include toxicity, mechanical interference, and the low nutritional value of cyanobacteria (Porter andOrcutt 1980, Gulati andDeMott 1997). Furthermore, the ratio between low quality or toxic food and high quality food can be important in determining grazer growth (Hiltunen et al. 2012). In line with this, higher Chlorella biomasses supported higher rotifer biomasses in cultures with 0% and 5% of the phage-resistant Nodularia genotype in both medium conditions. ...
Parasites, such as bacterial viruses (phages), can have large effects on host populations both at the ecological and evolutionary levels. In the case of cyanobacteria, phages can reduce primary production and infected hosts release intracellular nutrients influencing planktonic food web structure, community dynamics, and biogeochemical cycles. Cyanophages may be of great importance in aquatic food webs during large cyanobacterial blooms unless the host population becomes resistant to phage infection. The consequences on plankton community dynamics of the evolution of phage resistance in bloom forming cyanobacterial populations are still poorly studied. Here, we examined the effect of different frequencies of a phage‐resistant genotype within a filamentous nitrogen‐fixing Nodularia spumigena population on an experimental plankton community. Three Nodularia populations with different initial frequencies (0%, 5%, and 50%) of phage‐resistant genotypes were inoculated in separate treatments with the phage 2AV2, the green alga Chlorella vulgaris, and the rotifer Brachionus plicatilis, which formed the experimental plankton community subjected to either nitrogen‐limited or nitrogen‐rich conditions. We found that the frequency of the phage‐resistant Nodularia genotype determined experimental community dynamics. Cyanobacterial populations with a high frequency (50%) of the phage‐resistant genotype dominated the cultures despite the presence of phages, retaining most of the intracellular nitrogen in the plankton community. In contrast, populations with low frequencies (0% and 5%) of the phage‐resistant genotype were lysed and reduced to extinction by the phage, transferring the intracellular nitrogen held by Nodularia to Chlorella and rotifers, and allowing Chlorella to dominate the communities and rotifers to survive. This study shows that even though phages represent minuscule biomass, they can have key effects on community composition and eco‐evolutionary feedbacks in plankton communities.
... Such digestion resistance may promote coexistence and stabilize the dynamics even more than post-attack defended prey (see Appendix S1). Furthermore, toxicity of a prey may differ in the consequences on prey coexistence from the defense mechanisms considered here, especially when it interferes not only with the predator but also with the competitor (Hiltunen, Barreiro, & Hairston, 2012). However, for a large variety of defense strategies, for example, aposematism, weaponry or mimicry, the used classification regarding the phase at which the defense interrupts the predation sequence is adequate. ...
It is well‐known that prey species often face trade‐offs between defense against predation and competitiveness, enabling predator‐mediated coexistence. However, we lack an understanding of how the large variety of different defense traits with different competition costs affects coexistence and population dynamics. Our study focusses on two general defense mechanisms, that is, pre‐attack (e.g., camouflage) and post‐attack defenses (e.g., weaponry) that act at different phases of the predator—prey interaction. We consider a food web model with one predator, two prey types and one resource. One prey type is undefended, while the other one is pre‐ or post‐attack defended paying costs either by a higher half‐saturation constant for resource uptake or a lower maximum growth rate. We show that post‐attack defenses promote prey coexistence and stabilize the population dynamics more strongly than pre‐attack defenses by interfering with the predator's functional response: Because the predator spends time handling “noncrackable” prey, the undefended prey is indirectly facilitated. A high half‐saturation constant as defense costs promotes coexistence more and stabilizes the dynamics less than a low maximum growth rate. The former imposes high costs at low resource concentrations but allows for temporally high growth rates at predator‐induced resource peaks preventing the extinction of the defended prey. We evaluate the effects of the different defense mechanisms and costs on coexistence under different enrichment levels in order to vary the importance of bottom‐up and top‐down control of the prey community.
... Values are mean plus or minus standard deviation for n = 3, and those with asterisks are significantly different from the control. (Johnson et al., 2009;Hiltunen et al., 2012;Barreiro and Hairston, 2013b). Nutrient limitation strongly influenced allelopathic interactions between Microcystis and Anabaena. ...
Microcystis and Anabaena (Dolichospermum) are among the most toxic cyanobacterial genera and often succeed each other during harmful algal blooms. The role allelopathy plays in the succession of these genera is not fully understood. The allelopathic interactions of six strains of Microcystis and Anabaena under different nutrient conditions in co-culture and in culture-filtrate experiments were investigated. Microcystis strains significantly reduced the growth of Anabaena strains in mixed cultures with direct cell-to-cell contact and high nutrient levels. Cell-free filtrate from Microcystis cultures proved equally potent in suppressing the growth of nutrient replete Anabaena cultures while also significantly reducing anatoxin-a production. Allelopathic interactions between Microcystis and Anabaena were, however, partly dependent on ambient nutrient levels. Anabaena dominated under low N conditions and Microcystis dominated under nutrient replete and low P during which allelochemicals caused the complete suppression of nitrogen fixation by Anabaena and stimulated glutathione S-transferase activity. The microcystin content of Microcystis was lowered with decreasing N and the presence of Anabaena decreased it further under low P and high nutrient conditions. Collectively, these results indicate that strong allelopathic interactions between Microcystis and Anabaena are closely intertwined with the availability of nutrients and that allelopathy may contribute to the succession, nitrogen availability, and toxicity of cyanobacterial blooms.
... The chrysomonads themselves are on the menu of several larger metazoan grazers, mesozooplankton (Saunders et al. 1994). They can be toxic to mesozooplankton (Boxhorn et al. 1998; Leeper and Porter 1995; Hiltunen et al. 2012), but it is assumed that at normal field abundances of these organisms toxic effects will be hardly detectable (Boenigk and Stadler 2004). Grazing by chrysomonads on Microcystis can also reduce the toxicity of Microcystis to Daphnia (Zhang et al. 2009b). ...
While reduction in nutrient loading is a prerequisite for mitigation of harmful cyanobacterial blooms in nutrient-enriched waters, in certain surface waters eutrophication control is not always feasible due to practical and economic constraints or might be effective only in the long run. Yet, the urgent need to control cyanobacteria in water for drinking, irrigation, aquaculture, industry and recreation has spurred the development of a plethora of alternative methods that claim to be fast acting. Here, we provide a critical overview of several of these end-of-pipe measures: effective microorganisms (EM®), golden algae (Ochromonas), plant/tree extracts, ultrasound and artificial mixing of non-stratifying waters. Most of the end-of the pipe measures claim to provide sustainable control of harmful cyanobacterial blooms, while at best only targeting symptom relief rather than eutrophication relief. Support for “effective” microorganisms, golden algae, plant extracts, ultrasound and artificial mixing of non-stratifying waters to diminish eutrophication problems such that the resulting water quality meets societal and legislation demands is limited, and several proposed underlying mechanisms are doubtful. None of these curative measures seem the desired wide applicable solution to cyanobacterial nuisance; they should not be considered Columbus’s egg. A critical evaluation of end-of pipe measures is crucial for water authorities in their choice for mitigating measures.
... A number of chrysophytes are reported to be mixotrophic where particle phagocytosis is thought to supply nutrients for growth (Wilken et al. 2014). Similar to our CCMP2298, the chrysophyte Ochromonas malhamensis grew with urea as a nitrogen source (Pringsheim 1952, Hiltunen et al. 2012) but much slower when compared to growth with added ammonium (Lui and Roels 1970). The media used in these earlier studies was filter sterilized and some bacteria may have passed through the 0.45 µm filter. ...
In an effort to better understand the diversity of genes coding for nitrogen (N) uptake and assimilation pathways among microalgae, we analyzed the transcriptomes of five phylogenetically diverse single celled algae originally isolated from the same high arctic marine region. The five photosynthetic flagellates; a pelagophyte, dictyochophyte, chrysophyte, cryptophyte and haptophyte were grown on standard media and media with only urea or nitrate as a nitrogen source, cells were harvested during late exponential growth. Based on homolog protein sequences, transcriptomes of each alga were interrogated to retrieve genes potentially associated with nitrogen uptake and utilization pathways. We further investigated the phylogeny of poorly characterized genes and gene families that were identified. While the phylogeny of the active urea transporter (DUR3) was taxonomically coherent, those for the urea transporter (UT) superfamily, putative nitrilases and amidases indicated complex evolutionary histories and preliminary evidence for horizontal gene transfers. All five algae expressed genes for ammonium assimilation and all but the chrysophyte expressed genes involved in nitrate utilization and the urea cycle. Among the four algae with nitrate transporter (NRT2) transcripts, we detected lower expression levels in three of these (the dictyochophyte, pelagophyte and cryptophyte) grown in the urea only medium compared to cultures from the nitrate only media. The diversity of N pathway genes in the five algae and their ability to grow using urea as a nitrogen source suggest these flagellates are able to use variety organic nitrogen sources, which would be an advantage in an inorganic nitrogen limited environment such as the Arctic Ocean.This article is protected by copyright. All rights reserved.
... In our study, Gymnodinium and Strombidium were only abundant in the melt-pond aggregate, while sea ice was strongly dominated by the mixotroph Ochromonas sp. (Andersson et al. 1989;Hiltunen et al. 2012). These observations show that mixotrophic taxa not only constitute important contributors during the polar night but can also be dominant under the midnight sun or sea ice. ...
Protists in the central Arctic Ocean are adapted to the harsh environmental conditions of its various habitats. During the Polarstern cruise ARK-XXVI/3 in 2011, at one sea-ice station, large aggregates accumulated at the bottom of the melt ponds. In this study, the protist assemblages of the bottom layer of the sea-ice and melt-pond aggregate were investigated using flow cytometry and 454-pyrosequencing. The objective is to provide a first molecular overview of protist biodiversity in these habitats and to consider the overlaps and/or differences in the community compositions. Results of flow cytometry pointed to a cell size distribution that was dominated by 3-10 µm nanoflagellates. The phylogenetic classification of all sequences was conducted at a high taxonomic level, while a selection of abundant (≥1% of total reads) sequences was further classified at a lower level. At a high taxonomic level, both habitats showed very similar community structures, dominated by chrysophytes and chlorophytes. At a lower taxonomic level, dissimilarities in the diversity of both groups were encountered in the abundant biosphere. While sea-ice
chlorophytes and chrysophytes were dominated by Chlamydomonas/Chloromonas spp. and Ochromonas spp., the melt-pond aggregate was dominated by Carteria sp., Ochromonas spp. and Dinobryon faculiferum. We suppose that the similarities in richness and community structure are a consequence of melt-pond freshwater seeping through porous sea ice in late summer. Differences in the abundant biosphere nevertheless indicate that environmental conditions in both habitats vary enough to select for different dominant species.
... Similar approaches could be applied to aquatic invertebrates because these organisms have already shown great variation in their physiological responses to certain toxic compounds. Those organisms have already shown great variation in their physiological responses to some toxic compounds (Hiltunen et al. 2012). ...
A series of experiments was undertaken on three different marine microalgae to compare the effect of two metal oxide nanoparticles (NPs) on different physiological responses to stress: zinc oxide (ZnO), a known toxic compound for microalgae, and the never before tested yttrium oxide (Y2O3). The effect of these potential pollutants was estimated for different physiological variables and temporal scales: Growth, carbon content, carbon-to-nitrogen (C:N) ratio, and chlorophyll fluorescence were evaluated in long-term assays, and reactive oxygen species (ROS) production was evaluated in a short-term assay. Population growth was the most susceptible variable to the acute toxic effects of both NPs as measured in terms of number of cells and of biomass. Although Phaeodactylum tricornutum and Alexandrium minutum were negatively affected by ZnO NPs, this effect was not detected in Tetraselmis suecica, in which cell growth was significantly decreased by Y2O3 NPs. Biomass per cell was negatively affected in the most toxic treatments in T. suecica but was positively affected in A. minutum. ZnO treatments induced a sharper decrease in chlorophyll fluorescence and higher ROS than did Y2O3 treatments. The pronounced differences observed in the responses between the species and the physiological variables tested highlight the importance of analyzing diverse groups of microalgae and various physiological levels to determine the potential effects of environmental pollutants.
... Filamentous species of benthic cyanobacteria would also be good candidates as allelopathic species, because of the relatively low turbulence of their habitat and the motility of filaments. Among these filamentous or motile species that dominate phytoplankton during low-turbulence periods, we can find many examples of genus with known allelopathic species, such as cyanobacteria: Anabaena, Nodularia, Aphanizomenon, Cylindrospermopsis, Oscillatoria, Microcystis (LeBlanc et al. 2005); small flagellates: Prymnesium, Chrysochromulina, Ochromonas (Hiltunen et al. 2012), Chlamydomonas; dinoflagellates: Alexandrium, Karenia, Heterosigma, Pfiesteria, Prorocentrum (Xiaoqing et al. 2011). On the other hand, among those species that dominate phytoplankton communities during periods of strong mixing (mainly diatoms), we almost do not find examples of known allelopathic species (but see Ribalet et al. 2007;Yamasaki et al. 2010). ...
We chose four species of freshwater phytoplankton: the chlorophyceans Ankistrodesmus falcatus, Chlamydomonas reinhardtii and Selenastrum capricornutum, and the cyanobacteria Oscillatoria sp. in order to study their competitive abilities for nitrate and their allelopathic properties. We parameterized models of nitrate uptake and growth with laboratory experiments. According to them, the species were ranked (from the best to the worst competitors): S. capricornutum, C. reinhardtii, A. falcatus and Oscillatoria sp. C. reinhardtii and Oscillatoria sp. were previously reported as allelopathic. In the present work, Oscillatoria sp. was allelopathic only against A. falcatus. However, none of our species was sensitive to C. reinhardtii. Additionally, we found an unknown allelopathic effect of A. falcatus against Oscillatoria sp. Our findings point out the high specificity of allelopathic interactions. With these data, we constructed a model of interspecific competition for nitrate, including allelopathic interactions. By performing model simulations, we studied how three factors influence the outcome of competition: relative abundance of competing species, resistance to allelopathy, and nitrate concentration. Our simulations showed that the initial ratio of species abundances will significantly determine the outcome of competition. If the worst competitor was the allelopathic species, the more it needs to outnumber the competing species, unless it is very sensitive to allelopathy (not defended). Nitrate has an important influence, showing a non-intuitive outcome of competition experiments at low nitrate concentrations, where the worst competitor (allelopathic species) wins competition in the majority of cases, whereas at intermediate concentrations, the better competitor dominates except for unfavorable ratios of abundances. With the increased amounts of nitrate, conditions again favor the worst competitor (the stronger allelopathic species). Despite the potential for two species coexistence showed by previous theoretical analysis of systems was similar to ours, our simulations did not detect this outcome. We hypothesized that this is due to the strong allelopathic effect of Oscillatoria sp.
... Ochromonas, also a naked flagellate, is an obligate osmotroph (Pringsheim, 1952), and presumably able to use organic allelochemicals as a resource. In addition, because Ochromonas produces its own toxic allelochemicals (Hiltunen et al., 2012), it may simply be resistant to those produced by other phytoplankton. ...
Because we found previously that Chlamydomonas reinhardtii produces allelochemicals to which the rotifer Brachionus calyciflorus is sensitive, we explored its effects on other freshwater plankton. We used Chlamydomonas under light-, nitrogen- and phosphorus-limitation to test its allelopathic effect on Microcystis aeruginosa, Cryptomonas ozolinii, Ochromonas danica, Tetrahymena thermophila and Paramecium aurelia. Allelopathy depended strongly on the target organism. Only Cryptomonas suffered a marked negative effect. Among the resource limiting regimes, light limitation exerted the greatest effect.
Production of phytoplankton (microalgae and cyanobacteria) in commercial raceway ponds and other systems is adversely impacted by phytoplankton pathogens, including bacteria, fungi and viruses. In addition, cultures are susceptible to productivity loss, or crash, through grazing by contaminating zooplankton such as protozoa, rotifers and copepods. Productivity loss and product contamination are also caused by otherwise innocuous invading phytoplankton that consume resources in competition with the species being cultured. This review is focused on phytoplankton competitors, pathogens and grazers of significance in commercial culture of microalgae and cyanobacteria. Detection and identification of these biological contaminants are discussed. Operational protocols for minimizing contamination, and methods of managing it, are discussed.
Current high costs of commercial-scale algal biofuel production prevent the widespread use of this renewable fuel source. One cost-saving approach is the reuse of algae cultivation water after biomass harvesting, which reduces water pumping and treatment costs. However, dissolved compounds, cell debris, and microorganisms remaining in the water could affect subsequent algae generations. Previous studies demonstrate a variety of effects of recycled medium on algae growth, yet their results have not been collectively analyzed. Here we integrate data across 86 studies to determine the relative importance of different factors influencing algae growth in recycled medium. We found that algae taxa can have the greatest influence, while the harvesting method is less influential on growth outcomes. This meta-analysis identifies favorable taxa and thus provides a tool for algae cultivation decision-making when medium reuse is an important driver. Results can also aid in estimating relative algae yield and growth rates for technoeconomic assessments that incorporate water recycling.
Chemically mediated interactions between microalgae and between microalgae and other organisms, are widespread in nature. They are important in structuring algal communities, bloom formation, algal development, and they affect the productivity of algae. In recent years understanding of these types of interactions has greatly improved, but in many cases the exact mechanisms are still little understood, and the actual bioactive compounds are not known. Many instances of allelopathic interactions have been recorded, including the presence of autoinhibitors in some algae. Some of the allelopathic compounds identified include free fatty acids (e.g. in green algae), polyunsaturated aldehydes (in diatoms) and the alkaloid cylindrospermopsin (in cyanobacteria). Other chemically-mediated interactions include pheromones and hormones which affect algal reproduction and development. Finally, there is some evidence for microalgae affecting bacterial quorum sensing, and for quorum sensing in cyanobacteria.
The nature of the growth-rate response of grazing zooplankton to algal concentration depends critically upon food quality, which is often a plastic function of environmental conditions. Phytoplankton quality depends upon nutrient and light availability, which together affect cell C : P and C : N, so that the links from external environment to phytoplankton and then to zooplankton can vary in ways that influence consumer-resource interaction strengths, and ultimately, food web structure. We measured the effects of resource-limitation on the population growth rate of rotifers, Brachionus calyciflorus, feeding on the alga Chlamydomonas reinhardtii, and grown in nitrogen-limiting, phosphorus-limiting, or nutrient-sufficient conditions. Consumption of nutrient-sufficient algae produced a Type II numerical response with a low half saturation constant (K-s) and high asymptotic growth rate (lambda(max)) consistent with high food quality; P-limited algae also yielded a Type II response but with high K-s and low lambda(max), meaning poor food quality. In contrast, N-limited Chlamydomonas resulted in a novel Type IV numerical response in which rotifer growth rate rose to an intermediate lambda(max) and then declined at the highest algal densities, suggesting the production of toxic compounds whose negative effect on growth increases as a function of cell density. Experiments with mixed diets confirmed that N-limited food was indeed toxic, whereas P-limited food was simply nutritionally deficient compared with light-limited algae. Additional experiments showed that even the filtrate of N-limited algae can be detrimental to rotifer growth.
Research activity involving algae in the classes Chrysophyceae and Synurophyceae ('chrysophytes') has increased dramatically over the last decade. These beautiful and delicate organisms are pivotal for studies of protistan evolution, food web dynamics in oligotrophic freshwater ecosystems, and for the assessment of environmental degradation resulting from eutrophication and acid rain. They also represent excellent model cellular systems for studying processes inherent in basic metabolism, biomineralization, endo- and exo-cytosis and macro-assembly of cell surface layers. This book gives a broad overview of current research, emphasizing the phylogeny, ecology and development of these organisms. Each chapter also contains reviews of the literature, and presents ideas for future research. Phycologists, palaeoecologists, limnologists and plankton ecologists will find this a mine of invaluable information.
Mixotrophic flagellates can compete with obligately heterotrophic flagellates for the uptake of food particles, whereas mixotrophs and obligately phototrophic phytoplankton can compete for soluble nutrients. Competition for soluble nutrients is expected when photosynthesis covers a significant portion of the mixotrophs' carbon metabolism. When heterotrophy predominates, however, mixotrophs may release soluble nutrients and facilitate phototrophs. Mechanistic resource competition theory predicts that, due to their ability to utilize substitutable C and P sources, mixotrophs should be able to coexist with their more specialized competitors under certain conditions of resource supply. In laboratory experiments, the mixotrophic flagellate Ochromonas excluded heterotrophic flagellates when only phototrophic growth was possible. However, Ochromonas was excluded by heterotrophic flagellates when only phagotrophic growth was possible. Both coexisted when food bacteria and light were supplied simultaneously. Ochromonas coexisted with a P-limited phytoplankter, Cryptomonas sp., when soluble reactive phosphorus (SRP) and bacterial phosphorus were available as alternative P sources. In nature, the mixotrophic strategy may be successful when resources are limiting. This is supported by published data on the occurrence of mixotrophic chrysophytes.
Predation was a powerful selective force promoting increased morphological complexity in a unicellular prey held in constant environmental conditions. The green alga, Chlorella vulgaris, is a well-studied eukaryote, which has retained its normal unicellular form in cultures in our laboratories for thousands of generations. For the experiments reported here, steady-state unicellular C. vulgaris continuous cultures were inoculated with the predator Ochromonas vallescia, a phagotrophic flagellated protist (`flagellate'). Within less than 100 generations of the prey, a multicellular Chlorella growth form became dominant in the culture (subsequently repeated in other cultures). The prey Chlorella first formed globose clusters of tens to hundreds of cells. After about 10–20 generations in the presence of the phagotroph, eight-celled colonies predominated. These colonies retained the eight-celled form indefinitely in continuous culture and when plated onto agar. These self-replicating, stable colonies were virtually immune to predation by the flagellate, but small enough that each Chlorella cell was exposed directly to the nutrient medium.
During spring (May-June) 1988 an extensive subsurface bloom of the haptophycean flagellate Chrysochromulina polylepis developed in Scandinavian waters (the KattegatSkagerrak area). Here we report on the vertical distribution of bacteria, heterotrophic flagellates, ciliates and copepods at a permanent station in the Southern Kattegat during the bloom. At the height of the bloom, the density of C. polylepis reached 60 to 70 X 10' cells 1-' in the pycnocline. At this time no potential grazers were present in the subsurface bloom and bacterial production was extremely low. Field and laboratory experiments showed that C. polylepis inhibited the activity of planktonic bacteria, ciliates and copepods. During the decay of the bloom, algae were colonized by bacteria and the pycnocline was subsequently re-lnvaded by heterotrophic flagellates, small aloricate ciliates and copepods. Two weeks after the height of the bloom, the normal pelagic food web structure was re-established.
It is considered self-evident that chemical interactions are a component of competition in terrestrial systems, but they are largely unknown in aquatic systems. In this review, we propose that chemical interactions, specifically allelopathy, are an important part of phytoplankton competition. Allelopathy, as defined here, applies only to the inhibitory effects of secondary metabolites produced by one species on the growth or physiological function of another phytoplankton species. A number of approaches are used to study allelopathy, but there is no standard methodology available. One of the methods used is cross-culturing, in which the cell-free filtrate of a donor alga is added to the medium of the target species. Another is to study the effect of cell extracts of unknown constituents, isolated exudates or purified allelochemicals on the growth of other algal species. There is a clear lack of controlled field experiments because few allelochemicals have been identified. Molecular methods will be important in future to study the expression and regulation of allelochemicals. Most of the identified allelochemicals have been described for cyanobacteria but some known toxins of marine dinoflagellates and freshwater cyanobacteria also have an allelochemical effect. The mode of action of allelochemicals spans a wide range. The most common effect is to cause cell lysis, blistering, or growth inhibition. The factors that affect allelochemical production have not been studied much, although nutrient limitation, pH, and temperature appear to have an effect. The evolutionary aspects of allelopathy remain largely unknown, but we hypothesize that the producers of allelochemicals should gain a competitive advantage over other phytoplankton. Finally, we discuss the possibility of using allelochemicals to combat harmful algal blooms (HABs). Allelopathic agents are used for biological control in agriculture, e.g. green manures to control soil diseases in Australia, but they have not yet been applied in the context of HABs. We suggest that phytoplankton allelochemicals have the potential for management of HABs in localized areas.
The toxicity of the chrysophyte flagellate Poterioochromonas malhamensis to the rotifer Brachionus angularis was investigated. Fed rotifers exposed to the flagellate experienced a mortality rate indistinguishable from starvation. Unfed rotifers exposed to the flagellate experienced a higher mortality rate. The mortality rate appears to depend on the flagellate concentration. Higher doses of flagellates resulted in quicker rotifer death. These laboratory results are consistent with the hypothesis that the occurrence of B. angularis in the field may be negatively related to the presence of P. malhamensis and related flagellates.
The aim of this study was to determine the relative importance of the different processes/mechanisms by which the toxic haptophyte Prymnesium parvum, cultured under different nutrient conditions, affects non-toxic phytoplankton competitors and microzooplankton grazers. P. parvum was cultured under steady-state growth in different nutrient conditions: nitrogen depleted (-N), phosphorus depleted (-P) and balanced nitrogen and phosphorus (+NP). Cells from each nutrient condition and culture cell-free filtrates, alone and combined with non-toxic prey (Rhodomonas salina), were used as food for the rotifer Brachionus plicatilis. An additional experiment was carried out to test the effect of P. parvum cells and culture cell-free filtrate on R. salina. The highest haemolytic activity values were achieved by -P F parvum cultures, followed by -N. However, the negative effect of R parvum on R. salina and rotifers did not correlate with haemolytic activity but with the number of P. parvum cells. -N-cultured P. parvum were the most toxic for both R. salina and rotifers, followed by +NP. Therefore, haemolytic activity is not a good indicator of the total potential toxicity of R parvum. The growth rate of R. salina was negatively affected by cell-free filtrates but the effect of P, parvum predation was greater. Rotifers fed on both toxic and non-toxic algae, indicating that they did not select against the toxic alga. The P. parvum cell-free filtrate had an effect on B. plicatilis, although this was weak, B, plicatilis was also indirectly affected by P. parvum due to the negative effects of the toxic alga on their prey (R. salina). However, the greatest negative effect of P. parvum on the rotifers was due to ingestion of the toxic cells. Therefore, the phytoplankton competitor R. salina is more affected by P. parvum predation and the grazer B. plicatilis is more affected by ingestion of the toxic cells, the effects of excreted compounds being secondary.
Recently developed techniques for estimating bacterial biomass and productivity indicate that bacterial biomass in the sea is related to phytoplankton concentration and that bacteria utilise 10 to 50 % of carbon fixed by photosynthesis. Evidence is presented to suggest that numbers of free bacteria are controlled by nanoplankton~c heterotrophic flagellates which are ubiquitous in the marine water column. The flagellates in turn are preyed upon by microzooplankton. Heterotrophic flagellates and microzooplankton cover the same size range as the phytoplankton, thus providing the means for returning some energy from the 'microbial loop' to the conventional planktonic food chain.
Managing nitrogen and phosphorus pollution of fresh water may decrease the risk of cyanobacterial blooms, even in the face of warming temperatures.
Ecology Letters (2010) 13: 989–997
Abstract
Adaptive variation in the traits determining ecological interactions can lead to evolution so rapid that ecological dynamics change course while in progress (i.e., ‘eco‐evolutionary dynamics’). However, little is known about how the qualitative properties of eco‐evolutionary dynamics (e.g., cycling, equilibrium, etc.) are affected by the amount of heritable variation present. Here, we show that a change in the range of variation in a heritable prey defense trait determines what dynamics are observed in an experimental predator–prey system. We combine modelling and laboratory experiments to show that initial defense trait variation determines whether populations exhibit eco‐evolutionary cycles in which heritable variation is maintained, or converge to an equilibrium at which the prey population becomes monomorphic. Our results show how small changes in the amount of adaptive genetic variance initially present can radically alter eco‐evolutionary dynamics, and can ultimately determine whether heritable variation is maintained or lost.
Background:
The loss of photosynthesis has occurred often in eukaryotic evolution, even more than its acquisition, which occurred at least nine times independently and which generated the evolution of the supergroups Archaeplastida, Rhizaria, Chromalveolata and Excavata. This secondary loss of autotrophic capability is essential to explain the evolution of eukaryotes and the high diversity of protists, which has been severely underestimated until recently. However, the ecological and evolutionary scenarios behind this evolutionary "step back" are still largely unknown.
Methodology/principal findings:
Using a dynamic model of heterotrophic and mixotrophic flagellates and two types of prey, large bacteria and ultramicrobacteria, we examine the influence of DOC concentration, mixotroph's photosynthetic growth rate, and external limitations of photosynthesis on the coexistence of both types of flagellates. Our key premises are: large bacteria grow faster than small ones at high DOC concentrations, and vice versa; and heterotrophic flagellates are more efficient than the mixotrophs grazing small bacteria (both empirically supported). We show that differential efficiency in bacteria grazing, which strongly depends on cell size, is a key factor to explain the loss of photosynthesis in mixotrophs (which combine photosynthesis and bacterivory) leading to purely heterotrophic lineages. Further, we show in what conditions an heterotroph mutant can coexist, or even out-compete, its mixotrophic ancestor, suggesting that bacterivory and cell size reduction may have been major triggers for the diversification of eukaryotes.
Conclusions/significance:
Our results suggest that, provided the mixotroph's photosynthetic advantage is not too large, the (small) heterotroph will also dominate in nutrient-poor environments and will readily invade a community of mixotrophs and bacteria, due to its higher efficiency exploiting the ultramicrobacteria. As carbon-limited conditions were presumably widespread throughout Earth history, such a scenario may explain the numerous transitions from phototrophy to mixotrophy and further to heterotrophy within virtually all major algal lineages. We challenge prevailing concepts that affiliated the evolution of phagotrophy with eutrophic or strongly light-limited environments only.
The intracellular distribution and level of acid hydrolases in Ochromonas malhamensis were studied in cells grown osmotrophically in a defined medium, in a carbon-free starvation medium, and during phagotrophy in each of these media. By cytochemical techniques, little enzymic reaction product was observed in the vacuoles of osmotrophic cells grown in the defined medium. Starved cells, however, contained autophagic vacuoles and cannibalized other Ochromonas cells. Dense enzymic reaction product was observed in the digestive vacuoles and in the Golgi cisternae of these starved cells. Moreover, starved cells and cells grown in a nutritionally complete medium ingested Escherichia coli which appeared in digestive vacuoles containing enzymic reaction product. Biochemical assays for lysosomal acid phosphatase (E.C. 3.1.3.2 orthophosphoric monoester phosphohydrolase) and acid ribonuclease (E.C. 2.7.7.16 ribonucleate nucleotido-2'-transferase) were done on Ochromonas cultures in the same experimental treatments and under identical assay conditions as the cytochemical study. During starvation, the acid hydrolase specific activities were consistently twice those found in cells grown in an osmotrophic complete medium. Ochromonas fed E. coli showed no increase in acid hydrolase specific activity as compared to controls not fed E. coli. The latency of lysosomal acid hydrolases in cells fixed with glutaraldehyde was reduced, suggesting that this fixative increases lysosomal membrane permeability and may release enzymes or their reaction products into the cytoplasmic matrix during cytochemical analysis. This could explain the cytoplasmic staining artifact sometimes observed with glutaraldehyde-fixed cells when studied by the Gomori technique. This study confirms that Ochromonas malhamensis, a phytoflagellate, does produce digestive vacuoles and can ingest bacteria, thereby fulfilling its role as a heterotroph in an aquatic food chain. When Ochromonas is grown in a nutritionally complete osmotrophic medium, phagocytosis causes appearance of acid hydrolases in the digestive vacuoles, whereas the total activity of the enzymes remains unchanged. An organic carbon-free medium strongly stimulates acid hydrolaes activity and causes these enzymes to appear in the digestive vacuoles whether phagocytosis occurs or not.
Mixotrophic organisms combine light, mineral nutrients, and prey as supplementary resources. Based on theoretical assumptions and field observations, we tested experimentally the hypothesis that mixotrophs may invade established plankton communities depending on the trophic status of the system, and investigated possible effects on food web structure, species diversity, and nutrient dynamics. To test our hypothesis, we inoculated the mixotrophic nanoflagellate Ochromonas tuberculata into established planktonic food webs, consisting of specialist phototrophs, specialist phagotrophs, and bacteria at different supplies of soluble inorganic nutrients and dissolved organic carbon. Oligotrophic systems facilitated the invasion of O. tuberculata in two different ways. First, the combination of photosynthesis and phagotrophy gave mixotrophs a competitive advantage over specialist phototrophs and specialist phagotrophs. Second, low nutrient supplies supported the growth of small plankton organisms that fell into the food size spectrum of mixotrophs. Conversely, high nutrient supplies prevented O. tuberculata from successfully invading the food webs. Two important conclusions were derived from our experiments. First, in contrast to a paradigm of ecology, specialization may not necessarily be the most successful strategy for survival under stable conditions. Indeed, the use of several resources with lower efficiency can be an equally, or even more, successful strategy in nature. Second, when limiting nutrients promote the growth of bacterio- and picophytoplankton, invading mixotrophs may have a habitat-ameliorating effect for higher trophic levels, gauged in terms of food quantity and quality. Using given resources more efficiently, O. tuberculata generated higher biomasses and expressed an increased nutritional value for potential planktivores, due to decreased cellular carbon to phosphorus (C:P) ratios compared to specialized plankton taxa. Our findings may help to explain why energy transfer efficiency between phytoplankton and higher trophic levels is generally higher in oligotrophic systems than in nutrient rich environments.
In laboratory experiments, I studied the influences of bacterial density and light on the ingestion and growth rates, pigment contents, and the carbon and phosphorus turnover rates of the mixotrophic flagellate Ochromonas sp. The investigated strain is a bacterivorous flagellate that can enhance its photosynthetic apparatus and grow phototrophically when bacterial densities are low. This was also evident from significantly higher chlorophyll a contents during active photosynthetic growth phases. Moderate phototrophic growth should be possible even if bacteria were absent. Bacterial ingestion rates increased hyperbolically with bacterial density, and there was no difference between light- and dark-adapted cells. Ochromonas released soluble reactive phosphorus (SRP) when growth was predominantly phagotrophic, but it took up SRP when growth was phototrophic. The mixotrophic strategy in Ochromonas appears to be bound up with costs and trade-offs: Ochromonas needs high bacterial densities to reach maximum growth rates, its basic metabolic costs are higher than for obligately phagotrophic flagellates, and its phototrophic growth rates are lower than for obligately phototrophic phytoplankton of comparable size.
The chrysophyte genera Poterioochromonas and Ochromonas and their heterotrophic analogons, i.e. the 'Spumella-like' flagellates, account for a significant and often dominating fraction of the pelagic nanoplankton. Even though several osmotrophically and autotrophically grown strains of Ochromonas and Poterioochromonas are assumed to produce toxins, the potential toxicity has been investigated neither for its association with bacterivorous nutrition nor within the related exclusively heterotrophic 'Spumella- like' flagellates. We investigated the toxic potential of several flagellate strains using cultures of flagellates, cell extracts and filtrate of flagellate cultures. The effect on potential predators was exemplarily tested for the cladoceran Daphnia magna and the rotifer Platyias sp. All tested heterotrophic and mixotrophic flagellate strains were toxic to zooplankton at abundances exceeding 104 flagellates mL� 1. For the rotifers, survival on any of the flagellate strains was significantly lower than that in the control treatment (P < 0.001) already after 24 h. We conclude that (i) 'Spumella-like' flagellates can be toxic to zooplankton, (ii) all tested flagellates, i.e. heterotrophic and mixotrophic flagellates, feeding phagotrophi- cally can be toxic to zooplankton and (iii) sublethal effects may be observed at typical field abundances, even though acute toxicity seems to be restricted to flagellate abundances observed only at peak events.
Monitoring in Lake Ontario in 1970 and 1982 demonstrated that the zooplankton community was dominated by microzooplankton, which suggested a longer, perhaps inefficient food chain. In this study, annual monitoring of the offshore region of Lake Ontario between 1986 and 1992 was used to determine if microzooplankton were still dominant despite recent changes in nutrient loading and species introductions. Microzooplankton accounted for 49.7% of the total summer zooplankton biomass while small edible phytoplankton accounted for 67.0% of the biomass during the summer. By direct in situ measurement using a Haney grazing chamber, rather than size grazing relationships, the relative impact of micro- and mesozooplankton grazers on phytoplankton production during the summer of 1995 was evaluated. Microzooplankton filtration rates (%/d) for 1995 were significantly higher than mesozooplankton filtration rates. Zooplankton consumed only 17.5% /d of the primary production with microzooplankton grazing representing 69.8% to 93.2% of this amount. Microzooplankton are clearly still dominant and their consumption of primary production in Lake Ontario is low. The major pathway of energy transfer can not be through the classical phytoplankton > large zooplankton > planktivore > piscivore food chain but rather through the phytoplankton > microzooplankton and presumably predacious zooplankton and fish. The longer food chain is a result of the introduction of a size-selective planktivore, the alewive, which has decreased the length and presumably lowered the consumption rate of the entire zooplankton community. This structural impact, a longer food chain, theoretically creates a higher factor of biomagnification of organic chemicals for top-level predators along with lower rates of energy transfer within the food web and suggests lower fish production than in a shorter food web.
The wide variety of unicellular, phagotrophic eucaryotes known collectively as heterotrophic microflagellates has recently attracted much attention particularly among biological oceanographers. Knowledge of the morphology, systematic affinities, and general biology of members of this heterogeneous assemblage of protists is still far from complete. Even so, literature spanning over more than a century gives evidence of the diversity of these forms and of their ubiquitous occurrence. Lohmann (1911, 1920) attempted to quantify these small protozoans in seawater and assess their ecological significance, and Griessmann (1914) isolated a variety of forms in culture and described aspects of their biology.
Lake size and depth mediate the strength of interaction between fish and zooplankton. We test whether this variation in zooplanktivory indirectly affects the phytoplankton by comparing 19 lakes that represent two food webs resulting from the absence of piscivores in small, partial-winterkill lakes. Lakes with piscivorous fish are further distinguished by thermal stratification, which provides a refuge for zooplankton to avoid fish predation. We contrasted phytoplankton abundance in these three categories of lakes over six years, using both direct measures of concentration and a growth bioassay that measures phytoplankton from the perspective of a standard grazer (Daphnia). Contrary to expectations, phytoplankton abundance was largely unaffected by trophic structure or the presence of a deep-water refuge. However, grazer growth differed dramatically among the three categories of lakes. Consistent with trophic cascade, increased fish planktivory resulted in more phytoplankton food as measured from the grazer's perspective. This effect was independent of lake productivity or total abundance and size of phytoplankton. Instead, variation in food quality for grazers was associated with compositional differences in phytoplankton. These results indicate that persistent trophic cascades are more dramatic in the plankton than previously realized but primarily influence composition, rather than biomass. Although cryptic, such top-down effects create functional variation in grazer-resource coupling.
A species of the chrysophycean genus Ochromonas from England was grown in pure culture and compared with similar strains isolated in the United States. Although these organisms possess chromatophores with chlorophyll, they need organic substances not only as a source of nitrogen compounds, but as independent carbon and energy sources; they also require certain growth factors. Peptones are better as nitrogen sources than single amino-acids, few of which give satisfactory results. The utilization of inorganic nitrogen could not be demonstrated. As carbon sources sugars, alcohols, and fats, and, to a lesser degree, acetate, are suitable. Growth factors contained in liver extract, milk and yeast autolysate, and in smaller amounts in most peptones, are indispensable. Enzymes hydrolyzing starch, sucrose, fat, and protein are excreted.
Ochromonas ingests and digests starch grains, casein, oil droplets, and small organisms. Neither bacteria nor yeast nor small algae were found able to support growth of any of the strains, even in the light. An additional carbon compound and possibly special vitamins are required. The hypothesis is put forward that phagotrophy chiefly serves for obtaining chemical compounds which the cell cannot synthesize itself and which have the character of vitamins. Phagotrophy therefore supplements the other means of nutrition, in the main quantitatively, while sugar, &; c., supplement it quantitatively and are indeed indispensable.
The same media which support ample growth in the light do so also in the dark. This shows that photosynthesis is of little importance for the growth of the organisms, although it keeps them alive for long periods, while in the dark they soon die.
Correlated with the manifold ways of acquiring food, there is also a remarkable variability in the size and shape of the cells, and still more in the dimensions and pigmentation of the chromatophores, and in the reserves stored as leucosin, volutin, and oil. These features which now prove to depend so much on conditions have previously been widely used in the diagnosis of species. The basis of classification should therefore be revised. Apart from the stigma, which is specific, use ought to be made only of those characters whose variation with conditions is reasonably well known.
The extraordinary nutritional versatility of Ochromonas is considered to be a primitive character. From ancestors with a mixed nutritional habit, phototrophic, phagotrophic, and saprotrophic flagellates seem to have evolved, each with only one of the three modes of nutrition that are combined in Ochromonas.
Alternative models for the dynamics of edible phytoplankton were compared using long-term data from mesotrophic Paul Lake and eutrophic Lake Mendota. Alternative models fit to the data contrasted linear versus logistic algal growth, type I versus type II functional response, and prey-dependent versus ratio-dependent predation. In both lakes, the model with lowest prediction error had logistic algal growth and a type I, prey-dependent functional response. Under these models, the spring bloom and clear-water phase of productive lakes can be explained as an incomplete predator–prey cycle: the spring pulse of edible algae is followed by a peak of Zooplankton; then, edible algae are overgrazed leading to the clear-water phase and collapse of the grazer biomass. This study demonstrates the use of time series data at the ecosystem scale to identify process-based models, contrast alternative models on a probabilistic basis, and estimate parameters. This approach avoids the assumptions involved in extrapolating ecosystem models from smaller scale studies.
The majority of organisms can be grouped into those relying solely on photosynthesis (phototrophy) or those relying solely on the assimilation of organic substances (heterotrophy) to meet their requirements for energy and carbon. However, a special life history trait exists in which organisms combine both phototrophy and heterotrophy. Such "mixotrophy" is a widespread phenomenon in aquatic habitats and is observed in many protozoan and metazoan organisms. The strategy requires investment in both photosynthetic and heterotrophic cellular apparatus, and the benefits must outweigh these costs. In accordance with mechanistic resource competition theory, laboratory experiments revealed that pigmented mixotrophs combined light, mineral nutrients, and prey as substitutable resources. Thereby, they reduced prey abundance below the critical food concentration of competing specialist grazers [Rothhaupt, K. O. (1996) Ecology 77, 716-724). Here, we demonstrate the important consequences of this strategy for an aquatic community. In the illuminated surface strata of a lake mixotrophs reduced prey abundance steeply. The data suggest that, as a consequence, grazers from higher trophic levels, consuming both the mixotrophs and their prey, could not persist. Thus, the mixotrophs escaped from competition with and losses to higher grazers. Furthermore, the mixotrophs structured prey abundance along the vertical light gradient, creating low densities near the surface and a pronounced maximum of their algal prey at depth. Such deep algal accumulations are typical features of nutrient-poor aquatic habitats, previously explained by resource availability. We hypothesize instead that the mixotrophic grazing strategy is responsible for deep algal accumulations in many aquatic environments.
SYNOPSIS
Anacystis nidulans disappeared rapidly from culture in the presence of an unidentified species of Ochromonas. Disappearance was light‐independent and could be induced neither by bacteria associated with, nor by soluble products released from the flagellate. Electronmicrographs of mixed cultures revealed numerous A. nidulans cells in various stages of digestion within vacuoles of Ochromonas. Evidently the disappearance of the alga from culture resulted from phagotrophy by the chrysomonad. A 2‐stage digestive process is suggested whereby A. nidulans cells are initially sequestered in the posterior “leucosin” vacuole and then undergo the terminal stages of digestion and elimination in smaller, peripheral vacuoles.
The effects of the planktonic blue-green algae, Aphanizomenon gracile, Synechococcus elongatus, and Microcystis aeruginosa, on survival, growth, and food uptake of Daphnia pulicaria were determined. Synechococcus and Aphanizomenon were unsuitable food when offered alone, but did not affect the daphnids negatively when mixed with Scenedesmus. Microcystis was the only one found to be toxic. In pure suspensions of this blue-green, the daphnids did not survive more than 48 hours; they lived a little longer if Scenedesmus was supplied additionally. Growth was markedly reduced when only 50 μg carbon/l of Microcystis was added to the normal Scenedesmus food. It ceased at a concentration of 250 μg C/l. This can be explained by the reduction of food uptake. Very small quantities of Microcystis (10 μg C/l) present in the normal food caused a significant reduction of the filtering rate. Filtering inhibition was associated with the cells. Filtrate of Microcystis suspensions was not effective. Thus, the daphnids must ingest the blue-green cells in order to become toxified. Dual-labelling experiments showed that Microcystis cells are filtered from the medium by Daphnia with the same efficiency as Scendesmus and are not rejected. Toxicity of Microcystis is considered to be an effective defence mechanism against grazing pressure.
1. An overview is provided of the role of mixotrophic protists in plankton communities. Consideration of the importance of phagotrophy in the evolution of photosynthetic eucaryotes suggests that mixotrophy as a nutritional strategy can arise rather readily.
2. Mixotrophic protists actually present a spectrum of nutritional strategies. However, recognition of distinct groups of mixotrophs based on nutritional behaviour facilitates consideration of their functional role and of competitive interactions with other types of planktonic protists.
3. Consideration of the costs and benefits of mixotrophy as a nutritional strategy allows the development of several empirical predictions about the probable outcome of resource competition between mixotrophs and obligate phototrophs or phagotrophs. Existing results from laboratory and field experiments allow some of these predictions to be evaluated.
4. These results indicate that, under specified conditions, mixotrophs should represent an important link in the flux of materials through planktonic food webs. However, quantifying these fluxes remains a challenge for the future.
Mixotrophic organisms can combine two functionally different modes of nutrition to acquire carbon: (i) by using photosynthesis for inorganic carbon fixation; and (ii) by taking up organic sources. Because of these different metabolic pathways, their biochemical composition, for example, the amount and composition of consumer‐relevant compounds such as polyunsaturated fatty acids, varies, and thus, we tested the hypothesis that the mode of nutrition of an osmo‐mixotrophic flagellate determines the food quality for their consumers: three rotifer species.
Using life table experiments with auto‐, mixo‐ and heterotrophically grown Chlamydomonas acidophila as food sources, we found species‐specific differences in life span, fecundity, population growth rate, egg size and maternal effects on the starvation resistance of neonates between the three rotifer species.
Population growth of two out of the three rotifers ( Brachionus sericus and Elosa worallii ) was negatively affected when fed with heterotrophic food, compared to animals fed with autotrophic food. In contrast, Cephalodella sp. was able to use all C. acidophila with similar efficiency.
These results explain the vertical distribution of two of the rotifers in their natural habitat, where Cephalodella sp. dominates over E. worallii in deep water layers characterized by light intensities below the compensation point for autotrophic growth of C. acidophila . It is hypothesized that temporal changes in the mode of nutrition of mixotrophs have consequences for the outcome of the competition between consumers and for the carbon transfer in many planktonic food webs.
1. The photoautotrophic micro‐organisms collectively termed ‘micro‐algae’ (including micro‐eukaryotes and cyanobacteria) are known to produce a wide range of secondary metabolites with various biological actions. A small subset of these compounds has been identified. Some of them, termed allelopathic compounds, have been shown to play a role in allelopathy, defined here as inhibitory effects of secondary metabolites against either competitors or predators. Freshwater cyanobacteria also produce some secondary metabolites, termed toxins, which are highly toxic for animals.
2. While allelopathic compounds play a role in the interactions between the emitter organisms and their direct competitors or predators, toxins are categorised according to their toxic effect on several organisms, including some that may not be present in their immediate environment. However, these two definitions are not mutually exclusive. This review considers the evolutionary, ecological and physiological aspects of the production of allelopathic compounds by micro‐algae in freshwaters, and compares the characteristics of allelopathic compounds with those of toxins.
3. Allelopathic compounds include alkaloids, cyclic peptides, terpens and volatile organic compounds. Toxins include alkaloids, cyclic peptides and lipopolysaccharides. No allelopathic compound type is associated with a particular phylogenetic group of algae. In contrast, freshwater toxins are only produced by cyanobacteria belonging to a restricted number of genera. Allelopathic compounds have various modes of action, from inhibition of photosynthesis to oxidative stress or cellular paralysis. Toxins are often enzyme inhibitors, or interfere with cell membrane receptors.
4. The ecological roles of allelopathic compounds have been well identified in several cases, but those of toxins are still debated. In the light of descriptions of negative effects of toxins on both micro‐invertebrates and photoautotrophic organisms, we suggest that at least some toxins should actually be considered as allelopathic compounds. Further research on toxic secondary metabolites in freshwaters is now needed, with emphasis on the ecological effects of the compounds in the immediate environment of the emitter algae.
The aim of this study was to determine the relative importance of the different processes/mechanisms by which the toxic haptophyte Prymnesium parvum, cultured under different nutrient conditions, affects non-toxic phytoplankton competitors and microzooplankton grazers. P. parvum was cultured under steady-state growth in different nutrient conditions: nitrogen depleted (-N), phosphorus depleted (-P) and balanced nitrogen and phosphorus (+NP). Cells from each nutrient condition and culture cell-free filtrates, alone and combined with non-toxic prey (Rhodomonas salina), were used as food for the rotifer Brachionus plicatilis. An additional experiment was carried out to test the effect of P. parvum cells and culture cell-free filtrate on R. salina. The highest haemolytic activity values were achieved by -P F parvum cultures, followed by -N. However, the negative effect of R parvum on R. salina and rotifers did not correlate with haemolytic activity but with the number of P. parvum cells. -N-cultured P. parvum were the most toxic for both R. salina and rotifers, followed by +NP. Therefore, haemolytic activity is not a good indicator of the total potential toxicity of R parvum. The growth rate of R. salina was negatively affected by cell-free filtrates but the effect of P, parvum predation was greater. Rotifers fed on both toxic and non-toxic algae, indicating that they did not select against the toxic alga. The P. parvum cell-free filtrate had an effect on B. plicatilis, although this was weak, B, plicatilis was also indirectly affected by P. parvum due to the negative effects of the toxic alga on their prey (R. salina). However, the greatest negative effect of P. parvum on the rotifers was due to ingestion of the toxic cells. Therefore, the phytoplankton competitor R. salina is more affected by P. parvum predation and the grazer B. plicatilis is more affected by ingestion of the toxic cells, the effects of excreted compounds being secondary.
Historically most harmful algal species (HAS) have been thought to be strictly phototrophic. Mixotrophy, the use of phototrophy and heterotrophy in combination, has been emphasized as operative mainly in nutrient-poor habitats as a mechanism for augmenting nutrient supplies. Here we examine an alternate premise, that many harmful algae which thrive in eutrophic habitats are mixotrophs that respond both directly to nutrient inputs, and indirectly through high abundance of bacterial and algal prey that are stimulated by the elevated nutrients. From review and synthesis of the available data, mixotrophy occurs in all HAS examined thus far in the organic substrate- and prey-rich habitats of eutrophic estuarine and marine coastal waters. Where data are available comparing phototrophy versus mixotrophy, mixotrophy in eutrophic habitats generally is significant in nutrient acquisition and growth of HAS and, therefore, likely important in the development and maintenance of their blooms. In eutrophic habitats phagotrophic mixotrophs, in particular, have been shown to attain higher growth than when in phototrophic mode. Yet for many HAS, quantitative data about the role of mixotrophy in nutrition, growth, and blooms are lacking, especially relating laboratory information to natural field assemblages, so that the relative importance of photosynthesis, dissolved organic nutrients, and ingestion of prey largely remain unknown. Research is needed to assess simultaneously the roles of phototrophy, osmotrophy and phagotrophy in the nutritional ecology of HAS in eutrophic habitats, spanning bloom initiation, development and senescence. From these data, models that include the role of mixotrophy can be developed to gain more realistic insights about the nutritional factors that control harmful algae in eutrophic waters, and to strengthen predictive capability in predicting their blooms. An overall forecast that can be tested, as well, is that harmful mixotrophic algae will become more abundant as their food supplies increase in many estuaries and coastal waters that are sustaining chronic, increasing cultural eutrophication.
The structure of aquatic ecosystems is determined by complex interactions among individual organisms at different trophic levels. Although our basic understanding of how top-down and bottom-up processes interact to determine food-web dynamics has advanced, we still lack insights into how complex interactions and feedbacks affect the dynamics and structure of food webs. It is now becoming increasingly clear that, in addition to energy transfer from one trophic level to the other, there is exchange of information between these levels facilitated by the release of infochemicals by the organisms. There is evidence from recent studies that the exchange of chemical information in freshwater ecosystems is likely to play a decisive role in shaping structure and functioning of these systems. Chemical communication among freshwater organisms mediates many aspects of both predation and interspecific competition, which play key roles in determining community structure and ecosystem functioning. For example, consumer-induced defences in phytoplankton and zooplankton include modifications in the characteristics relating to life history, behaviour, morphology and biochemistry. These inducible defences affect trophic interactions by altering predator feeding rates through changes in attack rate or handling time, or both. Also host-specific fungal parasitism in phytoplankton is probably controlled by infochemicals. The motile fungi recognise their host by host-secreted compounds. Until now models describing the functioning of ecosystems mainly considered flows of biomass and energy. Integration of new knowledge about the role of chemical communication in these models may be one of the aims of ecological informatics. In this chapter I discuss how infochemicals may affect the dynamics and structure of planktonic food webs.
Flagellates are important bacterial grazers in most planktonic food webs. The prey-size preference of the mixotrophic flagellate, Ochromonas sp. (Chrysophyceae), isolated from an extremely acidic lake, Lake 111 (pH 2.6), was determined using fluorescently labelled microspheres (beads). According to grazing experiments with cultured bacteria, also isolated from Lake 111, the potential grazing impact on Lake 111’s single-celled bacterial production was calculated. Ochromonas sp. ingested the smallest beads offered (0.5 µm diameter) at the highest rate. Ingestion rate declined with increasing bead size. The highest prey volume-specific ingestion was measured for Ochromonas sp. feeding on intermediate-sized beads (1.9 µm). Ingestion rates were low due in part to the large fraction of inactive flagellates observed. According to the bacterial ingestion rate, a mean of 88% (epilimnion) and 68% (hypolimnion) of in situ single-celled bacterial production is potentially grazed daily by Ochromonas sp. In the epilimnion of Lake 111, the heterotrophic carbon gain is three times higher than the autotrophic production. Alongside carbon uptake, Ochromonas sp. also benefits from ingesting bacteria through the uptake of phosphorus. A biovolume minimum corresponding to the prey size at which Ochromonas sp. feeds most efficiently occurred in the Lake 111 epilimnetic bacterial community, implying top-down control of the bacterial community by Ochromonas sp.
Digestion of bacterial biomass by three species of phagotrophic flagellates was studied using radioactive tracer techniques and short-term feeding experiments. Macromolecules of two different bacterial strains and natural limnic bacterioplankton were pulse-chase-labelled with one of the following precursors H-3-thymidine, S-35-/C-14-methionine or C-14-leucine, before bacteria were fed to flagellates and radioactive labels were traced into flagellate macromolecules. The concentrations of prey and predators were monitored by flow cytometry. The aim of the work was to compare efficiencies of bacterial macromolecule accumulation by mixotrophic (Ochromonas) and heterotrophic (Spumella and Bodo) flagellates. We observed that flagellate accumulation efficiency of bacterial macromolecules labelled with thymidine (mean 15-30%, depending on flagellate species) was lower than of bacterial macromolecules labelled with amino acids (mean 26-68%). Heterotrophic flagellate species had similar accumulation efficiencies of bacterial molecules, when either leucine (26-42%) or methionine (31-41%) was used as a tracer. In contrast the mixotrophic flagellate accumulated significantly more residues of labelled methionine (68%) than of labelled leucine (54%). Methionine seems to be accumulated as an intact molecule and possibly Ochromonas preferentially accumulated methionine as an additional source of reduced sulphur. Protozoan accumulation efficiencies did not differ significantly whether the pulse-labelled bacterial prey were from growing or long-term starvation cultures. Our results suggest that labelled amino acids are more appropriate than labelled thymidine for studying transfer of bacterial biomass within food webs
The eukaryotic alga Ochromonas danica, a nutritionally versatile, mixotrophic chrysophyte, grew on phenol as the sole carbon source in axenic culture and removed the phenol carbon from the growth medium. Respirometric studies confirmed that the enzymes involved in phenol catabolism were inducible and that the alga oxidized phenol; the amount of oxygen consumed per mole of oxidized substrate was approximately 65% of the theoretical value. [U-14C]phenol was completely mineralized, with 65% of the 14C label appearing as 14CO2, approximately 15% remaining in the aqueous medium, and the rest accounted for in the biomass. Analysis of the biomass showed that 14C label had been incorporated into the protein, nucleic acid, and lipid fractions; phenol carbon is thus unequivocally assimilated by the alga. Phenol-grown cultures of O. danica converted phenols to the corresponding catechols, which were further metabolized by the meta-cleavage pathway. This surprising result was rigorously confirmed by taking the working stock culture through a variety of procedures to check that it was axenic and repeating the experiments with algal extracts. This is, as far as is known, the first definitive identification of the meta-cleavage pathway for aromatic ring degradation in a eukaryotic alga, though its incidence in other eukaryotes has been (infrequently) suggested.
Heterotrophic flagellates (HF) are known as most important grazers of bacteria in many aquatic ecosystem. HF cannot be treated as a black box since HF generally contain a diverse community of species significantly differing in their feeding behaviour and other ecological properties. Today it seems that the dominant taxonomic groups among heterotrophic nano- and microflagellate communities within different marine, brackish and limnetic pelagic communities (heterokont taxa, dinoflagellates, choanoflagellates, kathablepharids) and benthic communities (euglenids, bodonids, thaumatomonads, apusomonads, cercomonads) are relatively similar. HF among protista incertae sedis, often neglected in ecological studies, are abundant bacterivores in all investigated habitats. Recent studies of flagellate feeding processes indicated that there are significant species-specific differences and individual variability regarding the food uptake and food selection of bacterivorous flagellates: Variability of bacterivory is discussed regarding the prevailing feeding modes, the energy budgets, the considerable importance of slight deviations in the time budgets of feeding phases, the ingestion rates and the feeding microhabitat, respectively. The significant flexibility of the grazing impact of bacterivorous flagellate communities creates a complex top-down pressure on bacteria which should have lead to the evolution of efficient predator avoidance mechanisms in bacteria and should be at least partly responsible for the diversity of present bacteria.
cell )4.66 0.230 <0.0001 High Och
- High
High, only Och. cell )4.66 0.230 <0.0001 High Och. cells + good food )3.93 0.259 <0.0001 Mean difference from starvation control SE Sig.
Reverse evolution: driving forces behind the loss of acquired photosynthetic traits. PLoS One, 4, e8465. Doi: 10.1371/ journal Phagotrophic ingestion of a blue-green alga by Ochromonas
- F Castro
- U Gaedke
- J Boenigk
de Castro F., Gaedke U. & Boenigk J. (2009) Reverse evolution: driving forces behind the loss of acquired photosynthetic traits. PLoS One, 4, e8465. Doi: 10.1371/ journal.pone.0008465. Daley R.J., Morris J.P. & Brown S.R. (1973) Phagotrophic ingestion of a blue-green alga by Ochromonas. Journal of Eukaryotic Microbiology, 20, 58–61.
Ecology of harmful algae Mixotrophy in chrysophytes
- E Grané
- J T Turner
Grané E. & Turner J.T., (Eds) (2006). Ecology of harmful algae. Ecological Studies, 189, 413, ISBN: 3-540-32209-4, Springer, Berlin Holen D.A. & Boraas M.E. (1995) Mixotrophy in chrysophytes. In: Chrysophyte Algae: Ecology, Phylogeny and Development (Eds C.D. Sandgren, J.P. Smol & J.
Ecology of harmful algae
- Granéli
Granéli E. & Turner J.T., (Eds) (2006). Ecology of harmful
algae. Ecological Studies, 189, 413, ISBN: 3-540-32209-4,
Springer, Berlin