Phytoplankton Stoichiometry Research Articles

Correction to: Phytoplankton stoichiometry along the salinity gradient under limited nutrient and light supply

Correction to: Phytoplankton stoichiometry along the salinity gradient under limited nutrient and light supply

Different phytoplankton stoichiometry and nutrient status in the reservoirs of Fujian Province, China

Different phytoplankton stoichiometry and nutrient status in the reservoirs of Fujian Province, China

Direct and indirect cumulative effects of temperature, nutrients, and light on phytoplankton growth.

Temperature and resource availability are pivotal factors influencing phytoplankton community structures. Numerous prior studies demonstrated their significant influence on phytoplankton stoichiometry, cell size, and growth rates. The growth rate, serving as a reflection of an organism's success within its environment, is linked to stoichiometry and cell size. Consequently, alterations in abiotic conditions affecting cell size or stoichiometry also exert indirect effects on growth. However, such results have their limitations, as most studies used a limited number of factors and factor levels which gives us limited insights into how phytoplankton respond to environmental conditions, directly and indirectly. Here, we tested for the generality of patterns found in other studies, using a combined multiple-factor gradient design and two single species with different size characteristics. We used a structural equation model (SEM) that allowed us to investigate the direct cumulative effects of temperature and resource availability (i.e., light, N and P) on phytoplankton growth, as well as their indirect effects on growth through changes in cell size and cell stoichiometry. Our results mostly support the results reported in previous research thus some effects can be identified as dominant effects. We identified rising temperature as the dominant driver for cell size reduction and increase in growth, and nutrient availability (i.e., N and P) as dominant factor for changes in cellular stoichiometry. However, indirect effects of temperature and resources (i.e., light and nutrients) on species' growth rates through cell size and cell stoichiometry differed across the two species suggesting different strategies to acclimate to its environment.

Total alkalinity change: The perspective of phytoplankton stoichiometry

AbstractMany biogeochemical processes change total alkalinity: this has been reported for carbonate precipitation and dissolution, uptake and release of various nitrogen‐containing compounds, uptake of phosphate, sulfate reduction combined with methane oxidation. However, the list is not exhaustive. Here we discuss additional processes, namely the uptake of Mg, K, Ca by phytoplankton, and calculate their contribution based on the explicit conservative expression for TA and an extended (compared to Redfield's C : N : P) stoichiometry of phytoplankton. These additional contributions are of the same order of magnitude as that of phosphate uptake and thus much smaller than the contribution from nitrate uptake and of opposite sign to the contribution by nitrate and phosphate uptake.

Phytoplankton stoichiometry along the salinity gradient under limited nutrient and light supply.

Ongoing climate warming alters precipitation and water column stability, leading to salinity and nutrient supply changes in the euphotic zone of many coastal ecosystems and semi-enclosed seas. Changing salinity and nutrient conditions affect phytoplankton physiology by altering elemental ratios of carbon (C), nitrogen (N) and phosphorus (P). This study aimed to understand how salinity stress and resource acquisition affect phytoplankton stoichiometry. We incubated a phytoplankton polyculture composed of 10 species under different light, inorganic nutrient ratio and salinity levels. At the end of the incubation period, we measured particulate elemental composition (C, N and P), chlorophyll a and species abundances. The phytoplankton polyculture, dominated by Phaeodactylum tricornutum, accumulated more particulate organic carbon (POC) with increasing salinity. The low POC and low particulate C:N and C:P ratios toward 0psu suggest that the hypoosmotic conditions highly affected primary production. The relative abundance of different species varied with salinity, and some species grew faster under low nutrient supply. Still, the dominant diatom regulated the overall POC of the polyculture, following the classic concept of the foundation species.

Impact of Dynamic Phytoplankton Stoichiometry on Global Scale Patterns of Nutrient Limitation, Nitrogen Fixation, and Carbon Export

AbstractPhytoplankton stoichiometry modulates the interaction between carbon, nitrogen and phosphorus cycles. Environmentally driven variations in phytoplankton C:N:P can alter biogeochemical cycling compared to expectations under fixed ratios. In fact, the assumption of fixed C:N:P has been linked to Earth System Model (ESM) biases and potential misrepresentation of responses to future change. Here we integrate key elements of the Adaptive Trait Optimization Model (ATOM) for phytoplankton stoichiometry with the Carbon, Ocean Biogeochemistry and Lower Trophics (COBALT) ocean biogeochemical model. Within a series of global ocean‐ice‐ecosystem retrospective simulations, ATOM‐COBALT reproduced observations of phytoplankton N:P, and compared to static ratios, exhibited reduced phytoplankton P‐limitation, enhanced N‐fixation, and increased low‐latitude export, improving consistency with observations and highlighting the biogeochemical implications of dynamic N:P. We applied ATOM‐COBALT to explore the impacts of different physiological mechanisms hypothesized to underlie N:P variation, finding that two mechanisms together drove the observed patterns: proportionality of P‐rich ribosomes in phytoplankton cells to growth rates and reductions in P‐storage during scarcity. A third mechanism which linked temperature with phytoplankton biomass allocations to non‐ribosomal proteins, led only to relatively modest impacts because this mechanism decreased the temperature dependence of phytoplankton growth rates, compensating for changes in N:P. We find that there are quantitative response differences that associate distinctive biogeochemical footprints with each mechanism, which are most apparent in highly productive low‐latitude regions. These results suggest that variable phytoplankton N:P makes phytoplankton productivity and export resilient to environmental changes, and support further research on the physiological and environmental drivers of phytoplankton stoichiometry and biogeochemical role.

Integrating Trait‐Based Stoichiometry in a Biogeochemical Inverse Model Reveals Links Between Phytoplankton Physiology and Global Carbon Export

AbstractThe elemental ratios of carbon, nitrogen, and phosphorus (C:N:P) within organic matter play a key role in coupling biogeochemical cycles in the global ocean. At the cellular level, these ratios are controlled by physiological responses to the environment. But linking these cellular‐level processes to global biogeochemical cycles remains challenging. We present a novel model framework that combines knowledge of phytoplankton cellular functioning with global scale hydrographic data, to assess the role of variable carbon‐to‐phosphorus ratios (RC:P) on the distribution of export production. We implement a trait‐based mechanistic model of phytoplankton growth into a global biogeochemical inverse model to predict global patterns of phytoplankton physiology and stoichiometry that are consistent with both biological growth mechanisms and hydrographic carbon and nutrient observations. We compare this model to empirical parameterizations relating RC:P to temperature or phosphate concentration. We find that the way the model represents variable stoichiometry affects the magnitude and spatial pattern of carbon export, with globally integrated fluxes varying by up to 10% (1.3 Pg C yr−1) across models. Despite these differences, all models exhibit strong consistency with observed dissolved inorganic carbon and phosphate concentrations (R2 > 0.9), underscoring the challenge of selecting the most accurate model structure. We also find that the choice of parameterization impacts the capacity of changing RC:P to buffer predicted export declines. Our novel framework offers a pathway by which additional biological information might be used to reduce the structural uncertainty in model representations of phytoplankton stoichiometry, potentially improving our capacity to project future changes.

Elemental stoichiometry of the key calcifying marine phytoplankton Emiliania huxleyi under ocean climate change: A meta-analysis.

The elemental composition of marine microorganisms (their C:N:P ratio, or stoichiometry) is central to understanding the biotic and biogeochemical processes underlying key marine ecosystem functions. Phytoplankton C:N:P is species specific and flexible to changing environmental conditions. However, bulk or fixed phytoplankton stoichiometry is usually assumed in biogeochemical and ecological models because more realistic, environmentally responsive C:N:P ratios have yet to be defined for key functional groups. Here, a comprehensive meta-analysis of experimental laboratory data reveals the variable C:N:P stoichiometry of Emiliania huxleyi, a globally significant calcifying phytoplankton species. Mean C:N:P of E. huxleyi is 124C:16N:1P under control conditions (i.e. growth not limited by one or more environmental stressors) and shows a range of responses to changes in nutrient and light availability, temperature and pCO2 . Macronutrient limitation caused strong shifts in stoichiometry, increasing N:P and C:P under P deficiency (by 305% and 493% respectively) and doubling C:N under N deficiency. Responses to light, temperature and pCO2 were mixed but typically shifted cellular elemental content and C:N:P stoichiometry by ca. 30% or less. Besides these independent effects, the interactive effects of multiple environmental changes on E. huxleyi stoichiometry under future ocean conditions could be additive, synergistic or antagonistic. To synthesise our meta-analysis results, we explored how the cellular elemental content and C:N:P stoichiometry of E. huxleyi may respond to two hypothetical future ocean scenarios (increased temperature, irradiance and pCO2 combined with either N deficiency or P deficiency) if an additive effect is assumed. Both future scenarios indicate decreased calcification (which is predominantly sensitive to elevated pCO2 ), increased C:N, and up to fourfold shifts in C:P and N:P. Our results strongly suggest that climate change will significantly alter the role of E. huxleyi (and potentially other calcifying phytoplankton species) in marine biogeochemical processes.

Interactive effects of nitrogen and phosphorus on growth and stoichiometry of lake phytoplankton

AbstractPhytoplankton responses to nutrient enrichment are often assumed to be universal, but in practice they can significantly vary because the effect size to an increased supply of one nutrient may depend on the availability of the other. Here, we used two complementary two‐way factorial experiments to determine how responses of lake phytoplankton to increased N and P supply vary with increasing concentrations of the other nutrient. We manipulated dissolved N and P concentrations in a 4‐d bioassay conducted with lake phytoplankton and measured/determined chlorophyllaand carbon (C)‐specific growth rates, phytoplankton size‐classes, chlorophyll‐specific N and P removal, and seston C : N : P ratios. These data were used to assess the presence and type of interactive effects between N and P on phytoplankton. For most response variables, the effects of increased N supply depended on the background concentration of P and vice versa. The specific nature of effects differed among response variables and depended on the N and P concentrations present in the bioassay. Generally, increases of N or P alone elicited few and weaker effects than increasing the supply of one element in combination with the other. Overall, our results show that phytoplankton responses to increased N or P supplies are context dependent and likely reflect multiple processes involved in nutrient uptake and use. These results also show that phytoplankton responses to N and P supply ratios can depend on the supply rate of the other nutrient, which complicates understanding how single nutrient enrichment affects lake phytoplankton producers.

Imbalanced phytoplankton C, N, P and its relationship with seawater nutrients in Xiamen Bay, China

Anthropogenic activities dramatically alter biogeochemical cycling and stoichiometry of carbon (C), nitrogen (N), and phosphorus (P) within coastal marine ecosystems. Long-term nutrient input has led to significant deviation of the C, N and P stoichiometry of phytoplankton (C167N28P1) and surface seawater (C1299N24P1) from the Redfield ratio (C106N16P1), and overall P-limitation in Xiamen Bay. The bio-P in phytoplankton was spatially consistent with that of inorganic P in seawater; and the phytoplankton bio-C:N:P shifted towards the same trend as the seawater under prolonged nutrient stress, as one of the cascade effects of the imbalanced seawater elemental stoichiometry on the species composition and abundance, and in turn on bio-elemental stoichiometry, of phytoplankton community. It is suggested that the significant deviations in elemental stoichiometry of primary producers might impair their capacity of nutrient supply for organisms at higher trophic-levels of the food chains in the local coastal ecosystem and thus damage its health.

Copepod Feeding Responses to Changes in Coccolithophore Size and Carbon Content

Phytoplankton stoichiometry and cell size could result from both phenology and environmental change. Zooplankton graze on primary producers, and this drives both the balance of the ecosystem and the biogeochemical cycles. In this study, we performed incubations with copepods and coccolithophores including different prey sizes and particulate carbon contents by considering phytoplankton biovolume concentration instead of chlorophyll a level (Chl a) as is usually performed in such studies. The egestion of fecal pellet and ingestion rates were estimated based on a gut fluorescence method. The latter was calibrated through the relationship between prey Chl a level and the biovolume of the cell. Chl a/biovolume ratio in phytopkanton has to be considered in the copepod gut fluorescent content method. Both coccolithophore biovolume and particulate inorganic/organic carbon ratios affect the food foraging by copepods. Finally, we observed a non-linear relationship between ingestion rates and fecal pellet egestion, due to the presence of calcite inside the copepod’s gut. These results illustrate that both prey size and stoichiometry need to be considered in copepod feeding dynamics, specifically regarding the process leading to the formation of fecal pellets.

Seasonal Water Mass Evolution and Non-Redfield Dynamics Enhance CO2 Uptake in the Chukchi Sea.

The Chukchi Sea is an increasing CO2 sink driven by rapid climate changes. Understanding the seasonal variation of air-sea CO2 exchange and the underlying mechanisms of biogeochemical dynamics is important for predicting impacts of climate change on and feedbacks by the ocean. Here, we present a unique data set of underway sea surface partial pressure of CO2 (pCO2) and discrete samples of biogeochemical properties collected in five consecutive cruises in 2014 and examine the seasonal variations in air-sea CO2 flux and net community production (NCP). We found that thermal and non-thermal effects have different impacts on sea surface pCO2 and thus the air-sea CO2 flux in different water masses. The Bering summer water combined with meltwater has a significantly greater atmospheric CO2 uptake potential than that of the Alaskan Coastal Water in the southern Chukchi Sea in summer, due to stronger biological CO2 removal and a weaker thermal effect. By analyzing the seasonal drawdown of dissolved inorganic carbon (DIC) and nutrients, we found that DIC-based NCP was higher than nitrate-based NCP by 66%-84% and attributable to partially decoupled C and N uptake because of a variable phytoplankton stoichiometry. A box model with a non-Redfield C:N uptake ratio can adequately reproduce observed pCO2 and DIC, which reveals that, during the intensive growing season (late spring to early summer), 30%-46% CO2 uptake in the Chukchi Sea was supported by a flexible stoichiometry of phytoplankton. These findings have important ramification for forecasting the responses of CO2 uptake of the Chukchi ecosystem to climate change.

Estimating phytoplankton stoichiometry from routinely collected monitoring data.

Accurately estimating the elemental stoichiometry of phytoplankton is critical for understanding biogeochemical cycles. In laboratory experiments, stoichiometric ratios vary among species and with changes in environmental conditions. Field observations of total phosphorus (P) and total nitrogen (N) collected at regional and national scales can supplement and expand insights into factors influencing phytoplankton stoichiometry, but analyses applied to these data can introduce biases that affect interpretations of the observed patterns. We introduce an analytical approach for estimating the ratio between phytoplankton N and P from the particulate fraction of nutrient pools in lake samples. We use Bayesian models to represent observations of particulate P and N as the sum of contributions from nutrients bound within phytoplankton and nutrients associated with non-phytoplankton suspended sediment. Application of this approach to particulate nutrient data collected in Missouri impoundments yields estimates of the mass ratio of N:P in phytoplankton ranging from 8-10 across a variety of lakes and seasons. N:P in particulate matter ranged from 6 to 70, a variability driven by differences in nutrients bound to non-phytoplankton suspended sediment. We adapted the Bayesian models to estimate N:P using more commonly available measurements of total P and total N and applied this model to a continental-scale monitoring data set. We compared phytoplankton nutrient content estimated from the two analyses and found that when datasets lack direct measurements of particulate nutrient concentrations, the model estimate of phytoplankton nutrient content includes contributions from nutrients within phytoplankton and dissolved nutrients that are associated with changes in phytoplankton biomass.

Physiological and metabolic effects of glyphosate as the sole P source on a cosmopolitan phytoplankter and biogeochemical implications

Nutrient conditions influence the physiology and stoichiometry of marine phytoplankton. While extensive studies have documented the effects of abundances and types of nutrients such as nitrogen (N) and phosphorus (P), the effect of phosphonates as a P source is less understood and underexplored. Here, with the cosmopolitan coccolithophorid Emiliania huxleyi as a model phytoplankter, we investigated the effect of the phosphonate type of herbicide glyphosate as the sole P source in comparison with the P-depleted and P-replete (with 36 μM dissolved inorganic phosphate [DIP]) cultures. We measured changes in cellular C (carbon):P and N:P ratios and physiological performance and documented the corresponding transcriptomic and miRNAomic responses in E. huxleyi to glyphosate treatment. We found that glyphosate supported population growth but not to the full scale relative to DIP, and this was under the concerted regulation of DNA replication and cell cycle arrest genes as well as the growth-regulating miRNA. Furthermore, our data suggest that E. huxleyi took up glyphosate directly, bypassing extracellular hydrolysis, and this involved ABC transporters. Meanwhile, glyphosate-grown cultures displayed marked increases in cellular particulate organic C (POC) and PON contents, cell size, and transcription of genes for CO2 fixation and citrate cycle, nitrate transport, and protein biosynthesis. However, compared to DIP, the maximum absorption rate of glyphosate was only 33%, and glyphosate-grown E. huxleyi cells exhibited a mild P-stress symptom and elevated cellular C:P and N:P ratios. Interestingly, glyphosate-grown cells showed an increased sinking rate, suggesting that glyphosate as the sole P source might enhance the efficiency of C export by E. huxleyi, which would compensate for the expected decline in primary productivity (and hence carbon efflux) in the future more nutrient-depleted ocean. This biogeochemical implication needs to be further studied and verified, however.

Differential effects of elevated pCO2 and warming on marine phytoplankton stoichiometry

AbstractPhytoplankton stand at the base of the marine food‐web, and play a major role in global carbon cycling. Rising CO2 levels and temperatures are expected to enhance growth and alter carbon:nutrient stoichiometry of marine phytoplankton, with possible consequences for the functioning of marine food‐webs and the oceanic carbon pump. To date, however, the consistency of phytoplankton stoichiometric responses remains unclear. We therefore performed a meta‐analysis on data from experimental studies on stoichiometric responses of marine phytoplankton to elevated pCO2 and 3–5° warming under nutrient replete and limited conditions. Our results demonstrate that elevated pCO2 increased overall phytoplankton C:N (by 4%) and C:P (by 9%) molar ratios under nutrient replete conditions, as well as phytoplankton growth rates (by 6%). Nutrient limitation amplified the CO2 effect on C:N and C:P ratios, with increases to 27% and 17%, respectively. In contrast to elevated pCO2, warming did not consistently alter phytoplankton elemental composition. This could be attributed to species‐ and study‐specific increases and decreases in stoichiometry in response to warming. While our observed moderate CO2‐driven changes in stoichiometry are not likely to drive marked changes in food web functioning, they are in the same order of magnitude as current and projected estimations of oceanic carbon export. Therefore, our results may indicate a stoichiometric compensation mechanism for reduced oceanic carbon export due to declining primary production in the near future.

Phytoplankton antioxidant systems and their contributions to cellular elemental stoichiometry

AbstractOxidative stress plays a role in many aspects of cellular metabolism, and as a result, antioxidants have the potential to impact cellular stoichiometry and biogeochemical cycles. We reviewed how antioxidant systems influence macronutrient and micronutrient stoichiometry in marine phytoplankton and identified that antioxidant systems have important implications for micronutrient stoichiometry. By leveraging diatom proteomic data, we empirically estimated the level of micronutrient quota variation that can be attributed to antioxidant systems. Fe‐containing antioxidant expression may contribute to 3.3–10 μmol : mol variation in Fe : C, and superoxide dismutases appear to be important contributors to variation in Mn, Ni, Zn, and Cu quotas in phytoplankton. Critical next steps for the study of phytoplankton antioxidant systems are to (1) distinguish between oxidative stress and redox‐based gene regulation and (2) determine how antioxidants influence variation or consistency in micronutrient quotas under various environmental conditions.

Environmental control of marine phytoplankton stoichiometry in the North Atlantic Ocean

The stoichiometric coupling of carbon to limiting nutrients in marine phytoplankton regulates the magnitude of biological carbon sequestration in the ocean. While clear links between plankton C:N ratios and environmental drivers have been identified, the nature and direction of these links, as well as their underlying physiological and ecological controls, remain uncertain. We show, with a well-constrained mechanistic model of plankton ecophysiology, that while nitrogen availability and temperature emerge as the main drivers of phytoplankton C:N stoichiometry in the North Atlantic, the biological mechanisms involved vary depending on the spatiotemporal scale and region considered. We find that phytoplankton C:N stoichiometry is overall controlled by nitrogen availability below 40° N, predominantly driven by ecoevolutionary shifts in the functional composition of the phytoplankton communities, while phytoplankton stoichiometric plasticity in response to dropping temperatures and increased grazing pressure dominates at higher latitudes. Our findings highlight the potential of "organisms-to-ecosystems" modeling approaches based on mechanistic models of plankton biology accounting for physiology, ecology, and trait evolution to explore and explain complex observational data and ultimately improve the predictions of global ocean models.

Mixotrophy upgrades food quality for marine calanoid copepods

AbstractInorganic nutrient limitation affects the stoichiometry and nutritional quality of marine phytoplankton. Mixoplankton, able to photosynthesize and feed simultaneously in the one cell, can compensate shortage of nutrients by phagotrophy, theoretically upgrading their nutritional quality for their predators: the zooplankton. Yet, the additional value that phagotrophy in mixoplankton may provide to support zooplankton growth and recruitment has been poorly explored. Therefore, we investigated the feeding and reproductive performances of the copepods Paracartia grani and Centropages typicus on mono‐diets of the dinoflagellate Karlodinium veneficum grown as strict autotroph and as mixotroph, both under N and P depletion, and in nutrient‐balanced conditions (f/2 medium; only as autotroph). Feeding and reproduction outputs were generally higher in P. grani than in C. typicus. Both copepod species ingested the mixotrophic K. veneficum at similar rates than the autotrophic ones in either nutrient‐limited scenario. However, egg production and recruitment rates generally increased when feeding on mixotrophs, in P. grani on both N‐ and P‐limited diets, and in C. typicus under P limitation. In general, P limitation influenced copepod physiology more than N depletion. Our results show that phagotrophy upgrades nutritional quality in nutrient‐limited mixotrophs as prey for copepods compared to the strict autotrophic ones. These findings are among the first reported cases of copepod ingestion in the laboratory on actively feeding mixoplankton, and they highlight the importance of considering the trophic mode of the protist and the response by various zooplanktonic predators when attempting to understand the functioning of marine planktonic food webs.

Exogenous nutrient inputs restructure phytoplankton community and ecological stoichiometry of Eastern Indian Ocean

Exogenous nutrient inputs increasingly impact the structure and function of marine food weds through abiotic and biotic ways. The influence of nutrient inputs from atmospheric depositions and intermediate seawater supply on the phytoplankton growth and stoichiometry was studied in the Eastern Indian Ocean through multifactorial mesocosm experiments. Our results indicate that nitrogen inputs from atmospheric deposition and hydrodynamic processes did not only promote chlorophyll a biomass (5.3–58.52 μg·L-1) to increase the photosynthetically fixed carbon content but also generate a regime shift from picophytoplankton cyanobacteria to microphytoplankton diatom indicated by high relative abundance of microphytoplankton (>50%). These alternations of nutrient status and phytoplankton community structure reduced biodiversity of marine ecosystems (N-cultures, 0.18 to 0.56; control, 0.63) and generated the attendant C/N ratio of 5.6 ± 0.2 in cultures with nitrogen addition that was significantly lower than cultures with only phosphorus or iron addition. These results provide a thorough insight about the influence of nutrient inputs on marine biogeochemical cycle. Considering the universality of phytoplankton community alteration induced by exogenous nutrient inputs, integrating community compositions with phytoplankton stoichiometry may be helpful for clarify mechanisms of environment events impacting marine food weds.

MESMO 3: Flexible phytoplankton stoichiometry and refractory dissolved organic matter

Abstract. We describe the third version of Minnesota Earth System Model for Ocean biogeochemistry (MESMO 3), an Earth system model of intermediate complexity, with a dynamical ocean, dynamic–thermodynamic sea ice, and an energy–moisture-balanced atmosphere. A major feature of version 3 is the flexible C:N:P ratio for the three phytoplankton functional types represented in the model. The flexible stoichiometry is based on the power law formulation with environmental dependence on phosphate, nitrate, temperature, and light. Other new features include nitrogen fixation, water column denitrification, oxygen and temperature-dependent organic matter remineralization, and CaCO3 production based on the concept of the residual nitrate potential growth. In addition, we describe the semi-labile and refractory dissolved organic pools of C, N, P, and Fe that can be enabled in MESMO 3 as an optional feature. The refractory dissolved organic matter can be degraded by photodegradation at the surface and hydrothermal vent degradation at the bottom. These improvements provide a basis for using MESMO 3 in further investigations of the global marine carbon cycle to changes in the environmental conditions of the past, present, and future.