Aditee Mitra

Promotion of harmful algal blooms by zooplankton predatory activity.

The relationship between algae and their zooplanktonic predators typically involves consumption of nutrients by algae, grazing of the algae by zooplankton which in turn enhances predator biomass, controls algal growth and regenerates nutrients. Eutrophication raises nutrient levels, but does not simply increase normal predator–prey activity; rather, harmful algal bloom (HAB) events develop often with serious ecological and aesthetic implications. Generally, HAB species are outwardly poor competitors for nutrients, while their development of grazing deterrents during nutrient stress ostensibly occurs too late, after the nutrients have largely been consumed already by fast-growing non-HAB species. A new mechanism is presented to explain HAB dynamics under these circumstances. Using a multi-nutrient predator–prey model, it is demonstrated that these blooms can develop through the self-propagating failure of normal predator–prey activity, resulting in the transfer of nutrients into HAB growth at the expense of competing algal species. Rate limitation of this transfer provides a continual level of nutrient stress that results in HAB species exhibiting grazing deterrents protecting them from top-down control. This process is self-stabilizing as long as nutrient demand exceeds supply, maintaining the unpalatable status of HABs; such events are most likely under eutrophic conditions with skewed nutrient ratios.

Importance of Interactions between Food Quality, Quantity, and Gut Transit Time on Consumer Feeding, Growth, and Trophic Dynamics

Ingestion kinetics of animals are controlled by both external food availability and feedback from the quantity of material already within the gut. The latter varies with gut transit time (GTT) and digestion of the food. Ingestion, assimilation efficiency, and thus, growth dynamics are not related in a simple fashion. For the first time, the important linkage between these processes and GTT is demonstrated; this is achieved using a biomass‐based, mechanistic multinutrient model fitted to experimental data for zooplankton growth dynamics when presented with food items of varying quality (stoichiometric composition) or quantity. The results show that trophic transfer dynamics will vary greatly between the extremes of feeding on low‐quantity/high‐quality versus high‐quantity/low‐quality food; these conditions are likely to occur in nature. Descriptions of consumer behavior that assume a constant relationship between the kinetics of grazing and growth irrespective of food quality and/or quantity, with little or no recognition of the combined importance of these factors on consumer behavior, may seriously misrepresent consumer activity in dynamic situations.

Mixotrophy in the Marine Plankton

Mixotrophs are important components of the bacterioplankton, phytoplankton, microzooplankton, and (sometimes) zooplankton in coastal and oceanic waters. Bacterivory among the phytoplankton may be important for alleviating inorganic nutrient stress and may increase primary production in oligotrophic waters. Mixotrophic phytoflagellates and dinoflagellates are often dominant components of the plankton during seasonal stratification. Many of the microzooplankton grazers, including ciliates and Rhizaria, are mixotrophic owing to their retention of functional algal organelles or maintenance of algal endosymbionts. Phototrophy among the microzooplankton may increase gross growth efficiency and carbon transfer through the microzooplankton to higher trophic levels. Characteristic assemblages of mixotrophs are associated with warm, temperate, and cold seas and with stratification, fronts, and upwelling zones. Modeling has indicated that mixotrophy has a profound impact on marine planktonic ecosystems and may enhance primary production, biomass transfer to higher trophic levels, and the functioning of the biological carbon pump.

Ocean acidification with (de)eutrophication will alter future phytoplankton growth and succession

Human activity causes ocean acidification (OA) though the dissolution of anthropogenically generated CO2 into seawater, and eutrophication through the addition of inorganic nutrients. Eutrophication increases the phytoplankton biomass that can be supported during a bloom, and the resultant uptake of dissolved inorganic carbon during photosynthesis increases water-column pH (bloom-induced basification). This increased pH can adversely affect plankton growth. With OA, basification commences at a lower pH. Using experimental analyses of the growth of three contrasting phytoplankton under different pH scenarios, coupled with mathematical models describing growth and death as functions of pH and nutrient status, we show how different conditions of pH modify the scope for competitive interactions between phytoplankton species. We then use the models previously configured against experimental data to explore how the commencement of bloom-induced basification at lower pH with OA, and operating against a background of changing patterns in nutrient loads, may modify phytoplankton growth and competition. We conclude that OA and changed nutrient supply into shelf seas with eutrophication or de-eutrophication (the latter owing to pollution control) has clear scope to alter phytoplankton succession, thus affecting future trophic dynamics and impacting both biogeochemical cycling and fisheries.

Monster potential meets potential monster: pros and cons of deploying genetically modified microalgae for biofuels production.

Biofuels production from microalgae attracts much attention but remains an unproven technology. We explore routes to enhance production through modifications to a range of generic microalgal physiological characteristics. Our analysis shows that biofuels production may be enhanced ca fivefold through genetic modification (GM) of factors affecting growth rate, respiration, photoacclimation, photosynthesis efficiency and the minimum cell quotas for nitrogen and phosphorous (N : C and P : C). However, simulations indicate that the ideal GM microalgae for commercial deployment could, on escape to the environment, become a harmful algal bloom species par excellence, with attendant risks to ecosystems and livelihoods. In large measure, this is because an organism able to produce carbohydrate and/or lipid at high rates, providing stock metabolites for biofuels production, will also be able to attain a stoichiometric composition that will be far from optimal as food for the support of zooplankton growth. This composition could suppress or even halt the grazing activity that would otherwise control the microalgal growth in nature. In consequence, we recommend that the genetic manipulation of microalgae, with inherent consequences on a scale comparable to geoengineering, should be considered under strict international regulation.

The influence of changes in predation rates on marine microbial predator/prey interactions: a modelling study

A mathematical model was developed to represent the dynamics of predation and assimilation of ingested material by heterotrophic marine micro-zooplankton. Predation rate was made a rectangular hyperbolic function of prey carbon (C) concentration modified to simulate the prey selectivity that these organisms have been observed experimentally to exhibit in response to prey nutritional quality. We chose prey N:C ratio as an index of selectivity and related both the maximum predation rate (PM) and the assimilation efficiency (AE) to changes in prey nitrogen:carbon (N:C). Changes in PM simulated the phenomena of “surge feeding” and “prey rejection”. Changes in AE simulated sub-optimal assimilation of material from ingested prey, which in turn, served to decrease the ingestion rate on this material. The model was parameterised using laboratory data sets that followed ingestion of non-growing phytoplankton prey of different N:C ratio by a micro-flagellate predator. Investigative simulations in transient conditions, incorporating growing prey and hence with changing N:C ratio, indicated both PM and AE influenced the quantitative and temporal dynamics of C transfer to the higher trophic level. In particular, we noted that although various model formulations predicted similar trophic transfer of C, this was achieved on very different time scales. The inclusion of heterotrophic micro-zooplankton within food web models is a necessary step in accurate prediction of pelagic nutrient flux but requires physiological models carefully parameterised and tested in both steady state and transient conditions to ensure accurate simulation.

Metabolic and physiological changes in Prymnesium parvum when grown under, and grazing on prey of, variable nitrogen : Phosphorus stoichiometry

Mixotrophy is found in almost all classes of phytoplankton in a wide range of aquatic habitats ranging from oligotrophic to eutrophic marine and freshwater systems. Few studies have addressed how the nutritional status of the predator and/or the prey affects mixotrophic metabolism despite the realization that mixotrophy is important ecologically. Laboratory experiments were conducted to examine changes in growth rates and physiological states of the toxic haptophyte Prymnesium parvum when fed Rhodomonas salina of varying nutritional status. Haemolytic activity of P. parvum and prey mortality of R. salina were also measured. P. parvum cultures grown to be comparatively low in nitrogen (low-N), phosphorus (low-P) or low in both nutrients (low-NP) were mixed with low-NP, low-N, and low-P R. salina in all possible combinations, i.e., a 3×3 factorial design. N deficiency was obtained in the low-N cultures, while true P deficiency may not have been obtained in the low-P cultures. Mortality rates of R. salina (both due to ingestion and/or cell rupture as a function of grazing or toxic effects) were higher when R. salina cells were low-P, N-rich, regardless of the nutritional state of P. parvum. Mortality rates were, however, directly related to the initial prey:predator cell ratios. On the other hand, growth of the predator was a function of nutritional status and a significant positive correlation was observed between growth rates of P. parvum and cell-specific depletion rates of N, whereas no such relationship was found between P. parvum growth rates and depletion rates of P. In addition, the greatest changes in chlorophyll content and stoichiometric ratios of P. parvum were observed in high N:P conditions. Therefore, P. parvum may show enhanced success under conditions of higher inorganic N:P, which are likely favored in the future due to increases in eutrophication and altered nutrient stoichiometry driven by anthropogenic nutrient loads that are increasingly enriched in N relative to P.

Mixotrophy in Harmful Algal Blooms: By Whom, on Whom, When, Why, and What Next

The traditional view of the planktonic food web is simplistic: nutrients are consumed by phytoplankton that, in turn, support zooplankton, which ultimately support fish. This structure is the foundation of most models used to explore fisheries production, biogeochemical cycling, and climate change. In recent years, however, the importance of mixotrophs increasingly has been recognized. Mixotrophy, the combination of phototrophy and heterotrophy (the latter, including phago- and/or osmotrophy), enables planktonic protists traditionally labeled as “phytoplankton” or “microzooplankton” to function at multiple trophic levels. Mixotrophy enables primary producers to acquire nutrients directly from ingestion of prey such as bacteria and algal competitors and even from their own potential predators. Mixotrophy is not simply additive or substitutional; rather, it is synergistic. While most harmful algal species (except diatoms and cyanobacteria) are mixotrophic via phagotrophy, little is known about how these organisms modulate their phototrophic and phagotrophic activities or how the flow of energy and material through mixotrophic predator-prey interactions is altered under varying nutrient, temperature, light, pH, or pCO2 conditions. All of these factors are also rapidly changing in coastal and oceanic environments with accelerating eutrophication and climate change that, in turn, alters the potential for harmful algal blooms. Accurate parameterization, including consideration of mixotrophy in water quality or fisheries models that are used as aids to regional and/or international policy development, should be a high priority.

Biological or microbial carbon pump? The role of phytoplankton stoichiometry in ocean carbon sequestration

Once fixed by photosynthesis carbon becomes part of the marine food web. The fate of this carbon has two possible outcomes: it may be respired and released back to the ocean and potentially to the atmosphere as CO2 or retained in the ocean interior and/or marine sediments for extended time scales. The most important biologically mediated processes responsible for long term carbon storage in the ocean are the biological carbon pump (BCP) and the microbial carbon pump (MCP). While acting simultaneously in the ocean, the balance between these two mechanisms is thought to vary depending on the trophic state of the environment. Using previously published formulations, we propose a modelling framework to simulate variability in the MCP: BCP ratio as a function of external nutrients. Our results suggest that the role of the MCP might become more significant under future climate change conditions where increased stratification enhances the oligotrophic nature of the surface ocean. Based on these model results, we propose a conceptual framework in which the internal stoichiometry of phytoplankton, modulating both grazing pressure and DOM production (via phytoplankton exudation), plays a crucial role in regulating the MCP: BCP ratio.

Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance

This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.