Substantial energy expenditure for locomotion in ciliates verified by means of simultaneous measurement of oxygen consumption rate and swimming speed

Abstract

SUMMARY In order to characterize the energy expenditure of Paramecium, we simultaneously measured the oxygen consumption rate, using an optic fluorescence oxygen sensor, and the swimming speed, which was evaluated by the optical slice method. The standard metabolic rate (SMR, the rate of energy consumption exclusively for physiological activities other than locomotion)was estimated to be 1.18×10–6 J h–1cell–1 by extrapolating the oxygen consumption rate into one at zero swimming speed. It was about 30% of the total energy consumed by the cell swimming at a mean speed of 1 mm s–1, indicating that a large amount of the metabolic energy (about 70% of the total) is consumed for propulsive activity only. The mechanical power liberated to the environment by swimming Paramecium was calculated on the basis of Stokes' law. This power, termed Stokes power, was 2.2×10–9 J h–1 cell–1, indicating extremely low efficiency (0.078%) in the conversion of metabolic power to propulsion. Analysis of the cost of transport (COT, the energy expenditure for translocation per units of mass and distance) revealed that the efficiency of energy expenditure in swimming increases with speed rather than having an optimum value within a wide range of forced swimming, as is generally found in fish swimming. These characteristics of energy expenditure would be unique to microorganisms, including Paramecium, living in a viscous environment where large dissipation of the kinetic energy is inevitable due to the interaction with the surrounding water.

Load Response of the Flagellar Beat

“…Previous estimates for η reported values in the range η = 0.1 − 0.4 [36][37][38][39], see also SM. In our theory, we assume an active flagellar driving force that is independent of external load.…”

Propulsion of swimming microrobots inspired bymetachronal wavesin ciliates: from biology to material specifications

“…the motion within a channel). As a matter of fact, the prolate spheroid is a good approximation of the shape of the body of many ciliates, such as those of the genus Paramecium [24] (see Figure 2). The spheroid can be defined by the expression of its surface that, in a cylindrical reference frame rφz (adopted only as an auxiliary reference system for defining the variables related to the micro-swimmer), reads…”

“…Nevertheless, not all the parameters needed for this modelling work are usually measured, and, if so, they are often extracted in different and particular conditions. For Paramecium caudatum we found in [24] a set of values including dimensions a and b, beating frequency of cilia f (corresponding to the frequency of the travelling-wave deformation) and speed of motion v P c . The values of other parameters, such as amplitudes of deformation d ⊥ and d and the wavelength λ, were chosen within their typical ranges of variability generally found in Paramecia.…”

Evaluating efficiency and robustness in cilia design

“…In contrast, the energetic cost associated with locomotion consumes a significant portion of the metabolic budget in almost all motile organisms [21], thus justifying the need for an optimal or quasi-optimal gait. This is also true in cilia-driven locomotion such as in the protozoan Paramecium [22]. The Paramecium uses more than half its total energy consumption for swimming, while its hydrodynamic swimming efficiency is estimated to be as low as 0.77%.…”