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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.

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

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.