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Competing Interests: Competing interests statement:The authors declare no competing interest.

AbstractConventional analyses suggest that the metabolism of heterotrophs is thermally more sensitive than that of autotrophs, implying that warming leads to pronounced trophodynamic imbalances. However, these analyses inappropriately combine within- and across-taxa trends. Our new analysis separates these, revealing that 92% of the difference in the apparent thermal sensitivity between autotrophic and heterotrophic protists does indeed arise from within-taxa responses. Fitness differences among taxa adapted to different temperature regimes only partially compensate for the positive biochemical relationship between temperature and growth rate within taxa, supporting the hotter-is-partially-better hypothesis. Our work highlights the importance of separating within- and across-taxa responses when comparing temperature sensitivities between groups, which is relevant to how trophic imbalances and carbon fluxes respond to warming.

Marine herbivorous protists are often the dominant grazers of primary production. We developed a size-based model with flexible size-based grazing to encapsulate taxonomic and behavioral diversity. We examined individual and combined grazing impacts by three consumer sizes that span the size range of protistan grazers- 5, 50, and 200 μm-on a size-structured phytoplankton community. Prey size choice and dietary niche width varied with consumer size and with co-existence of other consumers. When all consumer sizes were present, distinct dietary niches emerged, with a range of consumer-prey size ratios spanning from 25:1 to 0.4:1, encompassing the canonical 10:1 often assumed. Grazing on all phytoplankton size classes maximized the phytoplankton size diversity through the keystone predator effect, resulting in a phytoplankton spectral slope of approximately -4, agreeing with field data. This mechanistic model suggests the observed size structure of phytoplankton communities is at least in part the result of selective consumer feeding., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Taniguchi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Why, contrary to theoretical predictions, do marine microbe communities harbor tremendous phenotypic heterogeneity? How can so many marine microbe species competing in the same niche coexist? We discovered a unifying explanation for both phenomena by investigating a non-cooperative game that interpolates between individual-level competitions and species-level outcomes. We identified all equilibrium strategies of the game. These strategies represent the probability distribution of competitive abilities (e.g. traits) and are characterized by maximal phenotypic heterogeneity. They are also neutral towards each other in the sense that an unlimited number of species can co-exist while competing according to the equilibrium strategies. Whereas prior theory predicts that natural selection would minimize trait variation around an optimum value, here we obtained a mathematical proof that species with maximally variable traits are those that endure. This discrepancy may reflect a disparity between predictions from models developed for larger organisms in contrast to our microbe-centric model. Rigorous mathematics proves that phenotypic heterogeneity is itself a mechanistic underpinning of microbial diversity. This discovery has fundamental ramifications for microbial ecology and may represent an adaptive reservoir sheltering biodiversity in changing environmental conditions., Competing Interests: The authors have declared that no competing interests exist.

Holographic microscopy has emerged as a tool for in situ imaging of microscopic organisms and other particles in the marine environment: appealing because of the relatively larger sampling volume and simpler optical configuration compared to other imaging systems. However, its quantitative capabilities have so far remained uncertain, in part because hologram reconstruction and image recognition have required manual operation. Here, we assess the quantitative skill of our automated hologram processing pipeline (CCV Pipeline), to evaluate the size and concentration measurements of environmental and cultured assemblages of marine plankton particles, and microspheres. Over 1 million particles, ranging from 10 to 200  μ m in equivalent spherical diameter, imaged by the 4-Deep HoloSea digital inline holographic microscope (DIHM) are analyzed. These measurements were collected in parallel with a FlowCam (FC), Imaging FlowCytobot (IFCB), and manual microscope identification. Once corrections for particle location and nonuniform illumination were developed and applied, the DIHM showed an underestimate in ESD of about 3% to 10%, but successfully reproduced the size spectral slope from environmental samples, and the size distribution of cultures ( Dunaliella tertiolecta , Heterosigma akashiwo , and Prorocentrum micans ) and microspheres. DIHM concentrations (order 1 to 1000 particles ml -1 ) showed a linear agreement ( r 2 = 0.73) with the other instruments, but individual comparisons at times had large uncertainty. Overall, we found the DIHM and the CCV Pipeline required extensive manual correction, but once corrected, provided concentration and size estimates comparable to the other imaging systems assessed in this study. Holographic cameras are mechanically simple, autonomous, can operate at very high pressures, and provide a larger sampling volume than comparable lens-based tools. Thus, we anticipate that these characterization efforts will be rewarded with novel discovery in new oceanic environments., Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (© 2020 The Authors. Limnology and Oceanography: Methods published by Wiley Periodicals LLC. on behalf of Association for the Sciences of Limnology and Oceanography.)

The impacts of grazing by meso- and microzooplankton on phytoplankton primary production (PP) was investigated in the surface layer of the western North Atlantic during spring. Shipboard experiments were performed on a latitudinal transect at three stations that differed in mixed layer depth, temperature, and mesozooplankton taxonomic composition. The mesozooplankton community was numerically dominated by Calanus finmarchicus at the northern and central station, with Calanus hyperboreus also present at the northern station. The southern station was >10 °C warmer than the other stations and had the most diverse mesozooplankton assemblage, dominated by small copepods including Paracalanus spp. Microzooplankton grazing was detected only at the northern station, where it removed 97% of PP. Estimated clearance rates by C. hyperboreus and C. finmarchicus suggested that at in-situ abundance these mesozooplankton were not likely to have a major impact on phytoplankton abundance, unless locally aggregated. Although mesozooplankton grazing impact on total phytoplankton was minimal, these grazers completely removed the numerically scarce > 10 µm particles, altering the particle-size spectrum. At the southern station, grazing by the whole mesozooplankton assemblage resulted in a removal of 14% of PP, and its effect on net phytoplankton growth rate was similar irrespective of ambient light. In contrast, reduction in light availability had an approximately 3-fold greater impact on net phytoplankton growth rate than mesozooplankton grazing pressure. The low mesozooplankton grazing impact across stations suggests limited mesozooplankton-mediated vertical export of phytoplankton production. The constraints provided here on trophic transfer, as well as quantitative estimates of the relative contribution of light and grazer controls of PP and of grazer-induced shifts in particle size spectra, illuminate food web dynamics and aid in parameterizing modeling-frameworks assessing global elemental fluxes and carbon export., Competing Interests: Susanne Menden Deuer is an Academic Editor for PeerJ. The other authors declare they have no competing interests., (©2020 Morison et al.)

The North Atlantic phytoplankton spring bloom is the pinnacle in an annual cycle that is driven by physical, chemical, and biological seasonality. Despite its important contributions to the global carbon cycle, transitions in plankton community composition between the winter and spring have been scarcely examined in the North Atlantic. Phytoplankton composition in early winter was compared with latitudinal transects that captured the subsequent spring bloom climax. Amplicon sequence variants (ASVs), imaging flow cytometry, and flow-cytometry provided a synoptic view of phytoplankton diversity. Phytoplankton communities were not uniform across the sites studied, but rather mapped with apparent fidelity onto subpolar- and subtropical-influenced water masses of the North Atlantic. At most stations, cells < 20-µm diameter were the main contributors to phytoplankton biomass. Winter phytoplankton communities were dominated by cyanobacteria and pico-phytoeukaryotes. These transitioned to more diverse and dynamic spring communities in which pico- and nano-phytoeukaryotes, including many prasinophyte algae, dominated. Diatoms, which are often assumed to be the dominant phytoplankton in blooms, were contributors but not the major component of biomass. We show that diverse, small phytoplankton taxa are unexpectedly common in the western North Atlantic and that regional influences play a large role in modulating community transitions during the seasonal progression of blooms.

Heterotrophic protists play pivotal roles in aquatic ecosystems by transferring matter and energy, including lipids, from primary producers to higher trophic predators. Using Oxyrrhis marina as a model organism, changes to the non-saponifiable protist lipids were investigated under satiation and starvation conditions. During active feeding on the alga Cryptomonas sp., the O. marina hexane soluble non-saponifiable fraction lipid profile reflected its food source with the observed presence of long chain mono-unsaturated fatty alcohols up to C25:1. Evidence of trophic upgrading in O. marina was observed with long chain mono-unsaturated fatty alcohol accumulation of up to C35:1. To the best of our knowledge, this is the first evidence that heterotrophic dinoflagellates are capable of producing ester derived alcohols and that dinoflagellates like O. marina are capable of synthesizing fatty alcohols up to C 35 . Additionally, we show evidence of trophic upgrading of lipids. During a 20-day resource deprivation, the lipid profile remained constant. During starvation, the mobilization of wax esters as energy stores was observed with long chain fatty alcohols mobilized first. Changes in lipid class profile and utilization of wax esters in O. marina provides insight into the types of lipids available for energy demand, the transfer of lipids through the base of marine food webs, and the catabolic response induced by resource deprivation., Competing Interests: Susanne Menden-Deuer is an Academic Editor for PeerJ.

To assess protistan grazing impact and temperature sensitivity on plankton population dynamics, we measured bulk and species-specific phytoplankton growth and herbivorous protist grazing rates in Disko Bay, West Greenland in April-May 2011. Rate estimates were made at three different temperatures in situ (0 °C), +3 °C and +6 °C over ambient. In situ Chlorophyll a (Chl a ) doubled during the observation period to ∼12  µg Chl a L -1 , with 60-97% of Chl a in the >20 µm size-fraction dominated by the diatom genus Chaetoceros. Herbivorous dinoflagellates comprised 60-80% of microplankton grazer biomass. At in situ temperatures, phytoplankton growth or grazing by herbivorous predators <200 µm was not measurable until 11 days after observations commenced. Thereafter, phytoplankton growth was on average 0.25 d -1 . Phytoplankton mortality due to herbivorous grazing was only measured on three occasions but the magnitude was substantial, up to 0.58 d -1 . Grazing of this magnitude removed ∼100% of primary production. In short-term temperature-shift incubation experiments, phytoplankton growth rate increased significantly (20%) at elevated temperatures. In contrast, herbivorous protist grazing and species-specific growth rates decreased significantly (50%) at +6 °C. This differential response in phytoplankton and herbivores to temperature increases resulted in a decrease of primary production removed with increasing temperature. Phaeocystis spp. abundance was negatively correlated with bulk grazing rate. Growth and grazing rates were variable but showed no evidence of an inherent, low temperature limitation. Herbivorous protist growth rates in this study and in a literature review were comparable to rates from temperate waters. Thus, an inherent physiological inhibition of protistan growth or grazing rates in polar waters is not supported by the data. The large variability between lack of grazing and high rates of primary production removal observed here and confirmed in the literature for polar waters implies larger amplitude fluctuations in phytoplankton biomass than slower, steady grazing losses of primary production., Competing Interests: Susanne Menden-Deuer is an Academic Editor for PeerJ.

To assess the effects of fluctuating prey availability on predator population dynamics and grazing impact on phytoplankton, we measured growth and grazing rates of three heterotrophic dinoflagellate species-Oxyrrhis marina, Gyrodinium dominans and Gyrodinium spirale-before and after depriving them of phytoplankton prey. All three dinoflagellate species survived long periods (> 10 d) without algal prey, coincident with decreases in predator abundance and cell size. After 1-3 wks, starvation led to a 17-57% decrease in predator cell volume and some cells became deformed and transparent. When re-exposed to phytoplankton prey, heterotrophs ingested prey within minutes and increased cell volumes by 4-17%. At an equivalent prey concentration, continuously fed predators had ~2-fold higher specific growth rates (0.18 to 0.55 d -1 ) than after starvation (-0.16 to 0.25 d -1 ). Maximum specific predator growth rates would be achievable only after a time lag of at least 3 d. A delay in predator growth poststarvation delays predator-induced phytoplankton mortality when prey re-emerges at the onset of a bloom event or in patchy prey distributions. These altered predator-prey population dynamics have implications for the formation of phytoplankton blooms, trophic transfer rates, and potential export of carbon., (© 2016 The Author(s) Journal of Eukaryotic Microbiology © 2016 International Society of Protistologists.)

The effects of ongoing changes in ocean carbonate chemistry on plankton ecology have important implications for food webs and biogeochemical cycling. However, conflicting results have emerged regarding species-specific responses to p CO2 enrichment and thus community responses have been difficult to predict. To assess community level effects (e.g., production) of altered carbonate chemistry, studies are needed that capitalize on the benefits of controlled experiments but also retain features of intact ecosystems that may exacerbate or ameliorate the effects observed in single-species or single cohort experiments. We performed incubations of natural plankton communities from Narragansett Bay, RI, USA in winter at ambient bay temperatures (5-13 °C), light and nutrient concentrations under three levels of controlled and constant CO 2 concentrations, simulating past, present and future conditions at mean p CO 2 levels of 224, 361, and 724 μatm respectively. Samples for carbonate analysis, chlorophyll a , plankton size-abundance, and plankton species composition were collected daily and phytoplankton growth rates in three different size fractions (<5, 5-20, and >20 μm) were measured at the end of the 7-day incubation period. Community composition changed during the incubation period with major increases in relative diatom abundance, which were similar across p CO 2 treatments. At the end of the experiment, 24-hr growth responses to p CO 2 levels varied as a function of cell size. The smallest size fraction (<5 μm) grew faster at the elevated p CO 2 level. In contrast, the 5-20 μm size fraction grew fastest in the Present treatment and there were no significant differences in growth rate among treatments in the > 20 μm size fraction. Cell size distribution shifted toward smaller cells in both the Past and Future treatments but remained unchanged in the Present treatment. Similarity in Past and Future treatments for cell size distribution and growth rate (5-20 μm size fraction) illustrate non-monotonic effects of increasing p CO 2 on ecological indicators and may be related to opposing physiological effects of high CO 2 and low pH both within and among species. Interaction of these effects with other factors (e.g., nutrients, light, temperature, grazing, initial species composition) may explain variability among published studies. The absence of clear treatment-specific effects at the community level suggest that extrapolation of species-specific responses or experiments with only present day and future p CO 2 treatments levels would produce misleading predictions of ocean acidification impacts on plankton production.

Motility is a key trait that phytoplankton utilize to navigate the heterogeneous marine environment. Quantifying both intra- and inter-specific variability in trait distributions is key to utilizing traits to distinguish groups of organisms and assess their ecological function. Because examinations of intra-specific variability are rare, here we measured three-dimensional movement behaviors and distribution patterns of seven genetically distinct strains of the ichthyotoxic raphidophyte, Heterosigma akashiwo. Strains were collected from different ocean basins but geographic distance between isolates was a poor predictor of genetic relatedness among strains. Observed behaviors were significantly different among all strains examined, with swimming speed and turning rate ranging from 33-115 μm s(-1) and 41-110° s(-1), respectively. Movement behaviors were consistent over at least 12 h, and in one case identical when measured several years apart. Movement behaviors were not associated with a specific cell size, carbon content, genetic relatedness, or geographic distance. These strain-specific behaviors resulted in algal populations that had distinct vertical distributions in the experimental tank. This study demonstrates that the traits of genetic identity and motility can provide resolution to distinguish strains of species, where variations in size or biomass are insufficient characteristics.

Competing Interests: The authors have declared that no competing interests exist.

In apparent contradiction to competition theory, the number of known, coexisting plankton species far exceeds their explicable biodiversity-a discrepancy termed the Paradox of the Plankton. We introduce a new game-theoretic model for competing microorganisms in which one player consists of all organisms of one species. The stable points for the population dynamics in our model, known as strategic behaviour distributions (SBDs), are probability distributions of behaviours across all organisms which imply a stable population of the species as a whole. We find that intra-specific variability is the key characteristic that ultimately allows coexistence because the outcomes of competitions between individuals with variable competitive abilities are unpredictable. Our simulations based on the theoretical model show that up to 100 species can coexist for at least 10,000 generations, and that even small population sizes or species with inferior competitive ability can survive when there is intra-specific variability. In nature, this variability can be observed as niche differentiation, variability in environmental and ecological factors, and variability of individual behaviours or physiology. Therefore, previous specific explanations of the paradox are consistent with and provide specific examples of our suggestion that individual variability is the mechanism which solves the paradox.

Diatoms are genetically diverse unicellular photosynthetic eukaryotes that are key primary producers in the ocean. Many of the over 100 extant diatom species in the cosmopolitan genus Thalassiosira are difficult to distinguish in mixed populations using light microscopy. Here, we examine shifts in Thalassiosira spp. composition along a coastal to open ocean transect that encountered a 3-month-old Haida eddy in the northeast Pacific Ocean. To quantify shifts in Thalassiosira species composition, we developed a targeted automated ribosomal intergenic spacer analysis (ARISA) method to identify Thalassiosira spp. in environmental samples. As many specific fragment lengths are indicative of individual Thalassiosira spp., the ARISA method is a useful screening tool to identify changes in the relative abundance and distribution of specific species. The method also enabled us to assess changes in Thalassiosira community composition in response to chemical and physical forcing. Thalassiosira spp. community composition in the core of a 3-month-old Haida eddy remained largely (>80%) similar over a 2-week period, despite moving 24 km southwestward. Shifts in Thalassiosira species correlated with changes in dissolved iron (Fe) and temperature throughout the sampling period. Simultaneously tracking community composition and relative abundance of Thalassiosira species within the physical and chemical context they occurred allowed us to identify quantitative linkages between environmental conditions and community response.

The ability of harmful algal species to form dense, nearly monospecific blooms remains an ecological and evolutionary puzzle. We hypothesized that predation interacts with estuarine salinity gradients to promote blooms of Heterosigma akashiwo (Y. Hada) Y. Hada ex Y. Hara et M. Chihara, a cosmopolitan toxic raphidophyte. Specifically, H. akashiwo's broad salinity tolerance appears to provide a refuge from predation that enhances the net growth of H. akashiwo populations through several mechanisms. (1) Contrasting salinity tolerance of predators and prey. Estuarine H. akashiwo isolates from the west coast of North America grew rapidly at salinities as low as six, and distributed throughout experimental salinity gradients to salinities as low as three. In contrast, survival of most protistan predator species was restricted to salinities >15. (2) H. akashiwo physiological and behavioral plasticity. Acclimation to low salinity enhanced H. akashiwo's ability to accumulate and grow in low salinity waters. In addition, the presence of a ciliate predator altered H. akashiwo swimming behavior, promoting accumulation in low-salinity surface layers inhospitable to the ciliate. (3) Negative effects of low salinity on predation processes. Ciliate predation rates decreased sharply at salinities <25 and, for one species, H. akashiwo toxicity increased at low salinities. Taken together, these behaviors and responses imply that blooms can readily initiate in low salinity waters where H. akashiwo would experience decreased predation pressure while maintaining near-maximal growth rates. The salinity structure of a typical estuary would provide this HAB species a unique refuge from predation. Broad salinity tolerance in raphidophytes may have evolved in part as a response to selective pressures associated with predation., (© 2012 Phycological Society of America.)

Vibrio cholerae is a human pathogenic marine bacterium inhabiting coastal regions and is vectored into human food and water supplies via attachment to particles including detritus, phytoplankton, and zooplankton. Particle colonization by the pathogen is inhibited by an antagonistic interaction with the particle-associated Vibrionales bacterium SWAT3, a producer of the antibiotic andrimid. By analyzing the individual movement behaviors of V. cholerae exposed to a gradient of andrimid in a microfluidics device, we show that the pathogen has a concentration dependent avoidance response to sub-lethal concentrations of the pure antibiotic and to the metabolites produced by a growing colony of SWAT3-wild-type. This avoidance behavior includes a 25% increase in swimming speeds, 30% increase in run lengths, and a shift in the direction of the bacteria away from the andrimid source. Consequently, these behavioral shifts at low concentrations of andrimid would lead to higher diffusivity and result in the dispersion of bacteria away from the competitor and source of the antibiotic. Such alterations in motility were not elicited in response to a non-andrimid-producing SWAT3 mutant, suggesting andrimid may be a negative effector of chemotaxis for V. cholerae. The behavioral response of colonizing bacteria to sub-inhibitory concentrations of competitor-produced antibiotics is one mechanism that can influence microbial diversity and interspecific competition on particles, potentially affecting human health in coastal communities and element cycling in the ocean.

In the plankton, heterotrophic microbes encounter and ingest phytoplankton prey, which effectively removes >50% of daily phytoplankton production in the ocean and influences global primary production and biochemical cycling rates. Factors such as size, shape, nutritional value, and presence of chemical deterrents are known to affect predation pressure. Effects of movement behaviors of either predator or prey on predation pressure, and particularly fleeing behaviors in phytoplankton are thus far unknown. Here, we quantified individual 3D movements, population distributions, and survival rates of the toxic phytoplankton species, Heterosigma akashiwo in response to a ciliate predator and predator-derived cues. We observed predator-induced defense behaviors previously unknown for phytoplankton. Modulation of individual phytoplankton movements during and after predator exposure resulted in an effective separation of predator and prey species. The strongest avoidance behaviors were observed when H. akashiwo co-occurred with an actively grazing predator. Predator-induced changes in phytoplankton movements resulted in a reduction in encounter rate and a 3-fold increase in net algal population growth rate. A spatially explicit population model predicted rapid phytoplankton bloom formation only when fleeing behaviors were incorporated. These model predictions reflected field observations of rapid H. akashiwo harmful algal bloom (HAB) formation in the coastal ocean. Our results document a novel behavior in phytoplankton that can significantly reduce predation pressure and suggests a new mechanism for HAB formation. Phytoplankton behaviors that minimize predatory losses, maximize resource acquisition, and alter community composition and distribution patterns could have major implications for our understanding and predictive capacity of marine primary production and biochemical cycling rates.

Quantitative linkages between individual organism movements and the resulting population distributions are fundamental to understanding a wide range of ecological processes, including rates of reproduction, consumption, and mortality, as well as the spread of diseases and invasions. Typically, quantitative data are collected on either movement behaviors or population distributions, rarely both. This study combines empirical observations and model simulations to gain a mechanistic understanding and predictive ability of the linkages between both individual movement behaviors and population distributions of a single-celled planktonic herbivore. In the laboratory, microscopic 3D movements and macroscopic population distributions were simultaneously quantified in a 1L tank, using automated video- and image-analysis routines. The vertical velocity component of cell movements was extracted from the empirical data and used to motivate a series of correlated random walk models that predicted population distributions. Validation of the model predictions with empirical data was essential to distinguish amongst a number of theoretically plausible model formulations. All model predictions captured the essence of the population redistribution (mean upward drift) but only models assuming long correlation times (minute), captured the variance in population distribution. Models assuming correlation times of 8 minutes predicted the least deviation from the empirical observations. Autocorrelation analysis of the empirical data failed to identify a de-correlation time in the up to 30-second-long swimming trajectories. These minute-scale estimates are considerably greater than previous estimates of second-scale correlation times. Considerable cell-to-cell variation and behavioral heterogeneity were critical to these results. Strongly correlated random walkers were predicted to have significantly greater dispersal distances and more rapid encounters with remote targets (e.g. resource patches, predators) than weakly correlated random walkers. The tendency to disperse rapidly in the absence of aggregative stimuli has important ramifications for the ecology and biogeography of planktonic organisms that perform this kind of random walk.