Teamwork in the viscous oceanic microscale

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Kanso, E. A., Lopes, R. M., Strickler, J. R., Dabiri, J. O., & Costello, J. H. Teamwork in the viscous oceanic microscale. Proceedings of the National Academy of Sciences of the United States of America, 118(29), (2021): e2018193118, https://doi.org/10.1073/pnas.2018193118.Nutrient acquisition is crucial for oceanic microbes, and competitive solutions to solve this challenge have evolved among a range of unicellular protists. However, solitary solutions are not the only approach found in natural populations. A diverse array of oceanic protists form temporary or even long-lasting attachments to other protists and marine aggregates. Do these planktonic consortia provide benefits to their members? Here, we use empirical and modeling approaches to evaluate whether the relationship between a large centric diatom, Coscinodiscus wailesii, and a ciliate epibiont, Pseudovorticella coscinodisci, provides nutrient flux benefits to the host diatom. We find that fluid flows generated by ciliary beating can increase nutrient flux to a diatom cell surface four to 10 times that of a still cell without ciliate epibionts. This cosmopolitan species of diatom does not form consortia in all environments but frequently joins such consortia in nutrient-depleted waters. Our results demonstrate that symbiotic consortia provide a cooperative alternative of comparable or greater magnitude to sinking for enhancement of nutrient acquisition in challenging environments.We are grateful to Y. Garcia for help with organism sampling and sorting. E.A.K. is funded by NSF-2100209, NSF RAISE IOS-2034043 and NIH R01 HL 153622-01A1. R.M.L. is a CNPq research fellow (grant # 310642/2017-5). J.H.C. and J.O.D. are funded by Grant NSF-2100705

Grazing in a turbulent environment: Behavioral response of a calanoid copepod, Centropages hamatus

Models of marine ecosystem productivity rely on estimates of small-scale interactions, particularly those between copepods and their algal food sources. Rothschild and Osborn [Rothschild, B. J. & Osborn, T. R. (1988) J. Plankton Res. 10, 465-474], hypothesized that small-scale turbulence in aquatic systems increases the perceived abundance of prey to predators. We tested this hypothesis by exposing the planktonic copepod Centropages hamatus to turbulent and nonturbulent environments at different prey concentrations. Our results fell into two main categories. First, the response to turbulence was characterized by an initial period having a high number of escape reactions. This period was followed by one of increased foraging. C. hamatus responded to the higher encounter rates due to turbulence as if it were experiencing altered prey concentrations. Second, the termination of turbulence resulted in an increased foraging response, which was not directly related to the encounter rate. Functional response curves do not adequately explain this foraging response because the time course of the foraging response depends on prior encounter experience and foraging motivation

The Ciliate Paramecium Shows Higher Motility in Non-Uniform Chemical Landscapes

We study the motility behavior of the unicellular protozoan Paramecium tetraurelia in a microfluidic device that can be prepared with a landscape of attracting or repelling chemicals. We investigate the spatial distribution of the positions of the individuals at different time points with methods from spatial statistics and Poisson random point fields. This makes quantitative the informal notion of “uniform distribution” (or lack thereof). Our device is characterized by the absence of large systematic biases due to gravitation and fluid flow. It has the potential to be applied to the study of other aquatic chemosensitive organisms as well. This may result in better diagnostic devices for environmental pollutants.University of Wisconsin--Milwaukee (SURF (Salary for Undergraduate Research Fellows) Award)National Science Foundation (U.S.) (grant DMS-016214

Fluid Mechanics of Plankton

These first lines of Hensen’s article (Figure 1) in the “Fünfter Bericht” (1887) translate as follows [...

Planktonic copepods reacting selectively to hydrodynamic disturbances

In the water column, planktonic copepods encounter small-scale hydrodynamic disturbances generated by fellow zooplankters. Our question is whether or not the copepods can distinguish between hydrodynamic disturbances created by predators, prey, conspecifics and/or mates. We used a Schlieren optical system with a density gradient in the water volume and filmed at 48 frames per second to record the behaviour of copepods during encounters with an artificial hydrodynamic disturbance. We observed the reactions of Cyclops scutifer and Epischura nordenskioldi towards disturbances of different strengths. We also re-examined an earlier report on tandem swimming in C. scutifer while attempting to mate, using novel mathematical tools to analyse possible correlations between the two mates. We conclude that the information within the hydrodynamic disturbances created by swimming zooplankters has enough content for differentiated reactions. We also suggest that the adaptive value of tandem swimming during mating results in offspring capable of executing escape reactions comparable in strength to the disturbances

Functional Significance of the Sexual Dimorphism in the Cephalic Appendages of Euchaeta Rimana Bradford

In Euchaeta rimana the cephalic appendages become profoundly sexually dimorphic at the final molt. The enlarged maxillipeds and robust maxillae, which are related to the predatory nature of this pelagic marine copepod are fully functional on the fifth copepodid (CV) males and adult females. The presumed prey detection sensory apparatus, a paired 4-point setal array on the antennules, is located within the capture volume of the feeding current of the CVs and adult females. SEMs reveal specialized basal articulations of the straight and curved setae of this array, that allow setal rotations that streamline the antennule during escape movements. In the final molt of the CV male to the adult stage, the maxillae are reduced to vestiges and the maxillipeds to half the size of the female's. The loss of functional prey capture appendages is accompanied by the loss of the prominent antennulary setal array, giving support for their postulated function as prey sensors. Instead, the male gains 19 more aesthetascs primarily in the proximal region of the antennules, where fluid velocities of the scanning current are greatest. Detection of pheromones transported within the feeding/scanning current is the hypothesized function of the chemosensory system of the adult male copepod. The parallel changes in the structure of the antennule as well as of the adjacent cephalic appendages suggest that a homeobox-like gene control system could be coordinating these morphological changes

Copepod flow modes and modulation: a modelling study of the water currents produced by an unsteadily swimming copepod

Video observation has shown that feeding-current-producing calanoid copepods modulate their feeding currents by displaying a sequence of different swimming behaviours during a time period of up to tens of seconds. In order to understand the feeding-current modulation process, we numerically modelled the steady feeding currents for different modes of observed copepod motion behaviours (i.e. free sinking, partial sinking, hovering, vertical swimming upward and horizontal swimming backward or forward). Based on observational data, we also reproduced numerically a modulated feeding current associated with an unsteadily swimming copepod. We found that: (i) by changing its propulsive force, a copepod can switch between different swimming behaviours, leading to completely different flow-field patterns in self-generated surrounding flow; (ii) by exerting a time-varying propulsive force, a copepod can modulate temporally the basic flow modes to create an unsteady feeding current which manipulates precisely the trajectories of entrained food particles over a long time period; (iii) the modulation process may be energetically more efficient than exerting a constant propulsive force onto water to create a constant feeding current of a wider entrainment range. A probable reason is that the modulated unsteady flow entrains those water parcels containing food particles and leaves behind those without valuable food in them

Oscillations in the near-field feeding current of a calanoid copepod are useful for particle sensing

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Giuffre, C., Hinow, P., Jiang, H., & Strickler, J. R. Oscillations in the near-field feeding current of a calanoid copepod are useful for particle sensing. Scientific Reports, 9(1), (2019): 17742, doi: 10.1038/s41598-019-54264-1.Calanoid copepods are small crustaceans that constitute a major element of aquatic ecosystems. Key to their success is their feeding apparatus consisting of sensor-studded mouth appendages that are in constant motion. These appendages generate a feeding current to enhance the encounter probability with food items. Additionally, sensing enables the organism to determine the position and quality of food particles, and to alter the near-field flow to capture and manipulate the particles for ingestion or rejection. Here we observe a freely swimming copepod Leptodiaptomus sicilis in multiple perspectives together with suspended particles that allow us to analyse the flow field created by the animal. We observe a highly periodic motion of the mouth appendages that is mirrored in oscillations of nearby tracer particles. We propose that the phase shift between the fluid and the particle velocities is sufficient for mechanical detection of the particles entrained in the feeding current. Moreover, we propose that an immersed algal cell may benefit from the excitation by increased uptake of dissolved inorganic compounds.We acknowledge funding from the Simons Foundation (grant #278436 to PH) during two visits of HJ to Milwaukee. HJ was also supported by NSF grant OCE-1559062. We thank Dr. Russell Cuhel (School of Freshwater Sciences, University of Wisconsin - Milwaukee) for collecting the animals from Lake Michigan and four unknown readers for valuable comments