Phytoplankton Physiology Research Articles

Intraspecific Diversity in Thermal Performance Determines Phytoplankton Ecological Niche.

Temperature has a primary influence on phytoplankton physiology and ecology. We grew 12 strains of Gephyrocapsa huxleyi isolated from different-temperature regions for ~45 generations (2 months) and characterised acclimated thermal response curves across a temperature range. Even with similar temperature optima and overlapping cell size, strain growth rates varied between 0.45 and 1 day-1. Thermal niche widths varied from 16.7°C to 24.8°C, suggesting that strains use distinct thermal response mechanisms. We investigated the implications of this thermal intraspecific diversity using an ocean ecosystem simulation resolving phytoplankton thermal phenotypes. Model analogues of thermal 'generalists' and 'specialists' resulted in a distinctive global biogeography of thermal niche widths with a nonlinear latitudinal pattern. We leveraged model output to predict ranges of the 12 lab-reared strains and demonstrated how this approach could broadly refine geographic range predictions. Our combination of observations and modelled biogeography highlights the capacity of diverse groups to survive temperature shifts.

Hydrodynamics Mediates Biogeochemical Dynamics of Particulate Organic Matter in the Shelf of the Northern South China Sea During Summer

AbstractEnvironmental conditions, physiology and community composition of phytoplankton and the carbon and nitrogen isotope signature (δ13CPOC and δ15NPN) of particulate organic matter (POM) often covary across marine environments. However, little was known on the link of δ13CPOC and δ15NPN and the community and biochemical composition of phytoplankton. In this study, particulate organic carbon (POC) and nitrogen (PN), δ13CPOC, δ15NPN, phytoplankton community composition and biomass were determined during summer, along with environmental variables, in the shelf of the northern South China Sea influenced by the Pearl River plume, upwelling and anticyclonic eddy. Our results show that variability in δ13CPOC and δ15NPN along an environmental gradient is coupled with shifts in phytoplankton community composition and carbon to chlorophyll a (C:Chl a) ratio of phytoplankton. Low δ13CPOC values (−28.4 to −27.0‰) at nearshore stations (salinity <21) were primarily due to terrestrial POM input. High δ13CPOC (>−21.0‰) and δ15NPN (>5.6‰) values are most likely attributed to high abundance of diatoms induced by riverine nutrients in the plume‐impacted waters with intermediate salinity (21< salinity <33). Low δ13CPOC (<−22.0‰) and δ15NPN (−1.1–3.7‰) values are associated with high abundance of slow‐growing cyanobacteria in the oligotrophic area (salinity >33), where the lowest δ15NPN is most likely attributed to high abundance of N2‐fixing Trichodesmium spp., due to the influence of the anticyclonic eddy. Therefore, hydrodynamics modulates the biochemical composition and community composition of phytoplankton, leading to changes in δ13CPOC and δ15NPN. Our findings advance our understanding of the coupling of physical and biogeochemical processes in marginal seas.

Determination of biogeochemical properties in sea waters using the inversion of the three-stream irradiance model

Inversion models, in the context of oceanography, relate the observed ocean color to the concentrations of the different biogeochemical components present in the water of the ocean. However, building accurate inversion models can be quite complex due to the many factors that can influence the observed ocean color, such as variations in the composition or the optical properties of biogeochemical products. Here we assess the feasibility of the inversion approach, by implementing the three-stream light inversion model in a one-dimensional water column configuration, represented at the BOUSSOLE site in the northwestern Mediterranean Sea. Moreover, we provide a comprehensive sensitivity analysis of the model’s skill by perturbing the parameters of the bio-optical properties and phytoplankton physiology. Analysis of the inversion indicates that the model is able to reconstruct the variability of the optical constituents. Results indicate that chlorophyll-a and coloured dissolved organic matter play a major role in light modulation. The sensitivity analysis shows that the parameterization of the ratio of chlorophyll-a to carbon is important for the performance of the inversion model. A coherent inversion model, as presented, can be used as an observational operator to assimilate remote sensing reflectance.

Different amino acid compositions and food quality of particulate organic matter driven by two major phytoplankton groups in the Ross Sea

Understanding the amino acid (AA) composition of phytoplankton-derived particulate organic matter (POM) is crucial for unraveling phytoplankton physiology and assessing food quality. This study investigated AA compositions and food quality of POM associated with two phytoplankton groups in the Ross Sea polynya. The Phaeocystis antarctica (P. antarctica)-predominant group, with P. antarctica overwhelmingly contributing to its composition, demonstrated a fresh state and heightened physiological activity. In contrast, the P. antarctica and diatoms-mixed group exhibited superior essential amino acids (EAAs) contributions and a higher EAA index (EAAI), indicating enhanced food quality. Dissimilarity Index values provided nuanced insights into degradation stages not captured by other indices. Despite lower physiological activity, diatoms in the mixed group stood out as crucial sources of high-quality nutrition for higher trophic levels in the Ross Sea polynya. The observed variations in AA compositions not only reflected the phytoplankton community structure but also provided insights into their physiological conditions. Given the ongoing climate-induced environmental changes potentially influencing phytoplankton communities, this study underscores the potential impacts on the intricate food web dynamics in the Ross Sea polynya. The assessment of AA composition emerged as a valuable tool for understanding the ecological implications for higher trophic levels in this polar region.

Ignited competition: Impact of bioactive extracellular compounds on organelle functions and photosynthetic systems in harmful algal blooms.

Prevalent interactions among marine phytoplankton triggered by long-range climatic stressors are well-known environmental disturbers of community structure. Dynamic response of phytoplankton physiology is likely to come from interspecies interactions rather than direct climatic effect on single species. However, studies on enigmatic interactions among interspecies, which are induced by bioactive extracellular compounds (BECs), especially between related harmful algae sharing similar shellfish toxins, are scarce. Here, we investigated how BECs provoke the interactions between two notorious algae, Alexandrium minutum and Gymnodinium catenatum, which have similar paralytic shellfish toxin (PST) profiles. Using techniques including electron microscopy and transcriptome analysis, marked disruptions in G. catenatum intracellular microenvironment were observed under BECs pressure, encompassing thylakoid membrane deformations, pyrenoid matrix shrinkage and starch sheaths disappearance. In addition, the upregulation of gene clusters responsible for photosystem-I Lhca1/4 and Rubisco were determined, leading to weaken photon captures and CO2 assimilation. The redistribution of lipids and proteins occurred at the subcellular level based on in situ focal plane array FTIR imaging approved the damages. Our findings illuminated an intense but underestimated interspecies interaction triggered by BECs, which is responsible for dysregulating photosynthesis and organelle function in inferior algae and may potentially account for fitness alteration in phytoplankton community.

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.

Heterotrophic bacteria trigger transcriptome remodelling in the photosynthetic picoeukaryote Micromonas commoda.

Marine biogeochemical cycles are built on interactions between surface ocean microbes, particularly those connecting phytoplankton primary producers to heterotrophic bacteria. Details of these associations are not well understood, especially in the case of direct influences of bacteria on phytoplankton physiology. Here we catalogue how the presence of three marine bacteria (Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14 and Polaribacter dokdonensis MED152) individually and uniquely impact gene expression of the picoeukaryotic alga Micromonas commoda RCC 299. We find a dramatic transcriptomic remodelling by M. commoda after 8 h in co-culture, followed by an increase in cell numbers by 56 h compared with the axenic cultures. Some aspects of the algal transcriptomic response are conserved across all three bacterial co-cultures, including an unexpected reduction in relative expression of photosynthesis and carbon fixation pathways. Expression differences restricted to a single bacterium are also observed, with the Flavobacteriia P. dokdonensis uniquely eliciting changes in relative expression of algal genes involved in biotin biosynthesis and the acquisition and assimilation of nitrogen. This study reveals that M. commoda has rapid and extensive responses to heterotrophic bacteria in ways that are generalizable, as well as in a taxon specific manner, with implications for the diversity of phytoplankton-bacteria interactions ongoing in the surface ocean.

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.

Proteomics analysis reveals differential acclimation of coastal and oceanic Synechococcus to climate warming and iron limitation.

In many oceanic regions, anthropogenic warming will coincide with iron (Fe) limitation. Interactive effects between warming and Fe limitation on phytoplankton physiology and biochemical function are likely, as temperature and Fe availability affect many of the same essential cellular pathways. However, we lack a clear understanding of how globally significant phytoplankton such as the picocyanobacteria Synechococcus will respond to these co-occurring stressors, and what underlying molecular mechanisms will drive this response. Moreover, ecotype-specific adaptations can lead to nuanced differences in responses between strains. In this study, Synechococcus isolates YX04-1 (oceanic) and XM-24 (coastal) from the South China Sea were acclimated to Fe limitation at two temperatures, and their physiological and proteomic responses were compared. Both strains exhibited reduced growth due to warming and Fe limitation. However, coastal XM-24 maintained relatively higher growth rates in response to warming under replete Fe, while its growth was notably more compromised under Fe limitation at both temperatures compared with YX04-1. In response to concurrent heat and Fe stress, oceanic YX04-1 was better able to adjust its photosynthetic proteins and minimize the generation of reactive oxygen species while reducing proteome Fe demand. Its intricate proteomic response likely enabled oceanic YX04-1 to mitigate some of the negative impact of warming on its growth during Fe limitation. Our study highlights how ecologically-shaped adaptations in Synechococcus strains even from proximate oceanic regions can lead to differing physiological and proteomic responses to these climate stressors.

Phytoplankton physiology and functional traits under artificial upwelling with varying Si:N

IntroductionArtificial upwelling has been discussed as a nature-based solution to fertilize currently unproductive areas of the ocean to enhance food web productivity and atmospheric CO2 sequestration. The efficacy of this approach may be closely tied to the nutrient stoichiometry of the upwelled water, as Si-rich upwelling should benefit the growth of diatoms, who are key players for primary production, carbon export and food web efficiency.MethodsWith a mesocosm experiment in subtropical waters, we assessed the physiological and functional responses of an oligotrophic phytoplankton community to artificial upwelling under varying Si:N ratios (0.07-1.33).ResultsDeep water fertilization led to strongly enhanced primary productivity rates and net autotrophy across Si scenarios. At the community level, Si-rich upwelling50 temporarily increased primary production and consistently enhanced diatom growth, producing up to 10-fold higher abundances compared to Si-deficient upwelling. At the organism level, contrasting effects were observed. On the one hand, silicification and size of diatom cells remained unaffected by Si:N, which is surprising given the direct dependency of these traits on Si. On the other hand, diatom Chlorophyll a density and carbon density were strongly reduced and particulate matter C:N was elevated under Si-rich upwelling.DiscussionThis suggests a reduced nutritional value for higher trophic levels under high Si:N ratios. Despite these strong qualitative changes under high Si, diatom cells appeared healthy and showed high photosynthetic efficiency. Our findings reveal great physiological plasticity and adaptability in phytoplankton under artificial upwelling, with Si-dependent trade-offs between primary producer quantity and quality.

A Tribute to Richard W. Eppley

Richard W. Eppley (1931–2023), better known as “Dick,” was a tour de force in biological oceanography. Most of his research life was at Scripps Institution of Oceanography (Scripps), where he studied marine phytoplankton and their roles in biogeochemical processes. Over the course of his career, he influenced many people, not only in science but also as exemplar of integrity and fundamental curiosity about the ocean. His formidable contributions to phytoplankton physiology and biological oceanography were appreciatively reviewed shortly after his retirement (Weiler et al., 1990), and with added perspective after his death (Cullen and Eppley, 2024). What follows are tributes from several of his former students, postdocs, and colleagues.

Characterization of a Southern Ocean deep chlorophyll maximum: Response of phytoplankton to light, iron, and manganese enrichment

AbstractSouthern Ocean phytoplankton growth is limited by low iron (Fe) supply and irradiance, impacting the strength of the biological carbon pump. Unfavorable upper ocean conditions, such as low nutrient concentrations, can lead to the formation of deep chlorophyll or biomass maxima (DCM/DBM). While common in the Southern Ocean, these features remain understudied due to their subsurface location. To increase our understanding of their occurrence, we studied the responses of phytoplankton communities from a Southern Ocean DCM to increasing light, Fe, and manganese (Mn) levels. The DCM communities were light‐ and Fe‐limited, but light limitation did not increase phytoplankton Fe requirements. The greatest physiological responses were observed under combined Fe/light additions, which stimulated macronutrient drawdown, biomass production and the growth of large diatoms. Combined Mn/light additions induced subtle changes in Fe uptake rates and community composition, suggesting species‐specific Mn requirements. These results provide valuable information on Southern Ocean DCM phytoplankton physiology.

Higher temperature, increased CO2, and changing nutrient ratios alter the carbon metabolism and induce oxidative stress in a cosmopolitan diatom

AbstractPhytoplankton are responsible for about 90% of the oceanic primary production, largely supporting marine food webs, and actively contributing to the biogeochemical cycling of carbon. Yet, increasing temperature and pCO2, along with higher dissolved nitrogen: phosphorus ratios in coastal waters are likely to impact phytoplankton physiology, especially in terms of photosynthetic rate, respiration, and dissolved organic carbon (DOC) production. Here, we conducted a full‐factorial experiment to identify the individual and combined effects of temperature, pCO2, and N : P ratio on the antioxidant capacity and carbon metabolism of the diatom Phaeodactylum tricornutum. Our results demonstrate that, among these three drivers, temperature is the most influential factor on the physiology of this species, with warming causing oxidative stress and lower activity of antioxidant enzymes. Furthermore, the photosynthetic rate was higher under warmer conditions and higher pCO2, and, together with a lower dark respiration rate and higher DOC exudation, generated cells with lower carbon content. An enhanced oceanic CO2 uptake and an overall stimulated microbial loop benefiting from higher DOC exudation are potential longer‐term consequences of rising temperatures, elevated pCO2 as well as shifted dissolved N : P ratios.

Genetic and physiological responses to light quality in a deep ocean ecotype of Ostreococcus, an ecologically important photosynthetic picoeukaryote.

Phytoplankton are exposed to dramatic variations in light quality when cells are carried by upwelling or downwelling currents or encounter sediment. We investigated the potential impact of light quality changes in Ostreococcus, a key marine photosynthetic picoeukaryote, by analysing changes in its transcriptome, pigment content, and photophysiology after acclimation to monochromatic red, green, or blue light. The clade B species RCC809, isolated from the deep euphotic zone of the tropical Atlantic Ocean, responded to blue light by accelerating cell division at the expense of storage reserves and by increasing the relative level of blue-light-absorbing pigments. It responded to red and green light by increasing its potential for photoprotection. In contrast, the clade A species OTTH0595, which originated from a shallow water environment, showed no difference in photosynthetic properties and minor differences in carotenoid contents between light qualities. This was associated with the loss of candidate light-quality responsive promoter motifs identified in RCC809 genes. These results demonstrate that light quality can have a major influence on the physiology of eukaryotic phytoplankton and suggest that different light quality environments can drive selection for diverse patterns of responsiveness and environmental niche partitioning.

Effects of phytoplankton physiology on global ocean biogeochemistry and climate.

The similarity of the average ratios of nitrogen (N) and phosphorus (P) in marine dissolved inorganic and particulate organic matter, dN:P and pN:P, respectively, indicates tight links between those pools in the world ocean. Here, we analyze this linkage by varying phytoplankton N and P subsistence quotas in an optimality-based ecosystem model coupled to an Earth system model. The analysis of our ensemble of simulations discloses various feedbacks between changes in the N and P quotas, N2 fixation, and denitrification that weaken the often-hypothesized tight coupling between dN:P and pN:P. We demonstrate the importance of particulate N:C and P:C ratios for regulating dN:P on the global scale, with marine oxygen level being an important control. Our analysis provides further insight into the potential interdependence of phytoplankton physiology and global climate conditions.

Estimation of the Seawater Lidar Ratio by MODIS: Spatial–Temporal Characteristics and Ecological Significance

The lidar ratio of seawater is an essential quantity related to both lidar retrieval and water constituent. However, few studies discuss its spatial–temporal characteristics and ecological significance, which limits its applications in lidar remote sensing and marine science. This paper investigates the spatial–temporal characteristics and ecological significance of the lidar ratio of seawater using satellite passive remote sensing, which is validated by in situ measurements. Spatially, nearshore lidar ratio values are higher than offshore, mainly owing to the high concentration of colored dissolved organic matter in nearshore water. Temporally, the lidar ratio in each hemisphere exhibits lower values in summer than in winter due to the annual boom–bust cycle of phytoplankton. Furthermore, the variability patterns of the lidar ratio are nearly consistent with those of the chlorophyll-to-carbon ratio, implying the high ecological significance of phytoplankton physiology. These findings will provide the foundation for the application of lidar ratio in marine science and lidar remote sensing.

No adaptation to warming after selection for 800 generations in the coccolithophore Emiliania huxleyi BOF 92

Ocean warming is suggested to exert profound effects on phytoplankton physiology and growth. Here, we investigated how the coccolithophore Emiliania huxleyi (BOF 92, a non-calcifying strain) responded to changes in temperature in short- and long-term thermal treatments. The specific growth rate after 10 days of acclimation increased gradually with increasing temperatures (14, 17, 21, 24, 28°C) and peaked at ~23°C, followed by a significant decrease to 28°C. Chlorophyll a content, cell size, photosynthetic rate, and respiratory rate increased significantly from 14°C to 24°C, but the cellular particulate organic carbon (POC) and nitrogen (PON) showed the lowest values at the optimal temperature. In contrast, during long-term thermal treatments at 17°C and 21°C for 656 days (~790 generations for 17°C treatment; ~830 generations for 21°C treatment), the warming significantly stimulated the growth in the first 34 days and the last 162 days, but there was no significant difference in specific growth rate from Day 35 to Day 493. Chlorophyll a content, cell size, cellular POC/PON, and the ratio of POC to PON, showed no significant difference between the warming and control for most of the duration of the long-term exposure. The warming-selected population did not acquire persistent traits in terms of growth and cell quotas of POC and PON, which resumed to the levels in the control temperature treatment after about 9 generations in the shift test. In summary, our results indicate that warming by 4°C (17°C and 21°C) enhanced the growth, but did not result in adaptative changes in E. huxleyi (BOF 92) over a growth period of about 800 generations, reflecting that mild or non-stressful warming treatment to E. huxleyi isolated from cold seas does not alter its phenotypic plasticity.

Marine phytoplankton downregulate core photosynthesis and carbon storage genes upon rapid mixed layer shallowing

Marine phytoplankton are a diverse group of photoautotrophic organisms and key mediators in the global carbon cycle. Phytoplankton physiology and biomass accumulation are closely tied to mixed layer depth, but the intracellular metabolic pathways activated in response to changes in mixed layer depth remain less explored. Here, metatranscriptomics was used to characterize the phytoplankton community response to a mixed layer shallowing (from 233 to 5 m) over the course of two days during the late spring in the Northwest Atlantic. Most phytoplankton genera downregulated core photosynthesis, carbon storage, and carbon fixation genes as the system transitioned from a deep to a shallow mixed layer and shifted towards catabolism of stored carbon supportive of rapid cell growth. In contrast, phytoplankton genera exhibited divergent transcriptional patterns for photosystem light harvesting complex genes during this transition. Active virus infection, taken as the ratio of virus to host transcripts, increased in the Bacillariophyta (diatom) phylum and decreased in the Chlorophyta (green algae) phylum upon mixed layer shallowing. A conceptual model is proposed to provide ecophysiological context for our findings, in which integrated light limitation and lower division rates during transient deep mixing are hypothesized to disrupt resource-driven, oscillating transcript levels related to photosynthesis, carbon fixation, and carbon storage. Our findings highlight shared and unique transcriptional response strategies within phytoplankton communities acclimating to the dynamic light environment associated with transient deep mixing and shallowing events during the annual North Atlantic bloom.

Biogeochemical‐Argo floats show that chlorophyll increases before carbon in the high‐latitude Southern Ocean spring bloom

AbstractIn the Southern Ocean, phytoplankton blooms are an annually recurring prominent feature that play a significant role in ocean CO2 uptake. Understanding the timing of the phytoplankton bloom is necessary to provide insights into the underlying physiological drivers, for the study of ecosystem dynamics and consequent patterns in downward carbon export. Previous studies have used chlorophyll (chl) and particulate organic carbon, from either satellites or biogeochemical‐Argo (BGC‐Argo) floats, to investigate bloom phenology, but provide inconsistent findings regarding bloom timing. Here, we compare bloom dynamics based on three diagnostics from 7114 BGC‐Argo float profiles, south of 60°S. Bloom onset consistently occurs earlier when calculated using chl than when based on phytoplankton carbon or nitrate uptake, and the decoupling increases with latitude. This suggests that phytoplankton synthesize increased chl to acclimate to low‐light conditions, before increasing their biomass. These results highlight the importance of considering phytoplankton physiology when choosing proxies for phytoplankton growth.

Summer phytoplankton photosynthetic characteristics in the Changjiang River Estuary and the adjacent East China Sea

IntroductionThe Changjiang (Yangtze) River is one of the largest rivers in the world, and its estuary and offshore plume create a diversity of ecological habitats for the phytoplankton community. The phytoplankton community has to balance between light limitation in the sediment-laden inshore waters and nutrient limitation in the offshore waters. Active fluorescence measurements can provide rapid, non-intrusive estimates of photosynthetic characteristics at high spatial and temporal resolution.MethodsIn the summer of 2020, a field survey of hydrodynamic characteristics, availability of nutrients, the maximum quantum efficiency of photosystem II (Fv/Fm), and rapid light curves across the Changjiang River Estuary and its adjacent sea was conducted, assessing relationships between photosynthetic physiology and biomass accumulation.ResultsThe photosynthetic activities significantly differed among the turbid river water, the stratified river plume water, and the oceanic East China Sea Water. The photosynthetic physiology of phytoplankton was the most active near the front of Changjiang Diluted Water, where the Fv/Fm was over 0.5.DiscussionPhytoplankton photosynthesis was alleviated from light limitation downstream of the river mouth, and benefited from phosphorus supply via tidal mixing and upwelling. The relatively suitable light and nutrients led to high photosynthetic activities, supporting increased productivity and biomass in this water. The phytoplankton in the Changjiang estuary rivermouth were under intense stress, suggested by the Fv/Fm values under 0.3. Also, the strong vertical mixing process diluted the river nutrients before the phytoplankton consumed them. Nutrients further limited the phytoplankton offshore in the East China Sea.