J. Fluid Mech. (2024), vol. 978, R1, doi:10.1017/jfm.2023.

849

Eukaryotic swimming cells are shaped by

hydrodynamic constraints

Maciej Lisicki1, †, ‡, Marcos F. Velho Rodrigues2, ‡ and Eric Lauga2, †

1 Faculty
of Physics, University of Warsaw, Warsaw, Pasteura 5, 02-093 Warsaw, Poland
2 Department of Applied Mathematics and Theoretical Physics, University of Cambridge,
Wilberforce Road, Cambridge CB3 0WA, UK

(Received 25 July 2023; revised 25 September 2023; accepted 3 October 2023)

Eukaryotic swimming cells such as spermatozoa, algae or protozoa use flagella or cilia
to move in viscous fluids. The motion of their flexible appendages in the surrounding
fluid induces propulsive forces that balance viscous drag on the cells and lead to a directed
swimming motion. Here, we use our recently built database of cell motility (BOSO-Micro)
to investigate the extent to which the shapes of eukaryotic swimming cells may be optimal
from a hydrodynamic standpoint. We first examine the morphology of flexible flagella
undergoing waving deformation and show that their amplitude-to-wavelength ratio is near
that predicted theoretically to optimise the propulsive efficiency of active filaments. Next,
we consider ciliates, for which locomotion is induced by the collective beating of short
cilia covering their surface. We show that the aspect ratios of ciliates are close to that
predicted to minimise the viscous drag of the cell body. Both results strongly suggest a key
role played by hydrodynamic constraints, in particular viscous drag, in shaping eukaryotic
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

swimming cells.
Key words: micro-organism dynamics, swimming/flying

1. Introduction
The cellular scale is home to a wide variety of biological swimmers, both in the prokaryote
and eukaryote domains (Yates 1986). Examples that have long been studied comprise the
spermatozoa of animals (including humans) (Gaffney et al. 2011), algae and planktonic
aquatic organisms (Pedley & Kessler 1992; Guasto, Rusconi & Stocker 2012; Goldstein
2015), protozoa (Jahn & Votta 1972) and bacteria (Lauga 2016). Prokaryotic swimmers
exploit the rotation of passive helical filaments to self-propel (Berg & Anderson 1973).
In contrast, swimming eukaryotes employ a more complex propulsion machinery in which

† Email addresses for correspondence: [email protected], [email protected]

‡ These authors contributed equally to this work.
© The Author(s), 2023. Published by Cambridge University Press 978 R1-1
 M. Lisicki, M.F. Velho Rodrigues and E. Lauga
flexible flagella actuated internally by molecular motors deform periodically in a wave-like
motion (Bray 2000).
During recent decades, the biophysical and fluid mechanics communities have devoted
considerable effort to quantify the interactions between cells and surrounding fluids
(Lighthill 1975, 1976; Lauga 2020a). Most studies use mathematical, or computational,
modelling to rationalise the dynamics of cells, from individual motion in bulk fluids
to collective interactions in complex environments (Lauga & Powers 2009; Koch &
Subramanian 2011; Elgeti, Winkler & Gompper 2015). These theoretical tools have in turn
allowed the impact of fluid forces on shaping the geometry and kinematics of swimming
cells to be explored, allowing in particular posing cellular swimming as an optimisation
problem, with notable successes.
In the case of bacteria, in search of an optimal prokayotic flagellum, Purcell (1997)
determined using simple arguments the shape of the most efficient helical propeller.
A later theoretical study of the polymorphic forms of the flagellum commonly found in
most bacteria by Spagnolie & Lauga (2011) showed that the so-called ‘normal’ helical
form is the most efficient by some significant margin, suggesting that fluid mechanical
forces may have played a role in the evolution of the flagellum. In addition to the flagellum,
overall swimming efficiency is also impacted by the shape of the cell body, as first shown
and optimised by Fujita & Kawai (2001) for a monotrichous bacterium. Recent work
considered the impact of other biological constraints on bacterial shape (Schuech et al.
2019).
In eukaryotic cells, optimal propulsion strategies result from an interplay between fluid
dynamics, elasticity and active driving mechanisms. In a study of over 400 mammalian
species, Tam & Hosoi (2011a) discovered that spermatozoa have an optimal tail-to-head
length ratio and that their most efficient swimming mode involves symmetrical,
non-sinusoidal travelling waves in the tail. Such travelling waves have been shown in many
contexts to lead to optimal motion in an active flagellum (Pironneau & Katz 1974, 1975;
Lauga 2020b). Lighthill (1975) found the two-dimensional hydrodynamically optimal
travelling-wave profile to be sawtooth-like, but the singular kinks are regularised by elastic
stresses (Spagnolie & Lauga 2010) or by properly modelling the irreversible work of
molecular motors within the active flagellum (Lauga & Eloy 2013). In ciliated organisms,
the beating pattern of individual cilia has also been shown to be optimal for propulsion
(Osterman & Vilfan 2011; Eloy & Lauga 2012). However, flagellar gaits may have local
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

optima, suited e.g. to distinct feeding and swimming modes, as investigated by Tam &
Hosoi (2011b) for biflagellated phytoplanktons. In larger organisms, multi-ciliated cells
can increase their efficiency by choosing an optimal number of cilia (from hundreds to
thousands) (Omori, Ito & Ishikawa 2020) and both optimal swimming and feeding have
been shown to involve surface metachronal waves (Michelin & Lauga 2010, 2011).
Beyond biological systems, the question of optimality has received a lot of attention in
the realm of biomimetic and engineered artificial swimmers. For example, swimming gaits
and shapes maximising swimming efficiency have been determined for simple swimmers
with only a few degrees of freedom (Tam & Hosoi 2007; Alouges, DeSimone & Lefebvre
2008; Golestanian & Ajdari 2008; Alouges, DeSimone & Lefebvre 2009; Nasouri,
Vilfan & Golestanian 2019), two-dimensional cell shapes (Avron, Gat & Kenneth 2004;
Montenegro-Johnson & Lauga 2014) and idealised kinematics of treadmilling (Leshansky
et al. 2007) or surface slip flow driven swimmers (Vilfan 2012). Other studies have sought
shapes that would minimise absolute dissipation (Nasouri, Vilfan & Golestanian 2021).
In this paper, we use data analysis to discover remarkable optimal properties of the
geometry of cell shapes. We rely on our recently assembled BOSO-Micro database
(Rodrigues, Lisicki & Lauga 2021): a comprehensive collection of data from the
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 Eukaryotic swimming shaped by hydrodynamic constraints
experimental literature on cellular swimming that contains data on swimming speed
and morphological characteristics of 382 unicellular organisms, including spermatozoa.
Building on the data, we first demonstrate that the amplitude-to-wavelength aspect ratios
of flagellated eukaryotes, including spermatozoa, are very close to the optimum predicted
by hydrodynamic theory. Next, we demonstrate that the aspect ratios (length-to-width) of
ciliate cell bodies are well predicted by the classical result for the shape of minimum drag
force subject to a fixed-volume constraint.

2. Results
The BOSO-Micro database (Rodrigues et al. 2021) provides us with novel means to
examine swimming and morphological relationships across species. The open-source
database contains swimming and morphological data published in scientific literature to
date; we refer to the original paper for all details on data-gathering. Apart from swimming
speed, many past investigations also contain data on the basic morphology of organisms,
such as the size and shape of the cell body, or the length and number of flagella or
cilia. Note that, in the database, the measurements and characterisation of organisms have
been performed under different physiological conditions and in various environments, and
therefore they do not represent a uniform sample. In cases where multiple values were
reported for the morphology of swimming cells, we used average values.

2.1. Propulsion of flagellated eukaryotes

First, we focus on studies providing the details of actuation in flagellated eukaryotes
and spermatozoa. We assume that the waveform of their flagellar oscillations can be
captured by a characteristic amplitude h and wavelength λ, as sketched in figure 1(a). The
database contains 23 different species of flagellated eukaryotes and 28 different species
of spermatozoa for which we found measurements of h and λ; note that these values were
either directly reported in each paper, or were estimated by us using experimental images,
see details in Rodrigues et al. (2021).
For all our data, we plot in figure 1(b) the histogram of the amplitude-to-wavelength
aspect ratio, h/λ. This ratio does not exceed 0.6 in the data set, with most organisms
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

showing the value below 0.25; hence the amplitude of a flagellar beat rarely exceeds
a quarter of the wavelength. For further insight, we plot the amplitude h against the
wavelength λ in figure 1(c). When multiple values are inferred for the same species, we
plot in figure 1(c) the average value but include error bars to reflect the variability within
the data reported for each species. Square markers represent flagellated eukaryotes, which
are generally smaller in size as compared with spermatozoa, marked with circles.
It is clear from the data in figure 1(c) that there is a systematic increase of flagellar
amplitude with wavelength. To rationalise and interpret these results, we performed a
least-squares linear fit of the h/λ = constant relationship to the data. The solid line shows
the result of fitting, with the 95 % confidence interval shaded in grey. For comparison
with theoretical predictions, we use the work of Lauga & Eloy (2013) who computed
numerically the optimal shape of an active flagellum. They considered an internally forced,
elastic planar flagellum deforming periodically and moving at a constant speed through a
viscous fluid and found the shape of the flagellum that maximises the swimming speed at
a fixed energetic cost, representing irreversible work of molecular motors. They concluded
that the optimal shape of the beating flagellum depends on a single dimensionless
combination of parameters, termed the Sperm number Sp (Lauga 2020a), and defined
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 M. Lisicki, M.F. Velho Rodrigues and E. Lauga
(a) (b) (c)
10
10
8

Cell count

h (µm)
6

λ 4 1
2h

0
0.1 0.2 0.3 0.4 0.5 0.6 10 40 90
h/λ λ (µm)
Dinophyceae Chlorophyceae Insecta
Echinoidea
Kinetoplastea Bicosoecida Mammalia Least squares 95% C.I.
Actinopterygii
Euglenida (Euglenophyceae) Prymnesiophyceae Amphibia Sp = 4
Aves
Zoomastigophora Dictyochophyceae Polychaeta Sp = 6
Bivalvia
Chrysophyceae Euglenida (Aphagea) Ascidiacea (Tunicata)

Figure 1. Aspect ratio of eukaryotic flagellar waves. (a) Sketch of flagellated eukaryotic cell with wave
amplitude h and wavelength λ. (b) Histogram of aspect ratios h/λ from experiments gathered in the
BOSO-Micro database (Rodrigues et al. 2021). (c) Mean value of h vs λ for all flagellated eukaryotes in our
database. Spermatozoa are marked with circles, while the remaining flagellated eukaryotes are marked with
squares. The solid line shows the least-square fit to the data and the shaded area is the 95 % confidence interval.
The dashed line shows the prediction from the optimal theory from Lauga & Eloy (2013) for Sp = 4 and the
dotted line for Sp = 6. Cells from the same class in the tree of life are plotted using the same colour scheme,
with all classes represented here listed in the inset of (b).

as the ratio of the wavelength λ to the elasto-hydrodynamic penetration length ,

 1/4
λ TB
Sp = , with  = , (2.1)
 ζ⊥
where T is the period of oscillatory actuation, B the bending rigidity of the flagellum,
and ζ⊥ the perpendicular resistance coefficient of the flagellum (i.e. the hydrodynamic
force exerted on the flagellum per unit length for motion in the fluid perpendicular to its
centreline). Thus the flagellum shape results from an interplay between the stiffness of the
filament, viscous drag of the medium and internal forcing. Accordingly, decreasing the
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

value of Sp results in flatter, smoother kinks in the flagellar beating (Lauga & Eloy 2013).
The typical values of the dimensionless Sp number for eukaryotes and spermatozoa
have been reported to be within the range of 1–10 (Kumar et al. 2019). For sea-urchin
Arbacia punctulata spermatozoa, Pelle et al. (2009) reported a bending rigidity of
B ≈ 0.4–0.9 × 10−21 Nm2 , while Howard (2001) assumes it to be the upper limit
of that range. In direct measurements, Okuno & Hiramoto (1979) found the stiffness
of echinoderm sperm flagella to be in the range of B ≈ 0.3–1.5 × 10−21 Nm2 , while
for Strongylocentrotus purpuratus, Okuno et al. (1981) estimated B ≈ 0.8 × 10−21 Nm2 .
Mechanical measurements for the flagella of wild-type Chlamydomonas yield B =
(0.84 ± 0.28) × 10−21 Nm2 (Xu et al. 2016), with similar values for mutant strains. In
water, we have ζ⊥ ≈ 2 × 10−3 Pa s, and the typical periods T vary across species from 0.02
to 0.05 s (Brennen & Winet 1977; Gray 1955; Rodrigues et al. 2021). From these numbers,
and typical lengths of dozens of µm (Rodrigues et al. 2021), we therefore estimate the
values of Sp to be in the range of Sp ≈ 2–7.
To compare the experimental measurements to predictions from theory, we use the work
of Eloy & Lauga (2012) where, for a given value of Sp, the shape of the optimal flagellum
was computed; for each optimal shape, we can then extract the corresponding optimal
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 Eukaryotic swimming shaped by hydrodynamic constraints
(a) (b) (c)
25
103
20
Cell count

B (µm)
15
B
102
10

0 101
W 2 4 6 8 10 101 102 103
B/W W (µm)
Litostomatea Heterotrichea Colpodea Least squares 95 % C.I.
Nassophorea
Spirotrichea Opalinea Parabasalia Optimal fixed-volume
Karyorelictea
Prostomatea Oligohymenophorea Armophorea Optimal fixed-area

Figure 2. Aspect ratio of ciliates cell body. (a) Sketch of ciliate body showing the cell width W and length B.
(b) Histograms of cell aspect ratios W/B from experimental data gathered in the BOSO-Micro database
(Rodrigues et al. 2021). (c) Mean value of body length B (in µm) plotted as a function of width W (in µm)
for all species in our database. The solid line shows the least-square fit to the data while the shaded area
is the 95 % confidence interval. The dashed line shows the prediction from the theory of fixed-volume drag
minimisation (B/W = 1.952) (Pironneau 1973) while the dotted line shows the drag minimum for a given
surface area (B/W = 4.037) (Montenegro-Johnson & Lauga 2015). Cells from the same class in the tree of life
are plotted using the same colour scheme, with all classes represented here listed in inset of (b).

aspect ratio, h/λ. In figure 1(c) we plot the aspect ratio as a linear curve h/λ = constant
for Sp = 4 (h/λ = 0.163, dashed line) and Sp = 6 (h/λ = 0.194, dotted line). Both lines
lie within the 95 % confidence interval of our dataset: the best fit for the data yields an
aspect ratio h/λ = 0.188, with the lower and upper bound of the 95 % confidence interval
at 0.163 and 0.213, respectively (R2 = 0.562).

2.2. Hydrodynamic drag force on ciliates

Ciliates constitute a large group of unicellular eukaryotic swimmers, characterised by
the presence of hair-like cilia which cover their bodies in dense active carpets; a model
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

organism, Paramecium, is sketched in figure 2(a). The internal structure of cilia is identical
to eukaryotic flagella but they are typically shorter and used to propel cells with relatively
much larger body sizes. This separation of scales has motivated mathematical models
dating back to Blake (1971) to represent the action of cilia layers covering the cell
bodies as a continuum boundary with prescribed actuation of the surrounding fluid.
This surface forcing sets the fluid in motion, and leads to swimming. The balance of
propulsion force and viscous drag force on the cell body determines the swimming
speed U (Lauga 2020a). Because the latter results from the overall shape of the body,
one possibility for cells to increase their swimming speed is to reduce the viscous drag
opposing their propulsion by choosing the appropriate drag-minimising shape, which have
been characterised theoretically (Pironneau 1973, 1974; Montenegro-Johnson & Lauga
2014).
To investigate if cells aligned with expectations from drag minimisation, we use our
eukaryotic microswimmers database (Rodrigues et al. 2021) to quantify the extent to which
the cell bodies of ciliates minimise drag forces. In figure 2(b), we plot the histogram for
the aspect ratio of the cell bodies, B/W, of the 91 ciliates in our database. When multiple
values were available for the same species, we use their average. Colours are used to code
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 M. Lisicki, M.F. Velho Rodrigues and E. Lauga
different classes of organisms. Clearly, the reported cells are typically prolate, and most of
them have a length of approximately twice their width, although more slender cell bodies
are also observed.
To further explore the correlation between the two length scales characterising the cell
bodies of ciliates, we present in figure 2(c) a scatter plot of the data, which suggests a
linear correlation between cell body and width. We plot the linear least-square fit to the
data with a solid line, corresponding to the slope B/W = 2.360 (R2 = 0.503), while grey
shading marks the 95 % confidence interval, for aspect ratios in the range (2.057, 2.664).
Remarkably, these results are very close to the classical prediction of a minimal-drag shape
in Stokes flow by Pironneau (1973), later computed by Bourot (1974), who demonstrated
numerically that the aspect ratio B/W = 1.952 is hydrodynamically optimal for bodies
with prescribed volumes (the corresponding optimal shape resembles a prolate spheroid
with pointy ends). We mark this theoretical prediction with a dashed line in figure 2(c), and
note that it lies just outside the confidence interval of our fit to data. In contrast, if instead
one considers the shape that has minimum drag for a prescribed surface area (instead of a
fixed volume), Montenegro-Johnson & Lauga (2014) found the optimal aspect ratio to be
4.037, marked in figure 2(c) with the dotted line; this lies well outside the data.
It is worth noting that the Stokes drag acting on an optimal fixed-volume prolate shape
is only 4.5 % less than that experienced by a sphere of the same volume, suggesting that
the energetic cost of diverting from the optimum is actually relatively low. It is therefore
perhaps all the more remarkable that such a small energetic gain seems to be reflected in
the empirical data. The small magnitude of the energetic improvement might in turn allow
a larger cell shape variability and explain the diversity of observed micron-scale shape
features.

3. Discussion
In this paper, we used morphological data gathered for swimming eukaryotic
microorganisms in the BOSO-Micro database which assembled published data from the
literature (Rodrigues et al. 2021) to test two outstanding questions regarding hydrodynamic
optimality of the geometric characteristics and shapes of the cells. First, we have shown
that for 51 different species of flagellated unicellular eukaryotes and spermatozoa, which
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

had the characteristics of their flagellar waves measured and reported in the literature, the
ratio of the wave amplitude to the wavelength was close to the optimal hydrodynamic
predictions for the shape of energetically optimal active filaments for Sperm numbers
comparable to estimates for natural swimmers. Second, we have analysed a dataset of
body widths and lengths of 91 species of ciliates and demonstrated that their cells have
an aspect ratio close to the theoretical optimum for the minimal drag on a body of a fixed
volume.
Our findings shed new light on the question of energetics of microscale swimming.
There is a long-standing argument in biophysics that the energetic cost of locomotion
is negligible when compared with metabolic constraints (Purcell 1977). Recent work
focusing on 169 species of eukaryotes has estimated that the operating costs of flagella
remain small, at a few per cent of the total energy budget, but flagellar construction costs
can be quite significant (Schavemaker & Lynch 2022). The results in the current work
strongly indicate that, in multiple species of swimming cells that span almost three orders
of magnitude in length, cellular shapes are consistent with energetic optimisation. This
remarkable agreement suggests that hydrodynamic forces might have played a key role in
shaping biological active swimmers.
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 Eukaryotic swimming shaped by hydrodynamic constraints
Clearly, not all swimmers in figures 1 and 2 follow exactly the theoretical curves.
Outliers in figure 1 that are the furthest from the best-fit line are Giardia lamblia,
cricket, worm, midge and rabbit spermatozoa (below the trend line), and Poteriodendron,
stick insect and fly spermatozoa (above the line). In figure 2 the outliers are
Halteria grandinella, Mesodinium rubrum (below the line) and Spirostomum spp. and
Trachelocerca spp. (above the line). Upon examining the shape of these specific organisms
we could not identify any systematic distinguishing features. Other factors are therefore at
play in determining the morphology of some species. In the case of bacteria, it is known
that cell shapes are the result of a delicate trade-off between efficient swimming, the
chemotaxis budget, and the costs related to cell construction (Schuech et al. 2019), which
points to the complexity of the overall energetic landscape.
Furthermore, in the case of ciliated organisms, minimising the drag force might not
be sufficient for maximising propulsion, since swimming is a balance between drag and
thrust. And yet, the available experimental data strikingly show that drag minimisation
appears to be important for ciliates, independently of the details of their propulsion
efficiency. We conjecture that this might stem from the necessity of these cells to not
only self-propel but also to respond to the external environmental flows to which they are
inevitably exposed.
Funding. This project has received funding from the European Research Council (ERC) under the European
Union’s Horizon 2020 research and innovation programme (grant agreement 682754 to EL), from the National
Science Centre of Poland (grant Sonata no. 2018/31/D/ST3/02408 to M.L.) and from Campus France (Eiffel
Scholarship no. 812884G to M.F.V.R.).

Declaration of interests. The authors report no conflict of interest.

Data availability statement. The data that support the findings of this study are openly available in the OSF
repository https://osf.io/4tyx6. They are also available and editable on GitHub: https://github.com/marcos-fvr/
BOSO-micro.

Author ORCIDs.
Maciej Lisicki https://orcid.org/0000-0002-6976-0281;
Marcos F. Velho Rodrigues https://orcid.org/0000-0002-8744-6966;
Eric Lauga https://orcid.org/0000-0002-8916-2545.

Author contributions. M.L. and M.F.V.R. contributed equally to this work.

https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

R EFERENCES
A LOUGES , F., D E S IMONE , A. & L EFEBVRE , A. 2008 Optimal strokes for low Reynolds number swimmers:
an example. J. Nonlinear Sci. 18, 277–302.
A LOUGES , F., D E S IMONE , A. & L EFEBVRE , A. 2009 Optimal strokes for axisymmetric microswimmers.
Eur. Phys. J. E 28, 279–284.
AVRON , J.E., GAT, O. & K ENNETH , O. 2004 Optimal swimming at low Reynolds numbers. Phys. Rev. Lett.
93, 186001.
B ERG , H.C. & A NDERSON , R.A. 1973 Bacteria swim by rotating their flagellar filaments. Nature 245,
380–382.
B LAKE , J.R. 1971 A spherical envelope approach to ciliary propulsion. J. Fluid Mech. 46, 199–208.
BOUROT, J.-M. 1974 On the numerical computation of the optimum profile in stokes flow. J. Fluid Mech. 65,
513–515.
B RAY, D. 2000 Cell Movements. Garland.
B RENNEN , C. & W INET, H. 1977 Fluid mechanics of propulsion by cilia and flagella. Annu. Rev. Fluid Mech.
9, 339–398.
E LGETI , J., W INKLER , R.G. & G OMPPER , G. 2015 Physics of microswimmers—single particle motion and
collective behavior: a review. Rep. Prog. Phys. 78, 056601.
E LOY, C. & L AUGA , E. 2012 Kinematics of the most efficient cilium. Phys. Rev. Lett. 109, 038101.

978 R1-7
 M. Lisicki, M.F. Velho Rodrigues and E. Lauga
F UJITA , T. & K AWAI , T. 2001 Optimum shape of a flagellated microorganism. JSME Intl J. Ser. C 44, 952–957.
GAFFNEY, E.A., GADELHA , H., S MITH , D.J., B LAKE , J.R. & K IRKMAN -B ROWN , J.C. 2011 Mammalian
sperm motility: observation and theory. Annu. Rev. Fluid Mech. 43, 501–528.
G OLDSTEIN , R.E. 2015 Green algae as model organisms for biological fluid dynamics. Annu. Rev. Fluid Mech.
47, 343–375.
G OLESTANIAN , R. & A JDARI , A. 2008 Analytic results for the three-sphere swimmer at low Reynolds
number. Phys. Rev. E 77, 036308.
G RAY, J. 1955 The movement of sea-urchin spermatozoa. J. Expl Biol. 32, 775–801.
G UASTO , J.S., RUSCONI , R. & S TOCKER , R. 2012 Fluid mechanics of planktonic microorganisms. Annu.
Rev. Fluid Mech. 44, 373–400.
H OWARD , J. 2001 Mechanics of Motor Proteins and the Cytoskeleton. Sinauer Associates.
JAHN , T.L. & VOTTA , J.J. 1972 Locomotion of protozoa. Annu. Rev. Fluid Mech. 4, 93–116.
KOCH , D.L. & S UBRAMANIAN , G. 2011 Collective hydrodynamics of swimming micro-organisms: living
fluids. Annu. Rev. Fluid Mech. 43, 637–659.
K UMAR , M., WALKAMA , D.M., G UASTO , J.S. & A RDEKANI , A.M. 2019 Flow-induced buckling dynamics
of sperm flagella. Phys. Rev. E 100, 063107.
L AUGA , E. 2016 Bacterial hydrodynamics. Annu. Rev. Fluid Mech. 48, 105–130.
L AUGA , E. 2020a The Fluid Dynamics of Cell Motility. Cambridge University Press.
L AUGA , E. 2020b Traveling waves are hydrodynamically optimal for long-wavelength flagella. Phys. Rev.
Fluids 5, 123101.
L AUGA , E. & E LOY, C. 2013 Shape of optimal active flagella. J. Fluid Mech. 730, R1.
L AUGA , E. & P OWERS , T.R. 2009 The hydrodynamics of swimming microorganisms. Rep. Prog. Phys. 72,
096601.
L ESHANSKY, A.M., K ENNETH , O., GAT, O. & AVRON , J.E. 2007 A frictionless microswimmer. New J.
Phys. 9, 126.
L IGHTHILL , J. 1975 Mathematical Biofluiddynamics. SIAM.
L IGHTHILL , J. 1976 Flagellar hydrodynamics—the John von Neumann lecture, 1975. SIAM Rev. 18, 161–230.
M ICHELIN , S. & L AUGA , E. 2010 Efficiency optimization and symmetry-breaking in an envelope model for
ciliary locomotion. Phys. Fluids 22, 111901.
M ICHELIN , S. & L AUGA , E. 2011 Optimal feeding is optimal swimming for all Péclet numbers. Phys. Fluids
23, 101901.
M ONTENEGRO -J OHNSON , T.D. & L AUGA , E. 2014 Optimal swimming of a sheet. Phys. Rev. E 89, 060701.
M ONTENEGRO -J OHNSON , T.D. & L AUGA , E. 2015 The other optimal stokes drag profile. J. Fluid Mech.
762, R3.
NASOURI , B., V ILFAN , A. & G OLESTANIAN , R. 2019 Efficiency limits of the three-sphere swimmer. Phys.
Rev. Fluids 4, 073101.
NASOURI , B., V ILFAN , A. & G OLESTANIAN , R. 2021 Minimum dissipation theorem for microswimmers.
Phys. Rev. Lett. 126, 034503.
O KUNO , M., A SAI , D.J., O GAWA , K. & B ROKAW, C.J. 1981 Effects of antibodies against dynein and tubulin
on the stiffness of flagellar axonemes. J. Cell Biol. 91, 689–694.
https://doi.org/10.1017/jfm.2023.849 Published online by Cambridge University Press

O KUNO , M. & H IRAMOTO , Y. 1979 Direct measurements of the stiffness of echinoderm sperm flagella. J.
Expl Biol. 79, 235–243.
O MORI , T., I TO , H. & I SHIKAWA , T. 2020 Swimming microorganisms acquire optimal efficiency with
multiple cilia. Proc. Natl Acad. Sci. USA 117, 30201–30207.
O STERMAN , N. & V ILFAN , A. 2011 Finding the ciliary beating pattern with optimal efficiency. Proc. Natl
Acad. Soc. USA 108, 15727–15732.
P EDLEY, T.J. & K ESSLER , J.O. 1992 Hydrodynamic phenomena in suspensions of swimming
microorganisms. Annu. Rev. Fluid Mech. 24, 313–358.
P ELLE , D.W., B ROKAW, C.J., L ESICH , K.A. & L INDEMANN , C.B. 2009 Mechanical properties of the
passive sea urchin sperm flagellum. Cell Motil. Cytoskel. 66, 721–735.
P IRONNEAU, O. 1973 On optimum profiles in stokes flow. J. Fluid Mech. 59, 117–128.
P IRONNEAU, O. 1974 On optimum design in fluid mechanics. J. Fluid Mech. 64, 97–110.
P IRONNEAU, O. & K ATZ , D.F. 1974 Optimal swimming of flagellated microorganisms. J. Fluid Mech. 66,
391–415.
P IRONNEAU, O. & K ATZ , D.F. 1975 Optimal swimming of motion of flagella. In Swimming and Flying in
Nature (ed. T.Y. Wu, C.J. Brokaw & C. Brennen), vol. 1, pp. 161–172. Plenum.
P URCELL , E.M. 1977 Life at low Reynolds number. Am. J. Phys. 45, 3–11.
P URCELL , E.M. 1997 The efficiency of propulsion by a rotating flagellum. Proc. Natl Acad. Sci. USA 94,
11307–11311.

978 R1-8
 Eukaryotic swimming shaped by hydrodynamic constraints
RODRIGUES , M.F.V., L ISICKI , M. & L AUGA , E. 2021 The bank of swimming organisms at the micron scale
(BOSO-Micro). PLoS One 16, e0252291.
S CHAVEMAKER , P.E. & LYNCH , M. 2022 Flagellar energy costs across the tree of life. eLife 11, e77266.
S CHUECH , R., H OEHFURTNER , T., S MITH , D.J. & H UMPHRIES , S. 2019 Motile curved bacteria are
pareto-optimal. Proc. Natl Acad. Sci. USA 116, 14440–14447.
S PAGNOLIE , S.E. & L AUGA , E. 2010 The optimal elastic flagellum. Phys. Fluids 22, 031901.
S PAGNOLIE , S.E. & L AUGA , E. 2011 Comparative hydrodynamics of bacterial polymorphism. Phys. Rev.
Lett. 106, 058103.
TAM , D. & H OSOI , A.E. 2007 Optimal stroke patterns for Purcell’s three-link swimmer. Phys. Rev. Lett. 98,
068105.
TAM , D. & H OSOI , A.E. 2011a Optimal kinematics and morphologies for spermatozoa. Phys. Rev. E 83,
045303.
TAM , D. & H OSOI , A.E. 2011b Optimal feeding and swimming gaits of biflagellated organisms. Proc. Natl
Acad. Soc. USA 108, 1001–1006.
V ILFAN , A. 2012 Optimal shapes of surface slip driven self-propelled microswimmers. Phys. Rev. Lett. 109,
128105.
X U, G., W ILSON , K.S., O KAMOTO , R.J., S HAO , J.-Y., D UTCHER , S.K. & BAYLY, P.V. 2016 Flexural
rigidity and shear stiffness of flagella estimated from induced bends and counterbends. Biophys. J. 110,
2759–2768.
YATES , G.T. 1986 How microorganisms move through water. Am. Sci. 74, 358–365.
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