Going ballistic in the plankton: anisotropic swimming behavior of marine protists

Diel vertical migrations (DVMs) of many plankton species, including single-celled protists, are well documented in the field and form a core component of many large-scale numerical models of plankton transport and ecology. However, the sparse quantitative data available describing motility behaviors of individual protists have frequently indicated that motility exhibits only short-term correlation on the order of a few seconds or hundreds of micrometers, resembling diffusive transport at larger scales—a result incompatible with DVM, which requires ballistic (straight-line) motion. We interrogated an extensive set of three-dimensional protistan movement trajectories in an effort to identify spatial and temporal correlation scales. Whereas the horizontal components of movement were diffusive, the vertical component remained highly correlated (i.e., nonrandom) for nearly all species for the duration of observation (up to 120 s and 6.1 mm) and in the absence of any environmental cues besides gravity. These persistent motility patterns may have been obscured in some previous studies due to the use of restrictive containers, dimensionally lumped, isotropic analyses, and/or an observation bias, inherent to observing free-swimming organisms with stationary cameras, which we accounted for in this study. Extrapolated over a 12-h period, conservative estimates of vertical travel ranges for the protists observed here would be 3–10 m, while diffusive horizontal motion would result in about 10 cm of travel at most. Hence, these extended observations of phylogenetically diverse swimming protists, coupled with a quantitative analysis that accounts for anisotropy in the data, illustrate the small-scale mechanistic underpinnings of DVM

The theory of games and microbe ecology

Using game theory, we provide mathematical proof that if a species of asexually reproducing microbes is not characterized by maximum variability in competitive abilities among its individual organisms, then that species is vulnerable to replacement by competitors. Furthermore, we prove that such maximally variable species are neutral towards each other in competition for limited resources; they coexist. Our proof is constructive: given one species which does not possess maximum variability, we construct a second species with the same (or lower) mean competitive ability which can outcompete the first, in the sense that its expected value in competition is positive, whereas the expected value of the non-maximally variable species is negative. Our results point towards the mechanistic underpinnings for the frequent observations that (1) microbes are characterized by large intra-specific variability and that (2) the number of extant microbe species is very large

Contribution to the Themed Section: Scaling from individual plankton to marine ecosystems HORIZONS Small bugs with a big impact: linking plankton ecology with ecosystem processes

As an introduction to the following Themed Section on the significance of planktonic organisms to the functioning of marine ecosystems and global biogeochemical cycles we discuss the ramifications size imparts on the biology of plankton. We provide examples of how the characteristics of these microscopic organisms shape plankton population dynamics, distributions, and ecosystem functions. Key features of the marine environment place constraints on the ecology and evolution of plankton. Understanding these constraints is critical in developing a mechanistic understanding and predictive capacity of how planktonic ecosystems function, render their capacities in terms of biogeochemical cycling and trophic transfer, and how planktonic communities might respond to changing climate conditions

Early Spring Phytoplankton Dynamics in the Subpolar North Atlantic: The Influence of Protistan Herbivory

We measured phytoplankton-growth (μ) and herbivorous-protist grazing (g) rates in relation to mixed-layer-depth (MLD) during the March/April 2012 EuroBasin cruise in the subpolar North Atlantic. We performed 15 dilution experiments at two open-ocean (∼ 1300 m) and one shelf (160 m) station. Of the two open-ocean stations one was deeply mixed (476 m), the other stratified (46 m). At the shelf station, MLD reached the bottom. Initial chlorophyll a (Chl a) varied from 0.2–1.9 μg L−1 and increased up to 2.7 μg L−1 at the shelf station. In 80% of experiments, regardless of MLD, growth-rates exceeded grazing-mortality rates. At the open-ocean stations, the deep ML coincided with μ and g that varied over the same range (≤ 0–0.6 d−1), whereas stratification corresponded to μ and g that ranged from 0.14–0.41 d−1 to 0.11–0.34 d−1, respectively. At the stratified station, the balance between μ and g explained 98% of in situ variations in Chl a, whereas at the deep-ML station, rate estimates had no explanatory power. The consistent relationship between μ and g, which corresponded to a grazing-removal of 64% of primary production, suggests that g might be predictable if μ is known, and that a coefficient of 0.64 may be a useful parameter for subarctic carbon models. Composition and persistence of the plankton assemblages differed at the stations and may have been a significant driver of grazing-pressure. Overall, these results showed no association of MLD with grazing-pressure and highlight the need to assess to what extent MLD represents the depth of active-mixing to understand the effects of protistan-grazing on the development of the North Atlantic spring bloom

Common temperature-growth dependency and acclimation response in three herbivorous protists

Phytoplankton growth dependence on temperature is recognized and has been quantified comprehensively. However, no similar relationship exists for the major phytoplankton predators, the herbivorous protists, especially at low temperatures representing polar and coastal oceans during most seasons. Their acclimation to changing temperatures is also largely unexplored. Here we report acclimated growth and acclimation rates from 0 to 22°C for 3 cosmopolitan herbivorous dinoflagellates. Due to interactive effects between size and temperature, growth increased 40% more rapidly with increasing temperature for production- compared to division-based growth rates (0.043 and 0.062 d-1 °C-1, respectively). Biomass-based growth rates were 10-fold higher than abundance-based rates at low temperatures, reflecting an average 50% increase in biovolume at ≤2°C. Thus, there was significant biomass accumulation at low temperatures, despite low cell-division rates. Testing different acclimation procedures, we established that acclimated rates emerged after 3 generations. Herbivores required 1.25 d °C-1 when acclimating towards higher temperatures and 2.5 d °C-1 when transitioning towards lower temperatures. Growth rates increased linearly with temperature, implying a weaker temperature effect on growth than the commonly assumed exponential dependency. A possible consequence is that herbivore growth rates are underestimated at cold and overestimated at warm temperatures. Current and future ocean assessments could thus underestimate trophic transfer rates in polar and cold-water regions and overestimate herbivore growth and thus grazing impact in future ocean predictions. Identifying physiological responses that transcend species-specificity supports cross-biome comparisons of ecosystem structure and function that rely on accurate predictions of matter and energy flow in planktonic food webs

Predator-Induced Fleeing Behaviors in Phytoplankton: A New Mechanism for Harmful Algal Bloom Formation?

In the plankton, heterotrophic microbes encounter and ingest phytoplankton prey, which effectively removes \u3e50% 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

Physical and optical properties of phytoplankton-rich layers in a coastal fjord: a step toward prediction and strategic sampling of plankton patchiness

Dense aggregations of phytoplankton in layers or patches alter the optical and physical properties of the water column and result in significant heterogeneity in trophic and demographic rates of local plankton populations. Determining the factors driving patch formation, persistence, intensity, and dissipation is key to understanding the ramifications of plankton patchiness in marine systems. Regression and multi-parametric statistical analyses were used to identify the physical and optical properties associated with 71 phytoplankton-rich layers (PRLs) identified from 158 CTD profiles collected between 2008 and 2010 in East Sound, Washington, USA. Generalized additive models (GAMs) were used to explore water column properties associated with and characterizing PRLs. Patch presence was associated with increasing water column stability represented by the Brunt-Väisälä frequency (N2), Thorpe scale (Lt), and turbulent energy dissipation rate (e). A predictive regression identified patch presence with 100% accuracy when log10(N2) = -1 and 70% of the cases when log10(e) = -3. A GAM of passively measured variables, which did not include fluorescence, was able to model patch intensity with considerable agreement (R2 = 0.58), and the fit was improved by including fluorescence (R2 = 0.69). Fluorescence alone was an insufficient predictor of PRLs, due in part to the influence of non-photochemical quenching (NPQ) in surface waters and the wide range of fluorescence intensities observed. The results show that a multi-parametric approach was necessary to characterize phytoplankton patches and that physical structure, resulting in steep gradients in bio-optical properties, hold greater predictive power than bio-optical properties alone. Integration of these analytical approaches will aid theoretical studies of phytoplankton patchiness but also improve sampling strategies in the field that utilize autonomous, in situ instrumentatio

Light fluctuations are key in modulating plankton trophic dynamics and their impact on primary production

Surface‐ocean mixing creates dynamic light environments with predictable effects on phytoplankton growth but unknown consequences for predation. We investigated how variations in average mixed‐layer (ML) irradiance shaped plankton trophic dynamics by incubating a Northwest‐Atlantic plankton community for 4 days at high (H) and low (L) light, followed by exposure to either sustained or reversed light intensities. In deep‐ML (sustained L), phytoplankton biomass declined (μ = −0.2 ± 0.08 d−1) and grazing was absent. In shallow‐ML (sustained H), growth exceeded grazing (μ = 0.46 ± 0.07 d−1; g = 0.32 ± 0.04 d−1). In rapidly changing ML‐conditions simulated by switching light‐availability, growth and grazing responded on different timescales. During rapid ML‐shoaling (L to H), μ immediately increased (0.23 ± 0.01 d−1) with no change in grazing. During rapid ML‐deepening (H to L), μ immediately decreased (0.02 ± 0.09 d−1), whereas grazing remained high (g = 0.38 ± 0.05 d−1). Predictable rate responses of phytoplankton growth (rapid) vs. grazing (delayed) to measurable light variability can provide insights into predator‐prey processes and their effects on spatio‐temporal dynamics of phytoplankton biomass

Persistent Intra-Specific Variation in Genetic and Behavioral Traits in the Raphidophyte, Heterosigma akashiwo

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