In hot water: Interactions of temperature, nitrogen form and availability and photosynthetic and nitrogen uptake responses in natural Karenia brevis populations.

During 2020-2021, an unusually prolonged bloom of the toxigenic dinoflagellate Karenia brevis persisted for more than 12 months along the Gulf coast of Florida, resulting in severe environmental effects. Motivated by the possibility that unusual nutrient conditions existed during summer 2021, the short-term interactions of temperature, nitrogen (N) forms (ammonium (NH4+), nitrate (NO3-), and urea) and availability on photosynthesis-irradiance responses and N uptake rates were examined in summer 2021 and compared to such responses from the earlier winter. Winter samples were exposed to temperatures of 15, 20, 25, 30 °C while summer samples were incubated at 15, 25, 30, 33 °C, representing the maximum range the cells might experience throughout the water column due to daytime surface heating or extreme weather events. Depending on thermal history of the cells, photosynthetic performance differed when cells were exposed to the same temperature, showing a capacity for thermal acclimation in this species. Although blooms generally do not persist throughout the summer, bloom biomass was remarkably higher in summer than during the winter. However, most of the photosynthetic parameters and N uptake rates, as well as total carbon (C) and N cell-1 were significantly lower in the summer populations, showing that the summer populations were photosynthetically and nutritionally stressed. When the summer cells were treated with urea, however, uptake rates and total C and N cell-1 were higher than with the other N substrates, especially in warmer waters, showing differential thermal responses depending on N forms.

Mixoplankton and mixotrophy: future research priorities.

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.

A three-dimensional mixotrophic model of Karlodinium veneficum blooms for a eutrophic estuary.

Blooms of dinoflagellate Karlodinium veneficum are widely distributed in estuarine and coastal waters and have been found to cause fish kills worldwide. K. veneficum has a mixed nutritional mode and relies on both photosynthesis and phagotrophy for growth; it is a mixotroph. Here, a model of mixotrophic growth of K. veneficum (MIXO) was developed, calibrated with previously-reported laboratory physiological data, and subsequently embedded in a 3D-coupled hydrodynamic (ROMS)-biogeochemical (RCA) model of eutrophic Chesapeake Bay, USA. The resulting ROMS-RCA-MIXO model was applied in hindcast mode to investigate seasonal and spatial distributions. Simulations showed that K. veneficum blooms occurred during June-August and were confined to the upper and middle Bay, consistent with long-term field observations. Autotrophic growth dominated in spring but heterotrophic growth dominated during the summer. The number of prey ingested by K. veneficum varied from 0.1 to 0.6 day-1 and the food vacuole content reached up to 50% of the core mixotroph biomass. The ingestion rate increased with prey density and also when P:N ratio fell below ∼0.03 (N:P ∼ 33), indicating that K. veneficum only switched to mixotrophic feeding in P-deficient waters when sufficient prey were available; this occurred during the summer months. The digestion rate increased with both the food vacuole content and temperature. The modeling analysis affirms K. veneficum as a phagotrophic 'alga' which is primarily photosynthetic but switches to mixotrophic feeding under nutrient deficient conditions.

Seasonal gut contents of the eastern oyster, Crassostrea virginica, in the Rhode River, Chesapeake Bay, USA: Growth, phytoplankton and signature pigment data.

A 2-year study was undertaken to understand feeding preferences of the eastern oyster Crassostrea virginica when growing in conditions of eutrophication and variable flow. Oysters were suspended in the Rhode River, a tributary of Chesapeake Bay, Maryland, USA, and a subset of these oysters was collected monthly, measured in height to determine growth, and the phytoplankton in their gut were examined both microscopically and using indicator pigments and compared with phytoplankton abundance and composition in the water column. The data herein summarize the oyster growth and the gut contents with respect to phytoplankton cell numbers and composition and with respect to signature pigments.

A three-dimensional mechanistic model of Prorocentrum minimum blooms in eutrophic Chesapeake Bay.

Planktonic Prorocentrum, common harmful dinoflagellate, are increasing in frequency, duration, and magnitude globally, as exemplified by the number of blooms of P. minimum in Chesapeake Bay that have nearly doubled over the past 3 decades. Although the dynamics of transport and seasonal occurrence of this species have been previously described, it has been challenging to predict the timing and location of P. minimum blooms in Chesapeake Bay. We developed a new three-dimensional mechanistic model of this species that integrates physics, nutrient cycling and plankton physiology and embedded it within a coupled hydrodynamic-biogeochemical model originally developed for simulating water quality in eutrophic estuarine and coastal waters. Hindcast simulations reproduced the observed time series and spatial distribution of cell density, in particular capturing well its peak in May in the mid-to-upper part of the estuary. Timing and duration of the blooms were mostly determined by the temperature-dependent growth function, while mortality due to grazing and respiration played a minor role. The model also reproduced the pattern of overwintering populations, which are located in bottom waters of the lower Bay, and are transported upstream in spring by estuarine flow. Blooms develop in the mid-upper parts of the estuary when these transported cells encounter high nutrient concentrations from the Susquehanna River and favorable light conditions. Diagnostic analysis and model-sensitivity experiments of nutrient conditions showed that high nitrogen:phosphorus conditions favor bloom development. The model also captured the observed interannual variations in the magnitude and spatial distribution of P. minimum blooms.

From hogs to HABs: impacts of industrial farming in the US on nitrogen and phosphorus and greenhouse gas pollution.

Nutrient pollution and greenhouse gas emissions related to crop agriculture and confined animal feeding operations (CAFOs) in the US have changed substantially in recent years, in amounts and forms. This review is intended to provide a broad view of how nutrient inputs-from fertilizer and CAFOs-as well as atmospheric NH3 and greenhouse gas emissions, are changing regionally within the US and how these changes compare with nutrient inputs from human wastewater. Use of commercial nitrogen (N) fertilizer in the US, which now exceeds 12,000,000 metric tonnes (MT) continues to increase, at a rate of 60,000 MT per year, while that of phosphorus (P) has remained nearly constant over the past decade at around 1,800,000 MT. The number of CAFOs in the US has increased nearly 10% since 2012, driven largely by a near 13% increase in hog production. The annualized inventory of cattle, dairy cows, hogs, broiler chickens and turkeys is approximately 8.7 billion, but CAFOs are highly regionally concentrated by animal sector. Country-wide, N applied by fertilizer is about threefold greater than manure N inputs, but for P these inputs are more comparable. Total manure inputs now exceed 4,000,000 MT as N and 1,400,000 MT as P. For both N and P, inputs and proportions vary widely by US region. The waste from hog and dairy operations is mainly held in open lagoons that contribute to NH3 and greenhouse gas (as CH4 and N2O) emissions. Emissions of NH3 from animal waste in 2019 were estimated at > 4,500,000 MT. Emissions of CH4 from manure management increased 66% from 1990 to 2017 (that from dairy increased 134%, cattle 9.6%, hogs 29% and poultry 3%), while those of N2O increased 34% over the same time period (dairy 15%, cattle 46%, hogs 58%, and poultry 14%). Waste from CAFOs contribute substantially to nutrient pollution when spread on fields, often at higher N and P application rates than those of commercial fertilizer. Managing the runoff associated with fertilizer use has improved with best management practices, but reducing the growing waste from CAFO operations is essential if eutrophication and its effects on fresh and marine waters-namely hypoxia and harmful algal blooms (HABs)-are to be reduced.

Climate-induced interannual variability and projected change of two harmful algal bloom taxa in Chesapeake Bay, USA.

Retrospective analysis of water quality monitoring data reveals strong interannual shifts in the spatial distribution of two harmful algal species (Prorocentrum minimum and Karlodinium veneficum) in eutrophic Chesapeake Bay. A habitat model, based on the temperature and salinity tolerance of the two species as well as their nutrient preferences, provides a good interpretation for the observed seasonal progression and spatial distribution of these taxa. It also points to climate-induced variability in the hydrological forcing as a mechanism driving the interannual shifts in the algal distributions: both P. minimum and K. veneficum shift downstream during wetter years but upstream during dry years. Climate downscaling simulations using the habitat model show upstream shifts of the two species in the estuary and longer blooming seasons by the mid-21st century. Salt intrusion due to sea level rise will raise salinity in the estuary and cause these HAB species to migrate upstream, but increasing winter-spring flows may also drive favorable salinity habitat downstream. Warming leads to longer growing seasons of P. minimum and K. veneficum but may suppress bloom habitat during their respective peak bloom periods.

Effect of allelochemicals on photosynthetic and antioxidant defense system of Ulva prolifera.

Ulva prolifera is a macroalgae that forms massive blooms, negatively impacting natural communities, aquaculture operations and recreation. The effects of the natural products, eugenol, ß-myrcene, citral and nonanoic acid on the growth rate, antioxidative defense system and photosynthesis of Ulva prolifera were investigated as a possible control strategy for this harmful taxon. Negative effects on growth were observed with all four chemicals, due to the excessive production of reactive oxygen species and oxidative damage to the thalli. However, the response of U. prolifera under the four chemicals stress was different at the cellular level. ß-myrcene, the most effective compound in terms of growth inhibition, induced oxidative stress as shown by the damage of total antioxidant capacity (T-AOC) and the downregulation of the glutathione-ascorbate (GSH-ASA) cycle which inhibited the antioxidative system. This chemical also inhibited photosynthesis and photoprotection mechanisms in U. prolifera, resulting in growth limitation. In contrast, U. prolifera was less affected by the second tested chemical, eugenol, and showed no significant change on photosynthetic efficiency in the presence of the chemical. The inhibition effects of the third and fourth tested chemicals, nonanoic acid and citralon, on growth and on the antioxidant defense system in U. prolifera were inferior. These results provide a potential avenue for controlling green tides in the future.

Harmful algae at the complex nexus of eutrophication and climate change.

Climate projections suggest-with substantial certainty-that global warming >1.5 °C will occur by mid-century (2050). Population is also projected to increase, amplifying the demands for food, fuel, water and sanitation, which, in turn, escalate nutrient pollution. Global projections of nutrient pollution, however, are less certain than those of climate as there are regionally decreasing trends projected in Europe, and stabilization of nutrient use in North America and Australia. In this review of the effects of eutrophication and climate on harmful algae, some of the complex, subtle, and non-intuitive effects and interactions on the physiology of both harmful and non-harmful taxa are emphasized. In a future ocean, non-harmful diatoms may be disproportionately stressed and mixotrophs advantaged due to changing nutrient stoichiometry and forms of nutrients, temperature, stratification and oceanic pH. Modeling is advancing, but there is much yet to be understood, in terms of physiology, biogeochemistry and trophodynamics and how both harmful and nonharmful taxa may change in an uncertain future driven by anthropogenic activities.

Distribution and potential toxicity of benthic harmful dinoflagellates in waters of Florida Bay and the Florida Keys.

Few studies have been carried out on benthic dinoflagellates along the Florida Keys, and little is known about their distribution or toxicity in Florida Bay. Here, the distribution and abundance of benthic dinoflagellates was explored in northern and eastern Florida Bay and along the bay and ocean sides of the Florida Keys. Isolates were brought into culture and their toxicity was tested with oyster larvae bioassays. Seven genera were detected, including Prorocentrum, Coolia, Ostreopsis, Amphidinium, Gambierdiscus, Fukuyoa (all included potentially toxic species) and Sinophysis. In general, distribution increased with water temperature and nutrient availability, especially that of phosphate. This study documented the first record of Coolia santacroce in the Florida Keys. Potential toxic effects of Gambierdiscus caribaeus, the abundance of which exceeded 1000 cells g-1 fw at some sites, were established using oyster larvae as a bioassay organism. These findings suggest a potential risk of ciguatera fish poisoning in this area.

Chesapeake Bay's "forgotten" Anacostia River: eutrophication and nutrient reduction measures.

The Anacostia River, a Chesapeake Bay tributary running through Washington, D.C., is small but highly polluted with nutrients and contaminants. There is currently a multi-billion dollar tunnel project underway, being built in several phases, aimed at diverting effluent to sewage treatment, especially during high flow periods, and improving water quality of the Anacostia and the river into which it flows, the Potomac. Here, 4 years of biweekly to monthly nutrient and phytoplankton data are analyzed to assess pre-tunnel eutrophication status and relationships to flow conditions. Under all flow conditions, nutrients prior to tunnel implementation were well in excess of values normally taken to be limiting for growth, and hypoxia was apparent during summer. Chlorophyll a was higher in summer (averaging 26.9 µg L-1) than in spring (averaging 14.8 µg L-1), and based on pigment composition, summer communities had proportionately more cyanobacteria (> 2-fold higher zeaxanthin to chlorophyll a ratios) compared to spring, which had proportionately more diatoms (> 2-fold higher fucoxanthin to chlorophyll a ratios). When all data from all years and sites were considered, there was a decrease in diatoms and increase in cyanobacteria with decreasing NO3- and increasing NH4+ concentrations, increasing ratios of NH4+ to NO3-, and increasing temperature. Tunnel implementation and associated nutrient reductions may reduce the severity of summer blooms but reductions of spring assemblages may be even greater because river flows are typically higher at that time of year.

Time series models of decadal trends in the harmful algal species Karlodinium veneficum in Chesapeake Bay.

The harmful dinoflagellate, Karlodnium veneficum, has been implicated in fish-kill and other toxic, harmful algal bloom (HAB) events in waters worldwide. Blooms of K. veneficum are known to be related to coastal nutrient enrichment but the relationship is complex because this HAB taxon relies not only on dissolved nutrients but also particulate prey, both of which have also changed over time. Here, applying cross-correlations of climate-related physical factors, nutrients and prey, with abundance of K. veneficum over a 10-year (2002-2011) period, a synthesis of the interactive effects of multiple factors on this species was developed for Chesapeake Bay, where blooms of the HAB have been increasing. Significant upward trends in the time series of K. veneficum were observed in the mesohaline stations of the Bay, but not in oligohaline tributary stations. For the mesohaline regions, riverine sources of nutrients with seasonal lags, together with particulate prey with zero lag, explained 15%-46% of the variation in the K. veneficum time series. For the oligohaline regions, nutrients and particulate prey generally showed significant decreasing trends with time, likely a reflection of nutrient reduction efforts. A conceptual model of mid-Bay blooms is presented, in which K. veneficum, derived from the oceanic end member of the Bay, may experience enhanced growth if it encounters prey originating from the tributaries with different patterns of nutrient loading and which are enriched in nitrogen. For all correlation models developed herein, prey abundance was a primary factor in predicting K. veneficum abundance.

Effects of prey of different nutrient quality on elemental nutrient budgets in Noctiluca scintillans.

Noctiluca scintillans (Noctiluca) is a cosmopolitan red tide forming heterotrophic dinoflagellate. In this study, we investigated its ingestion, elemental growth yield and excretion when supplied with different quality food (nutrient-balanced, N-limited and P-limited). Total cellular elemental ratios of Noctiluca were nearly homeostatic, but the ratio of its intracellular NH4+ and PO43- was weakly regulated. Noctiluca thus seems able to differentially allocate N and P to organic and inorganic pools to maintain overall homeostasis, and it regulated its internal N more strongly and efficiently than P. The latter was substantiated by its comparatively stable C:N ratio and compensatory feeding on N-limited prey. Using both starvation experiments and mass balance models, it was found that excretion of C, N, and P by Noctiluca is highly affected by prey nutritional quality. However, based on modeling results, nutrients seem efficiently retained in actively feeding Noctiluca for reproduction rather than directly released as was shown experimentally in starved cells. Moreover, actively feeding Noctiluca tend to retain P and preferentially release N, highlighting its susceptible to P-limitation. Recycling of N and P by Noctiluca may supply substantial nutrients for phytoplankton growth, especially following bloom senescence.

Bridging Food Webs, Ecosystem Metabolism, and Biogeochemistry Using Ecological Stoichiometry Theory.

Although aquatic ecologists and biogeochemists are well aware of the crucial importance of ecosystem functions, i.e., how biota drive biogeochemical processes and vice-versa, linking these fields in conceptual models is still uncommon. Attempts to explain the variability in elemental cycling consequently miss an important biological component and thereby impede a comprehensive understanding of the underlying processes governing energy and matter flow and transformation. The fate of multiple chemical elements in ecosystems is strongly linked by biotic demand and uptake; thus, considering elemental stoichiometry is important for both biogeochemical and ecological research. Nonetheless, assessments of ecological stoichiometry (ES) often focus on the elemental content of biota rather than taking a more holistic view by examining both elemental pools and fluxes (e.g., organismal stoichiometry and ecosystem process rates). ES theory holds the promise to be a unifying concept to link across hierarchical scales of patterns and processes in ecology, but this has not been fully achieved. Therefore, we propose connecting the expertise of aquatic ecologists and biogeochemists with ES theory as a common currency to connect food webs, ecosystem metabolism, and biogeochemistry, as they are inherently concatenated by the transfer of carbon, nitrogen, and phosphorous through biotic and abiotic nutrient transformation and fluxes. Several new studies exist that demonstrate the connections between food web ecology, biogeochemistry, and ecosystem metabolism. In addition to a general introduction into the topic, this paper presents examples of how these fields can be combined with a focus on ES. In this review, a series of concepts have guided the discussion: (1) changing biogeochemistry affects trophic interactions and ecosystem processes by altering the elemental ratios of key species and assemblages; (2) changing trophic dynamics influences the transformation and fluxes of matter across environmental boundaries; (3) changing ecosystem metabolism will alter the chemical diversity of the non-living environment. Finally, we propose that using ES to link nutrient cycling, trophic dynamics, and ecosystem metabolism would allow for a more holistic understanding of ecosystem functions in a changing environment.

Rates of nitrogen uptake by cyanobacterially-dominated assemblages in Lake Taihu, China, during late summer.

Lake Taihu has suffered an increasing number of cyanobacteria harmful algal blooms (CyanoHABs) over the past three decades, bringing about formidable ecological and economical losses. Efforts to control phosphate (P) and/or nitrogen (N) have been applied to mitigate these blooms, but there has been much less attention paid to N and its different forms on the ecology of the blooms. Therefore, kinetic and nutrient enrichment experiments were conducted to assess N uptake rates under differing conditions, and to examine effects of changes in N forms (NH4+, NO3- and urea) and P availability on phytoplankton community physiology. In 2014 these experiments involved mesocosm enrichments; in 2015 these experiments were conducted over a diurnal period. Both involved measurements of short-term N uptake. The kinetic results showed that the utilization of NH4+, NO3- and urea by Microcystis-dominated communities was not efficient at low ambient substrate concentrations. Maximum uptake rates by these phytoplankton was achieved on NH4+ and these rates were significantly higher than those on NO3- or urea with or without nutrient pretreatment. Moreover in the presence of PO43- enrichment, the maximal uptake velocity of NH4+ substantially increased without evidence of saturation. High amounts of NH4+ may have inhibited or repressed the uptake of NO3- at certain times in these studies. In the diurnal study, dissolved inorganic carbon and pH changed substantially throughout the day. The resulting high pH altered N and P in ways that may help to sustain nutrient cycling for the blooms.

Eutrophication, harmful algae and biodiversity - Challenging paradigms in a world of complex nutrient changes.

Eutrophication is a complex process and often associated with not only a change in overall algal biomass but also with a change in biodiversity. Common metrics of eutrophication (e.g., chlorophyll a), total nitrogen (TN) and phosphorus (TP) are not adequate for understanding biodiversity changes, especially those associated with harmful algal bloom (HAB) proliferations. Harmful algae can increase disproportionately with eutrophication, depending on which nutrients change and in what proportion. This paper challenges several classic paradigms in our understanding of eutrophication and associated biodiversity changes. The underlying message is that nutrient proportions and forms can alter biodiversity, even when nutrients are at concentrations in excess of those considered limiting. The global HAB problem is on a trajectory for more blooms, more toxins, more often, in more places. Our approach to management of HABs and eutrophication must consider the broader complexity of nutrient effects at scales ranging from physiological to ecological.

Nitrogen dynamics and phytoplankton community structure: the role of organic nutrients.

Dissolved organic nitrogen (DON) is recognised as an important N source for phytoplankton. However, its relative importance for phytoplankton nutrition and community composition has not been studied comprehensively. This study, conducted in a typical Scottish fjord, representative of near-pristine coastal environments, evaluates the utilisation of DON and dissolved inorganic nitrogen (DIN) by different microbial size fractions and the relationship of phytoplankton community composition with DON and other parameters. The study demonstrated that DON was important in supporting phytoplankton throughout the yearly production cycle. The higher-than-expected urea uptake rates and large fraction of the spring bloom production supported by DON suggested that organic N not only contributes to regenerated production and to the nutrition of the small phytoplankton fraction, but can also contribute substantially to new production of the larger phytoplankton in coastal waters. Multivariate statistical techniques revealed two phytoplankton assemblages with peaks in abundance at different times of the year: a spring group dominated by Skeletonema spp., Thalassiosira spp., and Pseudo-nitzschia spp. group delicatissima; and a summer/autumn group dominated by Chaetoceros spp., Scrippsiella spp., and Pseudo-nitzschia spp. group seriata. The multivariate pattern in community composition and abundance of these taxa was significantly correlated with the multivariate pattern of DON, urea, dissolved free amino acids, DIN, temperature, salinity, and daylength, with daylength and urea being particularly important, suggesting both physical and chemical controls on community composition.

Defining Planktonic Protist Functional Groups on Mechanisms for Energy and Nutrient Acquisition: Incorporation of Diverse Mixotrophic Strategies.

Arranging organisms into functional groups aids ecological research by grouping organisms (irrespective of phylogenetic origin) that interact with environmental factors in similar ways. Planktonic protists traditionally have been split between photoautotrophic "phytoplankton" and phagotrophic "microzooplankton". However, there is a growing recognition of the importance of mixotrophy in euphotic aquatic systems, where many protists often combine photoautotrophic and phagotrophic modes of nutrition. Such organisms do not align with the traditional dichotomy of phytoplankton and microzooplankton. To reflect this understanding, we propose a new functional grouping of planktonic protists in an eco-physiological context: (i) phagoheterotrophs lacking phototrophic capacity, (ii) photoautotrophs lacking phagotrophic capacity, (iii) constitutive mixotrophs (CMs) as phagotrophs with an inherent capacity for phototrophy, and (iv) non-constitutive mixotrophs (NCMs) that acquire their phototrophic capacity by ingesting specific (SNCM) or general non-specific (GNCM) prey. For the first time, we incorporate these functional groups within a foodweb structure and show, using model outputs, that there is scope for significant changes in trophic dynamics depending on the protist functional type description. Accordingly, to better reflect the role of mixotrophy, we recommend that as important tools for explanatory and predictive research, aquatic food-web and biogeochemical models need to redefine the protist groups within their frameworks.

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.

Margalef revisited: A new phytoplankton mandala incorporating twelve dimensions, including nutritional physiology.

Building on the classic depiction of the progression from a diatom to a dinoflagellate bloom as a function of nutrients and turbulence, known as the "Margalef mandala", a new conceptual model or mandala is presented here. The new mandala maps twelve response or effects traits, or environmental characteristics, related to different phytoplankton functional types: (1) relative preference for chemically reduced vs chemically oxidized forms of nitrogen; (2) relative availability of inorganic nitrogen and phosphorus; (3) adaptation to high vs low light and the tendency to be autotrophic vs mixotrophic; (4) cell motility; (5) environmental turbulence; (6) pigmentation quality; (7) temperature; (8) cell size; (9) relative growth rate; (10) relative production of bioactive compounds such as toxins or reactive oxygen species (ROS); (11) r vs K strategy; and (12) fate of the production in terms of grazing. The new mandala serves to highlight the differences and trade-offs between traits and/or environmental conditions, and illustrates some traits tend to track each other, a concept that may be helpful in trait-based modeling approaches and in understanding environmental factors associated with harmful algal blooms. It is hoped that this new mandala captures some of our recent insight into phytoplankton physiology and functional traits, and has contemporary relevance in light of anthropogenic changes in nutrient form and ratio.