Importance of dynamics of acquired phototrophy amongst mixoplankton; a unique example of essential nutrient transmission in community ecology

Transfers of energy and nutrients from producers to consumers are fundamental to ecosystem structure and functioning. A common example is the transfer of essential amino acids and fatty acids, produced by phototrophs, up through successive trophic levels. A highly specialised example is the transmission of acquired phototrophy between certain plankton. There are > 250 species of marine plankton that exploit acquired phototrophy; the Teleaulax-Mesodinium-Dinophysis (TMD) trinity is the most studied complex. In the TMD-trinity, plastids and nuclear material produced by the cryptophyte Teleaulax are transferred during feeding to the ciliate, Mesodinium and these acquired plastids are subsequently transferred from Mesodinium to its predator, the dinoflagellate Dinophysis. These plastidic non-constitutive mixoplankton, Mesodinium and Dinophysis, are globally ubiquitous and ecologically important organisms. Mesodinium can form red-tide blooms, while Dinophysis spp. cause diarrhetic shellfish poisoning events and shellfisheries closures. However, very little is known about the impact of different environmental stressors on the transmissions of acquired phototrophy, the subsequent decay of that phototrophic potential over time, and the implications for community trophic dynamics. Here, for the first time, the implications of the transmission dynamics of acquired phototrophy for the success of the TMD-trinity were explored under different nitrogen and phosphorus (N:P) nutrient ratios and loadings (eutrophic, mesotrophic, oligotrophic). Using a multi-nutrient simulator, bloom dynamics were shown to be markedly different under these scenarios, highlighting the importance of variable stoichiometry in community ecology. Importantly, dynamics were sensitive to the longevity (half-life) of the acquired phototrophy (especially for Dinophysis at low nutrient high N:P), a feature for which appropriate empirical data are lacking. This work highlights the need to enhance our understanding about how environmental stressors arising from anthropogenic activities (including climate change) will impact transference of acquired phototrophy between trophic levels and thence marine biodiversity and ecosystem services

Bridging the gap between marine biogeochemical and fisheries sciences; configuring the zooplankton link

Mitra, Aditee ... et. al.-- Special issue North Atlantic Ecosystems, the role of climate and anthropogenic forcing on their structure and function.-- 24 pages, 6 figures, 2 tablestrophic components interact. However, integrative end-to-end ecosystem studies (experimental and/or modelling) are rare. Experimental investigations often concentrate on a particular group or individual species within a trophic level, while tropho-dynamic field studies typically employ either a bottom-up approach concentrating on the phytoplankton community or a top-down approach concentrating on the fish community. Likewise the emphasis within modelling studies is usually placed upon phytoplankton- dominated biogeochemistry or on aspects of fisheries regulation. In consequence the roles of zooplankton communities (protists and metazoans) linking phytoplankton and fish communities are typically under-represented if not (especially in fisheries models) ignored. Where represented in ecosystem models, zooplankton are usually incorporated in an extremely simplistic fashion, using empirical descriptions merging various interacting physiological functions governing zooplankton growth and development, and thence ignoring physiological feedback mechanisms. Here we demonstrate, within a modelled plankton food-web system, how trophic dynamics are sensitive to small changes in parameter values describing zooplankton vital rates and thus the importance of using appropriate zooplankton descriptors. Through a comprehensive review, we reveal the mismatch between empirical understanding and modelling activities identifying important issues that warrant further experimental and modelling investigation. These include: food selectivity, kinetics of prey consumption and interactions with assimilation and growth, form of voided material, mortality rates at different age-stages relative to prior nutrient history. In particular there is a need for dynamic data series in which predator and prey of known nutrient history are studied interacting under varied pH and temperature regimes. © 2014 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY licenseAC is funded by the Ministry of Science and Innovation of Spain through project CTM2009-08783. AM was part funded by NERC UK project NE/K001345/1. KJF was funded by NERC UK through projects NE/H01750X/1 and NE/F003455/1. [...] This review was supported in part by project EURO-BASIN (Ref. 264933, 7FP, European Union), and by a Leverhulme International Network ‘‘Placing marine mixotrophs in context: modelling mixotrophy in a changing world’’Peer reviewe

Feeding in mixoplankton enhances phototrophy increasing bloom-induced pH changes with ocean acidification

Plankton phototrophy consumes CO2, increasing seawater pH, while heterotrophy does the converse. Elevation of pH (>8.5) during coastal blooms becomes increasingly deleterious for plankton. Mixoplankton, which can be important bloom-formers, engage in both photoautotrophy and phagoheterotrophy; in theory, this activity could create a relatively stable pH environment for plankton growth. Using a systems biology modelling approach, we explored whether different mixoplankton functional groups could modulate the environmental pH compared to the extreme activities of phototrophic phytoplankton and heterotrophic zooplankton. Activities by most mixoplankton groups do not stabilize seawater pH. Through access to additional nutrient streams from internal recycling with phagotrophy, mixoplankton phototrophy is enhanced, elevating pH; this is especially so for constitutive and plastidic specialist non-constitutive mixoplankton. Mixoplankton blooms can exceed the size of phytoplankton blooms; the synergisms of mixoplankton physiology, accessing nutrition via phagotrophy as well as from inorganic sources, enhance or augment primary production rather than depressing it. Ocean acidification will thus enable larger coastal mixoplankton blooms to form before basification becomes detrimental. The dynamics of such bloom developments will depend on whether the mixoplankton are consuming heterotrophs and/or phototrophs and how the plankton community succession evolves

A revised interpretation of marine primary productivity in the Indian Ocean: the role of mixoplankton

Traditional interpretations of marine plankton ecology, such as that in the Indian Ocean, mirror the plant-animal dichotomy of terrestrial ecology. Thus, single-celled phytoplankton produce food consumed by single-celled zooplankton, and these are in turn consumed by larger zooplankton through to higher trophic levels. Our routine monitoring surveys, research, models, and water management protocols all reflect this interpretation. The last decade has witnessed the development of an important revision of that traditional vision. We now know that the phytoplankton-zooplankton dichotomy represents, at best, a gross simplification. A significant proportion of the protist plankton at the base of the oceanic food-web can photosynthesise (make food ‘like plants’) and ingest food (eat ‘like animals’), thus contributing to both primary and secondary production simultaneously in the same cell. These protists are termed ‘mixoplankton’, and include many species traditionally labelled as ‘phytoplankton’ (a term now reserved for phototrophic microbes that are incapable of phagocytosis) or labelled as ‘protist zooplankton’ (now reserved for protist plankton incapable of phototrophy). Mixoplankton include various harmful algal species, most likely all the phototrophic dinoflagellates, and even iconic exemplar ‘phytoplankton’ such as coccolithophorids (which can consume bacteria). Like all significant revisions to ecology, the mixoplankton paradigm will take time to mature but to ignore it means that we fail to properly represent plankton ecology in teaching, science, management, and policy. This chapter introduces the mixoplankton functional groups and provides the first insight into the biogeography of these organisms in the Indian Ocean. A first attempt to consider the implications of the mixoplankton paradigm on marine primary productivity and ecology in the Indian Ocean is also given

From webs, loops, shunts, and pumps to microbial multitasking: evolving concepts of marine microbial ecology, the mixoplankton paradigm, and implications for a future ocean

Emerging knowledge of mixoplankton—ubiquitous microbes that employ phototrophy and phagotrophy synergistically in one cell—reshapes our knowledge of the flow of materials and energy, with wide-reaching impacts on marine productivity, biodiversity, and sustainability. Conceptual models of microbial interactions have evolved from food-chains, where carbon-fixing phytoplankton are conceived as being grazed solely by zooplankton that, in turn, support fisheries and higher trophic levels, to microbial webs, loops, and shunts, as knowledge about abundance, activity, and roles of marine microbial organisms—as well as the complexity of their interactions—has increased. In a future world, plankton that depend on a single strategy for acquiring nutrition (photo-autotrophy or phago-heterotrophy) may be disadvantaged with increasing temperatures and ocean acidification impacting vital rates, thermal stratification decreasing water column nutrient exchange, and anthropogenic pollution shifting amounts, forms, and proportions of nutrients. These conditions can lead to stoichiometric imbalances that may promote mixoplanktonic species with an increasing likelihood of harmful blooms. Such changes in plankton species composition alters the interconnectivity of oceanic microbes with direct consequences on biogeochemical cycling, trophic dynamics, and ecosystem services. Here, the implications of the mixoplankton paradigm relative to traditional concepts of microbial oceanography in a globally-changing, anthropogenically-impacted world are explored

Toward a mechanistic understanding of trophic structure: inferences from simulating stable isotope ratios

Stable isotope ratios (SIR) are widely used to estimate food-web trophic levels (TLs). We built systems dynamic N-biomass-based models of different levels of complexity, containing explicit descriptions of isotope fractionation and of trophic level. The values of δ15N and TLs, as independent and emergent properties, were used to test the potential for the SIR of nutrients, primary producers, consumers, and detritus to align with food-web TLs. Our analysis shows that there is no universal relationship between TL and δ15N that permits a robust prognostic tool for configuration of food webs even if all system components can be reliably analysed. The predictive capability is confounded by prior dietary preference, intra-guild predation and recycling of biomass through detritus. These matters affect the dynamics of both the TLs and SIR. While SIR data alone have poor explanatory power, they would be valuable for validating the construction and functioning of dynamic models. This requires construction of coupled system dynamic models that describe bulk elemental distribution with an explicit description of isotope discriminations within and amongst functional groups and nutrient pools, as used here. Only adequately configured models would be able to explain both the bulk elemental distributions and the SIR data. Such an approach would provide a powerful test of the whole model, integrating changing abiotic and biotic events across time and space

Mucus-trap-assisted feeding is a common strategy of the small mixoplanktonic prorocentrum pervagatum and P. cordatum (prorocentrales, dinophyceae)

Prorocentrum comprises a diverse group of bloom-forming dinophytes with a worldwide distribution. Although photosynthetic, mixoplanktonic phagotrophy has also been described. Recently, the small P. cf. balticum was shown to use a remarkable feeding strategy by crafting globular mucus traps to capture and immobilize potential prey. Here we present evidence showing that two additional related species, the recently described P. pervagatum and the cosmopolitan bloom-forming P. cordatum, also produce large (80–120 µm) mucus traps supporting their mixoplanktonic activity. Prey are captured within the traps either through passive entanglement upon contact with the outside surface, or through active water movement created by rotating Prorocentrum cells eddying particles to the inside surface where trapped live prey cells became immobilized. Entrapment in mucus assisted deployment into the prey of a peduncle extruded from the apical area of the Prorocentrum cell. Phagotrophy by P. pervagatum supported faster growth compared to unfed controls and time series quantification of food vacuoles revealed ingestion rates of ca. 10–12 Teleaulax prey cells day−1. Model calculations show clear advantages of deploying a mucus trap for increasing prey encounter rates. This study demonstrates that the large size and immobilization properties of mucus traps successfully increase the availability of prey for small Prorocentrum species, whose peduncle feeding mode impedes consumption of actively moving prey, and that this strategy is common among certain clades of small planktonic Prorocentrum species

Subtle differences in the representation of consumer dynamics have large effects in marine food web models

Projecting ocean biogeochemistry and fisheries resources under climate change requires confidence in simulation models. Core to such models is the description of consumer dynamics relating prey abundance to capture, digestion efficiency and growth rate. Capture is most commonly described as a linear function of prey encounter or by rectangular hyperbola. Most models also describe consumers as eating machines which “live-to-eat,” where growth (μ) is limited by a maximum grazing rate (Gmax). Real consumers can feed much faster than needed to support their maximum growth rate (μmax); with feeding modulated by satiation, they “eat-to-live.” A set of strategic analyses were conducted of these alternative philosophies of prey consumption dynamics and testing of their effects in the StrathE2E end-to-end marine food web and fisheries model. In an experiment where assimilation efficiencies were decreased by 10%, such as might result from a change in temperature or ocean acidity, the different formulation resulted in up to 100% variation in the change in abundances of food web components, especially in the mid-trophic levels. Our analysis points to a need for re-evaluation of some long-accepted principles in consumer-resource modeling

Simulating Effects of Variable Stoichiometry and Temperature on Mixotrophy in the Harmful Dinoflagellate Karlodinium veneficum

Results from a dynamic mathematical model are presented simulating the growth of the harmful algal bloom (HAB) mixotrophic dinoflagellate Karlodinium veneficum and its algal prey, Rhodomonas salina. The model describes carbon-nitrogen-phosphorus-based interactions within the mixotroph, interlinking autotrophic and phagotrophic nutrition. The model was tuned to experimental data from these species grown under autotrophic conditions and in mixed batch cultures in which nitrogen:phosphorus stoichiometry (input molar N:P of 4, 16, and 32) of both predator and prey varied. A good fit was attained to all experimentally derived carbon biomass data. The potential effects of temperature and nutrient changes on promoting growth of prey and thus K. veneficum bloom formation were explored using this simulation platform. The simulated biomass of K. veneficum was highest when they were functioning as mixotrophs and when they consumed prey under elevated N:P conditions. The scenarios under low N:P responded differently, with simulations showing larger deviation between mixotrophic and autotrophic growth, depending on temperature. When inorganic nutrients were in balanced proportions, lower biomass of the mixotroph was attained at all temperatures in the simulations, suggesting that natural systems might be more resilient against Karlodinium HAB development in warming conditions if nutrients were available in balanced proportions. These simulations underscore the need for models of HAB dynamics to include consideration of prey; modeling HAB as autotrophs is insufficient. The simulations also imply that warmer, wetter springs that may bring more N with lower N:P, such as predicted under climate change scenarios for Chesapeake Bay, may be more conducive to development of these HABs. Prey availability may also increase with temperature due to differential growth temperature responses of K. veneficum and its prey