Undergraduate Research Paper: Two Dimensional

Boundary Element Formulation of Flagellar Microorganisms

Swimming Motion in Microchannels
Metehan Çama

a Microfluidics and Lab-on-a-chip Research Group

Mechanical Engineering Department, İ.D. Bilkent University, 06800 Ankara, Turkey

Abstract

In this study, a special formulation to obtain rigid-body velocities of flagellar microorgan-

isms swimming within a microchannel is presented. The formulation is based on boundary
element method, and the large system matrices resulting from the analysis is reduced to a
system of linear equations with the unknowns being the rigid-body motion parameters of the
cell(s). This reduction is achieved through matrix multiplications which increases computa-
tional efficiency when compared with the solution of a large system of equations. Since the
formulation involves mainly matrix multiplications, parallelization is straightforward. With
the presented algorithm, only the position of the cell(s) are tracked through the solution of
their rigid-body velocities and an explicit time integration to obtain displacements. Due to the
boundary-only nature of the boundary element method, the cell swimming in close proximity
to the channel walls and the attractive effects of the channel walls on the swimming cell(s)
are very effectively modeled without any need for an adjustment. The presented method is
given in 2D, where the 3D formulation is straightforward. Current model is compared with
well-known flagellar hydrodynamics model named Resistive Force Theory. To demonstrate the
applicability of the method, besides the benchmark of our model with Resistive Force Theory,
thigmotaxis phenomenon is also studied. It is observed that present formulation offers an effi-
cient numerical model to be used for the simulation of the flagellar microorganism trajectory
for 2D microfluidic applications and can easily be extended for 3D multiphysics simulations.
Keywords: Boundary element method, Flagellar hydrodynamics, Stoke’s flow, Microfluidics

1 Introduction
Gray and Hancock in 1955 have developed one of the most prominent mathematical models in flagellar
hydrodynamics named as Resistive Force Theory, which was able to take the existence of an inert head
propelled by a flagellum into account unlikely to the previous works of Taylor and Hancock [1,2]. This
theory relates the tangential and normal components of the drag force induced by the surrounding fluid
on the flagellar cell to the coefficients of resistance, the transverse beating velocity of the flagellum and the
rigid body translation of the entire cell [1]. A flagellum can be modeled as a slender body, for which the
coefficient of resistance locally normal to the beating flagellum is ideally twice the coefficient of resistance
locally tangential to the flagellum. Gray and Hancock has showed that for the forward propulsion, the
Boundary Element Formulation of Flagellar Microorganisms Çam

coefficient of resistance in the normal direction should be greater than the coefficient in the tangential
direction. They concluded that the self-propulsive thrust induced by the microorganism is balanced by
the drag force induced by the surrounding fluid. The force equilibrium yields the corresponding swimming
velocities. Resistive Force Theory by its nature significantly depends on the accuracy of resistance coeffi-
cients. With the work of Lighthill in 1976 and Higdon in 1979, Slender-Body Theory has been improved
in which the Stokes equations were transformed into system of singular integral equations governing the
translational propulsive velocities, angular velocity and force distribution along the centerline of the flagel-
lum [2]. After Resistive Force Theory and Slender Body Theory, Boundary Element Method turns out to
be the third fundamental mathematical modelling framework, where the Stokes equations are written as
boundary integral equations using Somigliana identity and we integrate the fundamental solutions of the
Stokes equation over the boundary of the solution domain [3,4]. Therefore, Boundary Element Method re-
quires boundary-only discretization of the solution domain. In this study, we introduce a modified version
Impedance Formulation based on Boundary Element Method (BEM). The BEM has several advantages
over other numerical methods (such as the FEM or the FVM) most important of those, considering the
flagellar microorganisms swimming problem are listed below:

• The BEM models and discretizes only the boundary of the solution domain, which results in shorter
modeling times and less computational effort in remeshing. Also, since the boundary mesh need not
be continuous (at the nodes), parallel remeshing algorithms can be employed.

• The BEM is referred to as a ”semi-analytical” method, for the reason that it satisfies the weak form
derived from the governing equations in an exact sense (analytically), only the resulting boundary
integrals are solved numerically. Also it can be said that, the governing equations and continuity
and compatibility conditions within the solution domain are satisfied exactly; approximation errors
occur only due to the discretization of the boundary for the evaluation of the resulting integrals.
Therefore, the BEM provides better approximations.

• The derivative quantities, e.g. the flux or stress/strain within the solution domain is determined in
the BEM by analytical differentiation; therefore, such quantities can be determined more accurately
in the BEM when compared with the numerical methods that involve domain discretization.

• In BEM, we can carry out our analysis for microorganisms with distinct characteristics of beating
patterns and geometry. Additionally, we are not restricted in the geometry of the microchannel,
which allows us to design novel microchannel geometries, especially for microfluidic fertilization
devices, flagellar microorganism alike microrobots designing as well as bacterial and sperm focusing
and separation.

• Impedance Formulation is able to model multiple flagellar microorganisms simultaneously analyzing

the interaction of cells with any confinement in the solution domain and interaction within the
individual organisms.

• As one the formulation schemes of BEM, Impedance Formulation allows us to directly superpose
the effect of the external field on the swimming microorganisms as required in bacterial and sperm
manipulation employing dielectrophoretic, acoustophoretic and magnetic effects.

In this study, a formulation to track the motion of the flagellar microorganisms within a microchannel
flow is presented. The method involves the re-organization of the BE matrices that are evaluated for the
flow problem, and through several manipulations, reducing the problem to a linear system of equations
Boundary Element Formulation of Flagellar Microorganisms Çam

where the only unknowns are the motion parameters (eg., the translational and rotational velocities of
the centers of gravity) of the microorganisms [5]. With such manipulation, the dimension of the linear
system of equations to be solved is reduced drastically, resulting in a comparably fast solution. Since the
presented manipulations are all matrix multiplications, the procedure can easily be parallelized. To assess
the formulation presented, we utilize the Resistive Force Theory as the benchmark model. Impedance
Formulation is able to capture the hydrodynamic effects induced by the confinements on the swimming
microorganisms; therefore, besides the benchmark of the sea-urchin spermatozoa swimming in a quiescent
bulk of fluid, near surface swimming of flagellar microorganisms has been also analyzed to assess the
capabilities of the presented formulation [6]. This mathematical modelling framework offers an efficient
numerical model to be used for the simulation of the swimming microorganisms’ trajectory for microfluidic
applications and can easily be extended for 3D multiphysics simulations.

2 The boundary element formulation for Stoke’s flow

Boundary Element Method (BEM) is a numerical technique which is used in the solution of linear partial
differential equations and requires boundary-only discretization of solution domain. Boundary Element
Method originates from the integration of the free space Green’s functions defining the fundamental solu-
tions of governing equations of interest. Boundary Element Method converts partial differential equations
into integral equations using integral identities and in slow viscous flow, these identities are derived by
Lorentz and provide the starting point for the direct Boundary Element Method [3]. Due to the boundary-
only discretization of numerical method, field variables, velocity and traction values in Stoke’s flow, are
only defined on boundaries of the solution domain and if necessary, field variables inside the domain can
be obtained by postprocessing. In this section, the boundary element formulation of Stoke’s flow has been
explained.
Starting from the vector form of the Navier-Stokes Equations governing the viscous fluid dynamics of
self-propulsion,  
∂u
ρ + u · ∇u = −∇p + µ∇2 u + |{z}
f (2.1)
∂t | {z } | {z }
| {z } 2 3 4
1

To characterize the fluid flow, we employ the dimensionless Reynolds number formulated as follows,

U Lρ
Re = (2.2)
µ

,where U is the typical velocity scale, L is the characteristic length, which corresponds to the flagellum
length of the self-propelling micro-organisms, ρ is the fluid density and µ is the fluid viscosity. We consider
the self-propulsion characteristics of micro-organisms in a relatively low viscosity medium such as water,
with ρ ≈ 103 kg m-3 and µ ≈ 10−3 Pa s. For a typical human sperm cell, the flagellum length is 50µm
and the average swimming speed is 70µm/s [2]. Therefore, Reynolds number for a typical human sperm
turns out to be 3.5 · 10−3 << 1, which physically means that in the fluid dynamics of self-propulsion, the
viscous effects dominate the inertial effects, which validate the Stoke’s assumption. In this assumption,
we ignore the inertial terms in the Navier-Stokes Equations and assume steady flow, specifically terms
denoted with 1, corresponding to unsteady and convective accelerations respectively, in the equation 2.1.
At this point, we define a modified pressure as P = p − ρg · x where x represents the spatial coordinates
and ρg represents the body forces to incorporate the term denoted by 4 in the equation 2.1. For now, we
Boundary Element Formulation of Flagellar Microorganisms Çam

do not take any other body force into account. Therefore, for this fluid mechanics problem, we use the
following Stoke’s Equation as the governing equation, which models the flow by the motion of a fluid with
zero density (infinite viscosity),
−∇P + µ∇2 u = 0 (2.3)

,where u is the velocity vector (its components will be denoted as ui ). Denoting the components of the
hydrodynamic traction as ti on the boundary of the solution domain, the integral representation for the
Stoke’s Flow can be derived from Green’s formulae in 2D and can be stated as follows ;
Z Z
0 0 ∗ 0
Cij (X )ui (X ) = uij (X , x)tj (x)dS − p∗ij (X0 , x)uj (x)dS (2.4)
S S

In the equation 2.4, Cij = δij if X0 ∈ V and Cij = δij /2 if X0 is on a smooth boundary and 0 if X0 ∈
/ V . In
the equation 2.4 and in the following equations, unless otherwise is explicitly stated, Einstein’s summation
convention is used, which requires summation over a repeated index in the range of that index. In the
equation 2.4, u∗ij is the fundamental velocity known as Stokeslet and p∗ij is the fundamental traction known
as the stresslet. The fundamental solutions in the Boundary Element integral equations are in the form of:

1
u∗ij (X0 , x) = [− ln(r)δij + r,i r,j ] (2.5)
4πµ

r,i r,j ∂r r,i r,j

p∗ij (X0 , x) =
· = · r,i ni (2.6)
πr ∂n πr
for the two dimensional problems, where r = |X0 − x| and r,j = Xj0 − xj /r [1] . In the continuation

of this section, we will conclude that the fundamental solutions in the equations 2.5 and 2.6 will form
the system matrices, denoted by G and H, of the resultant linear system of equations. To be consistent,
starting from this point, we denote the fundamental velocity as Gij and the fundamental traction as Hij
and re-write the integral formulation in equation 2.4 as follows,
Z Z
Cij (X0 )ui (X0 ) = Gij (X0 , x)tj (x)dS − Hij (X0 , x)uj (x)dS (2.7)
S S

In this study, for boundary discretization of field variables as velocity and traction values, constant element
approach has been employed, where the variation of any field variable over the element is taken to be
constant with the value at the computational node of the element. Discretizing the boundary of the
solution domain with N constant elements, equation 2.7 can be written at a fixed point of X0l belonging
to the element l as:
1 l lk
ui + Hij · ukj = Glk k
ij · tj (2.8)
2
,where uli and ukj are the ith and j th components of the velocity vector evaluated at the nodes of the lth
and kth elements respectively, and similarly tkj is the j th component of the traction vector evaluated at
the node of the kth element, where the indices k and l trace all of the boundary elements as (l, k = 1...N ).
The terms Glk lk
ij and Hij can be formulated as follows,

Z Z
Glk
ij = Gij (X0l , xk ) ds & lk
Hij = Hij (X0l , xk ) ds (2.9)
Ck Ck

,where Ck represents the boundary of the kth element, xk represents the varied (integration) point over
the kth element’s boundary and X0l represents the fixed point from which the line integrals in the equation
2.9 are computed. For each fixed point denoted as xk , we trace all of the elements on the boundary as
Boundary Element Formulation of Flagellar Microorganisms Çam

l = 1, 2, ..., N and calculate the line integrals. In this study, in order to discretize the line integrals in the
equation 2.9, we employ Gaussian Quadrature which discretizes the definite integrals as follows,
Z b
f (x) dx (2.10)
a

,for which we employ the following change of variable,

b+a b−a b−a b−a

x= + ·τ & dx = · dτ → J = (2.11)
2 2 2 2

, where J represents the Jacobian of the transformation. Finally Gaussian Quadrature discretization is
completed as follows,
Z b Z +1 Z +1 N
b−a X
I= f (x) dx = f (x(τ )) · dx = F (τ ) · J dx = J · F (Tn ) · ωn (2.12)
a −1 2 −1 n=1

,where in the equation 2.12, Tn are the Gauss points defined within −1 to +1 and ωn are the Gauss weights
where the order of the Gaussian Quadrature is given by the number of terms in the series expansion, N .
After considering Gaussian Quadrature, if the diagonals Hllii are augmented with the coefficient of 1/2, we
can re-write the equation 2.8 as follows,

lk
Hij · ukj = Glk k
ij · tj (2.13)

The relation in equation 2.13 yields a set of 2N equations in terms of 4N unknowns:

H·u=G·t (2.14)

The imposition of the boundary conditions can be achieved by the column swapping within coefficient,
system, matrices as H and G after which the linear system of equations take the form as:

K·x=L·b (2.15)

,where x represents the unknowns vector and b represents the vector formed by the boundary conditions
of the system. Finally, we convert the linear system in equation 2.15 into the following resultant form:

A·x=b
b −→ A = K & b =L·b
b (2.16)

Consequently, by the constant element discretization of the boundary of the solution domain and Gaussian
Quadrature discretization of the line integrals of fundamental solutions, starting from the Green’s integral
identities, we have converted a linear partial differential equation, Stoke’s Equation, to a linear system of
equations.

2.1 Formulation of Particle Trajectory and Calculation of Rigid Body

Velocities
The resultant drag force on the particle can be determined by integrating the hydrodynamic-stress tensor,

Th = −pI + µ(∇u + ∇uT ), (2.17)

Boundary Element Formulation of Flagellar Microorganisms Çam

over the particle surface. From the above relation, we can find the hydrodynamic force on the particle.
After finding the resultant-net force on the particle, we can employ the Newton’s second law of motion to
calculate the acceleration and then the acceleration can be integrated to calculate the new position of the
particle. This approach can be applied for any geometry and it inherently includes the particle-particle
interaction and also the interaction of the particle with the field.
In this approach, we do not compute the rigid-body velocities directly; instead, an indirect time
integration of acceleration is employed. Additionally, this approach is computationally expensive, if domain
discretization as in Finite Element Method is needed, since as the particle or cell moves in the channel,
the mesh has to be updated constantly. However, Boundary Element Method only requires boundary-only
discretization; therefore, as the particle or cell moves, the meshes on the boundary move accordingly so
they are not required to be remeshed. They are just shifted,updated according to the calculated rigid-
body velocities. Since we keep track of the node points on the boundary, we do not have to carry out an
interpolation for the internal field variables, specifically velocity and traction values. Such an interpolation
is required in Finite Element Method, which inherently introduces an error. Due to these advantages,
Boundary Element Method is frequently utilized in particulate flows under the action of electrophoretic
and electro-osmotically driven flows.
The purpose of this study is to track the trajectory of flagellar microorganisms, specifically sper-
matozoon cells and amphitrichous bacteria. Therefore, the solution of the field variable on the channel
boundaries and the boundaries of the moving cell is of no practicle use; what is the most important is the
rigid motion parameters, that is, the translational and rotational velocities of the rigid-body. In this study,
we are going to utilize a modified version of Impedance Formulation, which credits to the studies of Argeso
and Mengi on poroelastic and poroviscoelastic media, and Yalcin and Mengi on wave load analysis. To
successfully model the self-propulsion phenomenon, we employ a modification on the classical version of
Impedance Formulation of Stokes Flow, which is designed to track the trajectories of the passive particles,
’passive’ means that the particles do not give any disturbance to the surrounding fluid, under the action
of electric, acoustic or magnetic field. Flagellar microorganisms are non-passive particles since they propel
themselves via the disturbance they give to the surrounding fluid by beating.
The imposition of boundary conditions requires, at all points of the defined boundary, the definition
of one and only one of the couples (um m
n , tn ), or a combination of the two, where m represents the node

number and n is the direction of the component of the vector. When the motion of a particle within the
fluid is considered, neither the velocity components nor the traction components nor a combination of the
two is known at a given element m. Instead we impose the rigid body motion conditions:

ui = uB
i + ωr t̂i (2.18)

where ui represents the velocity components of the node on the particle, uB

i are the velocity components

of the center of gravity (CG) of the particle, ω is the angular velocity of the particle about the CG, r
represents the distance from the corresponding node to the CG and t̂i are the components of the unit
vector that is normal to the line segment drawn from the CG of the particle to the node (the direction
of the normal is selected using right hand rule, counter-clockwise). In flagellar microorganisms, center
of gravity is taken as the centroid of the head since the great portion of the total mass of the cell is
concantrated on the head part, not on the flagella. If we were dealing with the passive particles, at each
Boundary Element Formulation of Flagellar Microorganisms Çam

particle node, a matrix relation as

uP = M · uB (2.19)

could be written where  


 u1 


 
 ( )
 u2
 
 u1
uP = .. ; with us = (2.20)

 . 
 u2

 
 s
 
uS
 

is the vector that contains the nodal velocities at the nodes of the particle boundary (s = 1..S represents
the node on the particle where S is the total number of nodes on the particle). Similarly,
n oT
uB = uB
1 uB
2 ω (2.21)

represents the rigid body velocity components of the particle center and M is a (2S × 3) matrix structured
as  

 M1 


 
 " #
 M2 (s)
r(s) t̂1
 
 1 0
M= ; with Ms = (2.22)
 ...
 
 0 1 r(s) t̂2
(s)

 

 
MS
 

(s)
In forming the Ms submatrices, the term r(s) represents the distance of the node to the CG and t̂i rep-
resents the components of the tangential vector field, normal to the line segment drawn from the center of
gravity of the particle to the node point, at the sth node. It should be noted that, the index s is contained
within parenthesis to emphasize that the summation convention is not used.

At this point, we have to employ an extremely important modification to capture the physics of the
self-propulsion phenomenon on the matrix relation given in equation 2.19. In passive particles, according
to an external observer, all of the nodes on the boundary move with the same velocities of the center
of gravity. Therefore, all of the nodes have the same net velocity values. However, flagellar microorgan-
isms have an undulating,beating flagellum. The beating flagellum’s geometry is modeled by the following
equation,
2π
y(x, t) = b(x)sin (k(x + Vw t)) where k= (2.23)
λ
,where b(x) = b · exp ( − kx/a) turns out to be the position-dependant amplitude function. In flagellar
microorganisms, as we move away from the connection part of the flagellum to the head,called nonbeating
midpiece, towards the end of the flagellum, beating amplitudes increase. To incorporate this increase,
we utilize an exponential function where a is the exponential envelope parameter and b is the uniform
amplitude of the beating flagellum. As the exponential envelope parameter a goes to infinity, the amplitude
of beating waves on the flagellum becomes uniform; therefore, to model microorganisms with smooth
amplitude beating, we input rather high numerical values for the a parameter. In the self-propulsion
phenomenon, the flagellum beat only in the transverse direction, specifically perpendicular to the axis of
propulsion of the cell. To find the prescribed beating velocities, we take the time derivative of the above
mathematical modelling for the flagellum as follows,
 
dy(x, t) 2πVw b −kx
Vbeating = = exp cos (k · (x + Vw t)) (2.24)
dt λ a
Boundary Element Formulation of Flagellar Microorganisms Çam

Regardless of the position of the flagellar microorganism with respect to the external observer, we have
to make sure that the beating velocities are always perpendicular to the instantaneous axis of propulsion
of the cell and are given as prescribed finite velocity- no slip boundary condition on the cell boundary as
follows,
Vx = −sin(θ) · Vbeating and Vy = cos(θ) · Vbeating (2.25)

,where θ is the relative angle between the cell-fixed frame and stationary microchannel (external observer)-
fixed frame depicted as in the following figure.

Figure 1: Transverse Beating Perpendicular to the Axis of Propulsion of the Cell

At this point, we can turn back to the details of the modification on Impedance Formulation. From the
above modelling, we know the beating velocities are prescribed by the mathematical formulation we use to
model the undulating flagellum. The flagellar microorganisms in general has three major parts as head and
midpiece, which are both unbeating parts of the cell and flagellum which is beating. When we carry out the
entire Impedance Formulation, we solve for the rigid body velocities at the center of gravity and we update
the meshes belonging to each of these three subparts with the same velocity values as computed at the
center of gravity. However, with respect to the stationary microchannel-fixed frame,which is regarded as the
external observer in our dynamic analysis, the meshes on the flagellum move with the rigid body
velocities of the center of gravity plus beat in the transverse direction with the prescribed
velocities. Equation 2.19 is the only equation that relates the velocity values on the particle to the rigid
body velocities of the center of gravity; therefore, we have to modify this relation in the following manner
to incorporate the fact that the flagellum has a relative beating velocity with respect to the center of
Boundary Element Formulation of Flagellar Microorganisms Çam

gravity of the translating and rotating microorganism,

uP = M · uB + uS (2.26)

,where the term uS represents the prescribed beating velocities, whose components belonging to the head
and midpiece are always zero and those belonging to the flagellum have prescribed velocity values found
from the equation 2.24. Now, let us continue with the force relations as well before we progress to the
insertion of modified uS term into the final form of the formulation. The force on any element can be
calculated through integration of the traction vectors on that element. In this study, constant elements
are employed, therefore this integration can be obtained simply using
Z Z
(s) (s) (s)
fi = ti (Ps )ds = ti ds = ti L(s) (2.27)
Cs Cs

where fi are the components of the force vector, Cs represents the element boundary, L(s) is the length of
the element and tsi are the traction components. The moment of this force about the CG is given by

(s) (s) (s) (s)

m(s) = r1 · f2 − r2 · f 1 (2.28)

(s)
where ri are the components of the relative position vector of the element node with respect to the CG
and the moment, m, is taken in counterclockwise sense. With Eq. 2.27 and 2.28, one can write the matrix
relation
f B = F · tP (2.29)

where  

 t1 


 
 ( )
 t2
 
 t1
tP = .. ; with ts = (2.30)

 . 
 t2

 
 s
 
tS
 

is the vector containing the traction components at each element,

n oT
fB = f1 f2 m (2.31)
B

is the augmented (with m) resultant force vector at the CG, and

 
h i 1 0
 
F= F1 F2 ··· FS ; with Fs = 
 0 1 
 (2.32)
(s) (s)
−r2 r1

is the coefficient matrix. At this point, we re-partition Eq. 2.14 to get

" # ( ) " # ( )
H00 H0P u0 G00 G0P t0
· = · (2.33)
HP 0 HP P uP GP 0 GP P tP

Here, the subscript 0 represents the corresponding variables are evaluated on the non-moving boundary
and the subscript P represents the same for moving (particle) boundary. Similarly, for coefficient matrices,
the first index represents the location of the fixed point (eg., if 0 fixed point is on non-moving else if P it
Boundary Element Formulation of Flagellar Microorganisms Çam

is on moving boundary) and the second index represents the location of the varied point (or the location
of the element being integrated). We assume the vector u0 is fully known and t0 is fully unknown, which
would not affect the formulation, if necessary column changes are made for unknown-known variables. For
instance, sometimes we give zero-traction boundary condition at the outlet of the microchanel to model
the continuation of the domain within the longitudinal direction. The first matrix row of Eq. 2.33 can be
written as:
H00 · u0 + H0P · uP = G00 · t0 + G0P · tP (2.34)

One can re-write this equation in terms of t0 as:

t0 = G−1 −1 −1
00 · H00 · u0 + G00 · H0P · uP − G00 · G0P · tP (2.35)

When the second set defined in Eq. 2.33 is written as:

HP 0 · u0 + HP P · uP = GP 0 · t0 + GP P · tP (2.36)

one can insert Eq. 2.35 into 2.36 to obtain

HP 0 · u0 + HP P · uP = GP 0 · G−1
00 · H00 · u0

+GP 0 · G−1
00 · H0P · uP

−GP 0 · G−1
00 · G0P · tP

+GP P · tP ,

which, when re-structured gives

B · tP = A · uP + C · u0 , (2.37)

where

HP P − GP 0 · G−1
 
A = 00 · H0P ,

GP P − GP 0 · G−1
 
B = 00 · G0P ,

HP 0 − GP 0 · G−1
 
C = 00 · H00 .

At this point it is important to note that, with N nodes on the non-changing boundary (eg., channel
walls and any motionless inclusion) and S nodes on the moving particle, the matrices A and B are of order
(2S × 2S) and the matrix C is of order (2S × 2N ). Note that, initially we have assumed u0 is known,
therefore we can replace the term C · u0 with a column vector b of order (2S × 1). From Eq. 2.37 one can
obtain
tp = B−1 · A · uP + B−1 · b (2.38)

At this point, we employ our modification formulated as uP = M · uB + uS and employ the force relation
formulated as f B = F · tP and insert to the above equation and get,

f B = F · B−1 · A · M · uB + F · B−1 · A · uS + F · B−1 · b (2.39)

Boundary Element Formulation of Flagellar Microorganisms Çam

,which is finally converted to the form solved for the rigid body velocities denoted as uB ,

(F · B−1 · A · M) · uB = f B − F · B−1 · b − F · B−1 · A · uS (2.40)

,where the term f B represents the resultant-net external force on the center of gravity of the microorgan-
ism,which might be induced by the electric, acoustic or magnetic field, the term F · B−1 · b represents
the hydrodynamic effect on the cell-tracked particle induced by the channel walls-confinement and lastly
the term F · B−1 · A · uS represents the self-propulsion phenomenon, i.e. the term physically incorpo-
rating the effect of the transverse beating flagellum on the translational and rotational velocities of the
entire moving cell. Note that this constitutes a system of three equations for three unknowns, which can
be solved easily. In self-propulsion phenomenon, the cells move without being exposed to any external
force. As described and formulated as Resistive Force Theory by Gray and Hancock,the propulsion of a
spermatozoon, flagellar microorganisms in general, depends on the fact that the retarding effect of all the
tangential forces acting along the body is compensated by propulsive components of forces acting normally
to the surface of the body. Therefore, self-propulsion is a force-free problem imposing f B = 0. Note also
that, the formulation can simply be extended to include more cells; in this case, the vectors uB and tB
will be modified as (3K × 1) vectors where K is the number of cells. Correspondingly, the resulting fi-
nal equation will give a linear system of 3K unknowns. Also, the matrices M and F will be modified
to include all rigid body motions of the particles and integration of the tractions over all cell surfaces.
Consequently, Impedance Formulation is able to capture the effect of the confinement,channel walls, on
the flagellar cell, such as thigmotaxis phenomenon, multiple interacting cell propulsion and any external
field can be directly inserted to the final equation,equation 2.40, into the term f B , for instance to analyze
dielectrophoretic effects on the self-propelling creatures.

2.2 Computational Aspect of the Formulation

The general form of the algorithm implemented to track the position of the particle(s)/cell(s) is presented
in Fig.2. For time integration, first order forward difference scheme (Newton explicit) is used with ∆t
representing the time increment selected for the analysis. Some comments on the presented method are
given below:
First, in the presented formulation, the matrices H00 and G00 are evaluated only once at the beginning
of the program since the microchannel mesh is not updated in time. Also, before particle tracking the matrix
G00 is inverted only once to obtain G−1
00 . In the problems of particle,cell flow within microchannels, the

discretization of the non-moving boundary (the microchannel boundary and those of the fixed boundaries
within the microchannel) is done with a large number of elements. Especially, if the particle is (or gets)
close to the microchannel walls, then the element sizes should also be decreased to avoid near-singularity
problems and increase accuracy. As a result, the stated matrices constitute to a very large portion of the
assembled coefficient matrices. With the application of presented procedure, at each time increment, the
solution of a very large linear system is avoided - instead through matrix multiplications the system is
reduced to a linear system of equations with three unknowns per each particle.
Secondly, as the particle motion is tracked at each time increment, only the matrix B is inverted. The
rest of the formulation involves only matrix multiplications. When compared with the solution of a very
large system of equations (eg. using LU decomposition or any other direct or iterative technique) this will
constitute to a less computational effort. Since the tracking involves many increments in time, a shorter
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 2: Particle Tracking Algorithm

computational time at each increment will result in a considerable amount of time savings in simulation.
A third note is on parallel programming. Matrix multiplication is not a costly operation in parallel
configurations. Shared memory (MP) parallellization can be simply employed in the presented algorithm
with almost no additional coding. Also, in the latest computer configurations, graphical processing units
(GPU) are preferred in parallellization since they can perform the matrix multiplications exceptionally fast.
Therefore the presented method can easily be implemented in a GPU processor. Considering the linear
system solvers, eg. a direct algorithm like LU decomposition or an iterative algorithm like Gauss-Seidell,
the parallel implementations are not common. This gives a very promising advantage to the presented
method.
Another advantage of the presented method is its readiness of application to other types of particle
motion. In this analysis, the particle experiences no external forces, so f B is assumed to be zero and a
solution for uB is obtained. Alternatively, for a fixed particle or a cell in the flow, the reverse could be used,
setting uB = 0 would easily compute the total drag force and torque on the particle. Also, if the particle
experiences external forces, such as forces that result from the application of electical/magnetic/acoustic
fields, then simply letting f B to include these resultant forces, the particle velocities at the given increment
can be obtained.
Boundary Element Formulation of Flagellar Microorganisms Çam

A major disadvantage of the presented method is that the flow inside the solution domain is not solved.
So, if any field variable in the flow (for example the traction on the channel walls) is required, then this
algorithm will not serve the purpose. But this can be thought as post processing: after the computation
of the particle motion and velocity components at each time increment, one can easily re-compute the
necessary field variables through boundary element equation for given locations of the particle. Simply,
we construct a grid mesh inside the domain and for each internal point, we write the boundary integral
equation one more time and compute the field variables as velocity and traction values.

3 Assessment of the Formulation

3.1 Sea-Urchin Spermatozoa Benchmark with Resistive Force Theory
Gray and Hancock in their work of The Propulsion of Sea-Urchin Spermatozoa, they derive the Resistive
Force Theory for microorganisms with single flagellum, whose tail executes a transverse beating and the
entire cell is moving with a forward propulsion velocity. They have derived the following equation, which
relates the ratio of the forward propulsive speed of the entire cell to the relative beating velocity of the
flagellum with respect to the head, as a function of geometric properties of the organism,

1 !−1
2π 2 b2 4π 2 b2 2π 2 b2 2 3a
 
Vx d 1
= · 1+ − 1+ · · log + (3.1)
Vw λ2 λ2 λ2 nλ 2λ 2

,where Vx is the mean propulsive speed of the entire microorganism, Vw is the relative flagellum beating
speed, b is the uniform amplitude, λ is the wavelength of one fully developed beating wave, a is the effective
radius of the head, which should not be confused with the exponential envelope parameter since the above
benchmark formulation is derived for microorganisms with uniform amplitude beating, n is the number
of simultaneous fully-developed beating waves on the flagellum and lastly d is the uniform radius of the
tail. In the above formulation, the relative beating speed as Vw = λf , where f is the frequency of the
beating. Gray and Hancock have taken Sea-Urchin Spermatozoa as the model flagellar microorganism
whose geometric properties as follows,

b = 4µm λ = 24µm n = 1.3 f = 35s−1 a = 0.5µm d = 0.2µm (3.2)

According to the equation 3.1, the mean propulsive speed predicted by the Resistive Force Theory is
191µm · s−1 . At this point, we have to give some remarks on the Resistive Force Theory (RFT). First of
all, the mathematical expression is not derived under the action of any external confinement even if the
observational data come from the cells close to air or glass surface. The mathematical formulation assumes
the cell swims in bulk of fluid ;therefore, it is a prediction theory for flagellar microorganisms swimming
in the bulk of fluid. In the close proximity of any confinement, such as microchannel wall, we expect the
calculated rigid body velocities to deviate from the RFT predictions. Secondly, Resistive Force Theory is
mainly constructed on the force equilibrium on the self-propelling microorganism. The theory relates the
tangential and normal forces on the body to the propulsive translational velocity of the entire cell and the
relative beating speed of the flagellum by neglecting the transverse oscillations of the cell from side
to side and any rotational velocity of the cell. Lastly, Resistive Force Theory models the flagellum
as the combination of infitesimal line segments, which turn out to be infitesimal cylinders in 3D-analysis.
Boundary Element Formulation of Flagellar Microorganisms Çam

As it will be explained in detail below, all these remarks constitute the fundamental differences in between
the Resistive Force and Boundary Element modellings of the flagellar microorganisms.

Let us return our benchmark analysis. Our very first purpose is to benchmark the sea-urchin sperma-
tozoa with Resistive Force Theory mean propulsive velocity as Vx = 191µm · s−1 . In the first case, we aim
to model the self-propulsion of the sperm cell in quiescent bulk of fluid. Impedance Formulation requires
the existence of an outer boundary, which corresponds to the microchannel in our case. To successfully
model the propulsion in bulk of fluid, we have to make sure that the dimensions of the microchannel are
sufficiently large compared to the characteristic dimension of the tracked cell. For this reason, we determine
the width and height of the microchannel as 300µm and 150µm respectively. Since we are trying to model
the cell in bulk of fluid, we initially locate the cell at the centerline of the microchannel; therefore, the cell
does not swim in close proximity to the channel walls, which eliminates the usage of extremely fine mesh
on the channel walls. We use 0.5µm uniform mesh on the channel walls and on the surface of the sperm
cell, we use 0.05µm uniform mesh, which is one order finer compared to the meshes on the channel wall.
The prominent reason to use remarkably finer mesh on the sperm cell can be attributed to the fact that:
the sperm cell has a very long flagellum, 31.2µm, compared to the radius of its head as 0.5µm and the
flagellum has only 0.2µm width. To resolve flow field induced by the beating flagellum to the surrounding
fluid successfully, we should utilize meshes on the flagellum surface, which are at least one fourth of the
width of the flagellum. That’s why, the great portion of the meshes on the sperm boundary come from the
flagellum. As for the time step, since the beating frequency of the sperm cell is 35Hz, the period for one
1
fully-developed beating wave to travel along the flagellum is 35
s and we solve 20 quasi steady state cases
1
for each period and determine the time step as 35∗20
= 0.0014s. Lastly, as for boundary conditions, for
top and bottom walls of the microchannel, we have no-slip boundary condition as ux = 0 and uy = 0. For
the left,inlet wall of the microchannel, we have no-slip boundary condition as ux = Uin and uy = 0, where
for quiescent fluid Uin is set to zero. For the right,outlet wall of the microchannel, we have zero traction
boundary condition on longitudinal direction as tx = 0 and no-slip boundary condition in the transverse
direction as uy = 0. On the sperm boundary, we have prescribed beating velocities as ux = −sin(θ) · uS
and uy = cos(θ) · uS . For non-beating parts of the sperm cell as head and the midpiece, the beating
velocities are always set to zero. The meshing schematics of the benchmark problem are given as follow,
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 3: Meshing Schematic of the Sperm Cell

Figure 4: Meshing Schematic of the Benchmark Problem

Boundary Element Formulation of Flagellar Microorganisms Çam

Rigid body velocities of the tracked sea-urchin spermatozoa for the total amount of time that 20
fully-developed beating waves have passed over the flagellum are given as follows,

Figure 5: Rigid Body Velocities of the Sea-Urchin Spermatozoa Released from Centerline

For each time instant, our mathematical model computes the rigid-body parameters as x- and y-
translational velocities and rotational velocity. As we observe from the above graph, the cell released
from the centerline executes rather small-valued pure periodic angular velocity values, whose mean value
is −0.00561rad · s−1 , which can be attributed to the numerical error of our model. Since we do not release
the cell in the close proximity to any confinement, the flow field induced by the microorganism is symmetric
and there is no close boundary that distorts this symmetry and executes an attractive or repulsive effect on
the organism. The interesting outcome is encountered in y-translational velocity values. Even if the overall
mean of the y-translational velocities is −0.3967µm · s−1 , which is again sufficiently small to be attributed
to the numerical error of our model, instantenous y-translational velocities periodically oscillate within
±344µm · s−1 . In experimental sperm observations, it is recorded that when sperms propel themselves,
their head oscillate very rapidly from side to side; however, the cells do not translate in that direction. This
observation is well predicted by our model as well, which was not taken into account by Gray and Hancock
in the derivation of Resistive Force Theory. In the analytical derivation of the theory, they assume that
the beating of the flagellum will purely compensate the propulsive components of the forces on the cell;
therefore, the cell is assumed to translate smoothly without any transverse oscillation. Most importantly,
as for x-translational velocities, that is the propulsive velocities of interest, the Resistive Force Theory’s
prediction was Vx = 191µm · s−1 , for which our model yields a mean propulsive speed of 255µm · s−1 .
Boundary Element Formulation of Flagellar Microorganisms Çam

The major reason behind the deviation is the fact that Resistive Force Theory models the flagellum as the
combination of infitesimal cylinders; however, our two dimensional analysis regards that the sperm cell has
an infinite width in the direction perpendicular to page, which naturally introduces a positive shift on the
Resistive Force Theory’s prediction. Additionally, RFT provides a mean velocity and does not consider
sharp oscillations of head in the transverse direction.
As it is mentioned before, in the quiescent bulk of fluid, the flagellar microorganisms propel themselves
by giving beating disturbance to the surrounding fluid, which is observed by the following velocity post-
processing of our mathematical model,

Figure 6: Quiver Plot of the Velocity Post-Processing of Sea-Urchin Spermatozoa in Quiescent

Fluid
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 7: ContourField Plot of the Velocity Post-Processing of Sea-Urchin Spermatozoa in Quies-

cent Fluid

As you observe from the above contour-field and quiver post-processing plots of the velocity field in the
close proximity of the sperm cell, the greatest disturbance is given to the surrounding fluid by the flagellar
cell in the portions of the flagellum, which attain the highest values of transverse beating velocities at
that particular instant. As we move away from the flagellar cell, the density of the disturbance fades away
and vanishes towards the quiescent bulk of fluid. Due to the fact that the beating waves travel along the
flagellum to a particular direction, the flagellum continuously disturbs the flow to that particular direction
accordingly, which induces the backward or forward proupulsion of the entire cell.

3.2 Near-Wall Swimming Characteristics of Sea-Urchin Spermatozoa

The close proximity of a wall or a solid boundary distorts the flow field induced by the sperm cell, which
might yield a net attractive or repulsive force on the microorganism. The approach of the sperm cells
to the solid surfaces and their subsequent accumulation have always been a long-standing problem in
flagellar hydrodynamics. Boundary Element Method is able to capture the reciprocal interaction within
the channel walls and the flagellar microorganism; therefore, we expect to observe that our mathematical
model is able to capture the approach of sperm cells towards the solid boundaries, which can be regarded
as a thigmotaxis phenomenon. In this assessment, we still consider the sea-urchin spermatozoa with the
identical beating patterns and geometric parameters. Boundary conditions are also identical and the sperm
cell swims in the quiescent bulk of fluid. The major difference is that in this simulation, we do not release
Boundary Element Formulation of Flagellar Microorganisms Çam

the sperm cell from the centerline of the micro-channel; instead, we release the sperm cell just 20µm away
from the top side of the microchannel. In the previous simulation, we have used 0.5µm uniform mesh on
the channel walls; however, in this case, we expect the sperm cell to be attracted by the microchannel
walls, which might introduce near-singularity issues as the distance between the cell and the wall decreases.
For this reason, now we utilize 0.2µm uniform mesh on the channel walls. The trajectory of the sperm
cell, within the period of time for 20 fully-developed beating waves passing over the flagellum, is given in
the next page,
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 8: Near-wall Swimming Trajectory of a Sea-Urchin Spematozoa

Boundary Element Formulation of Flagellar Microorganisms Çam

For the above configuration of near-wall sea-urchin spermatozoa swimming, the mean x-translational
velocity turns out to be 247µm · s−1 , which is slightly lower than the mean propulsion speed of the sperm
cell released along the centerline as 255µm · s−1 . The decrease in the mean propulsion speed is expected
since as the sperm swims in the close proximity of a wall, the wall attracts the sperm cell, which introduces
a net y-direction translational velocity towards the wall and also the wall causes a net rotation of the
sperm cell in the counterclockwise direction due to the fact that the boundary is on the upper side of the
microorganism. When we release the sperm cell on the lower-half side of the microchannel, the sperm cell
approaches towards the wall with same magnitude of mean y-direction translational velocity and the wall
in that configuration rotates the sperm cell in clockwise direction. When we release the sperm cell along the
centerline of the microchannel, the net y-direction translational velocity turns out to be −0.3967µm · s−1
despite the large oscillations in transverse direction and we have attributed the net y-direction velocity
to the numerical error of our mathematical modelling. However, in near-wall swimming, still we observe
the sharp oscillations within the transverse direction and we end up with a net y-direction translational
velocity as 12.4µm · s−1 , which causes the resultant deviation from the initial position by 7.1µm towards
the wall. As the sperm cell swims towards the wall, it approaches with higher y-direction translational
velocities. As the sperm cell approaches towards the solid boundary, in order to prevent near-singularity
issues, we have to use very fine mesh, even on the order of the meshes we use on the sperm boundary, for
the microchannel walls. Otherwise, numerical scheme will not be able to resolve the flow field concentrated
within the sperm cell and the microchannel wall and will start to repel the sperm cell away from the wall
instead of modelling the expected accumulation of microorganisms on the channel walls in spite of the
continuation of flagellar beating. Lastly, let us consider the contour field plot of the velocity field induced
by the sperm cell in the close proximity of the wall, as 12µm away from the microchannel wall.
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 9: ContourField Plot of the Velocity Post-Processing of Sea-Urchin Spermatozoa in the

Close Proximity of the Microchannel Wall

As we observe from the previous post-processing of the velocity field, the highest velocity values are
concentrated on the parts of the flagellum executing the highest beating velocities and disturbing the
surrounding fluid at most. However, in this case, due to the close proximity of the microchannel wall to
the sperm cell, the velocity contours are densely concentrated on the upper side of the flagellum and on
the lower side, we observe a less dense velocity disturbance contours fading away more smoothly to the
quiescent fluid. As expected, the existence of the wall disturbs the symmetry of the velocity fields and
causing a net propulsion towards the microchannel wall. Actually, asymmetry induced by the microchannel
walls introduces velocity gradient and which introduces pressure gradient. At this point of our research,
we are also trying to embedd the pressure field post-processing into our mathematical model and observe
the pressure field in the close proximity of the microchannel wall. For this, we are writing a program that
calculates the boundary integrals belonging to the fundamental traction and fundamental pressure values.
Even from the velocity contour field plot, we can make an inference that a low pressure field emerges on
the top side of the sperm cell and respectively, a high pressure field emerges on the bottom side, which
causes a net traction accumulation on the entire body of the cell in the positive y-direction and make the
cell approach towards the channel boundary.
Boundary Element Formulation of Flagellar Microorganisms Çam

4 Current Research Problems

Currently, we are working on two major research problems as the modelling of multiple spermatozoa in a
microchannel and the modelling of the single spermatozoon along a corner structure under the influence
of a poiseuille flow. In multiple sperm cell modeling, our major motivation is to model the asymmetric
thigmotaxis phenomenon simultaneously; that is, we expect to observe that the sperm released from
the upper half of the microchannel will approach towards the top side of the microchannel and the one
released from the lower half will approach to the bottom side. In the meantime, we do not expect the sperm
released along the centerline undergo a huge transverse deviation from the initial y-position. Additionally,
we expect the sperm cell released along the centerline to trace greater horizontal distance because of its less
vulnerability to the effects of microchannel walls compared to sperm cells in the close proximity of walls.
The mesh schematic of the problem is given as follows for which all the sperms are identical sea-urchin
spermatozoon,

Figure 10: Mesh Schematic of the Multiple Sperm Cells

In our initial analyses, we have observed a very similar thigmotaxis phenomenon in near-wall swimming
of amphitrichous bacteria as follows,
Boundary Element Formulation of Flagellar Microorganisms Çam

Figure 11: Near Wall Swimming of Amphitrichous Bacteria

We are also applying the simulatenous modeling of multiple flagellar microorganism problem to am-
phitrichous bacteria as follows,

Figure 12: Mesh Schematic of the Multiple Amphitrichous Bacteria

Lastly, we are working on the near corner swimming characteristics of sperm cells and amphitrichous
bacteria under the influence of a poiseuille flow, which is induced by an inlet velocity boundary condition.
The mesh schematic and the velocity-field post processing of the problem are given below. At this point,
Boundary Element Formulation of Flagellar Microorganisms Çam

we encounter a physically expected velocity contour field for this problem; therefore, the post-processing
plot is really helpful to understand the physics of the problem.

Figure 13: Mesh Schematic of the Near Corner Swimming Characteristics of Spermatozoon Cell

Figure 14: Velocity Post Processing of Corner Turning Spermatozoon Cell

Boundary Element Formulation of Flagellar Microorganisms Çam

5 Conclusions
So far, in my undergraduate research, I have successfully applied Impedance Formulation to multi-particulate
flows and modified the Impedance Formulation for flagellar hydrodynamics. We had been working on three
candidate modifications; however, the modification presented in this paper turned out to be the most
promising one in terms of benchmark results with Resistive Force Theory and the physics of the flagellar
propulsion. At this point of our research, we successfully model the self propulsion of spermatozoa and
amphitrichous bacteria with distinct geometries and beating patters and the near-wall swimming charac-
teristics of both types of flagellar microorganisms. We have been working on multi-flagellar microorganism
problems and near corner flagellar hydrodynamics, which provide promising results. Our modified version
of Impedance Formulation does not require any comprehensive adjustment to model any microchannel ge-
ometry, multiple microorganisms simultaneously and external field (e.g., dielectrophoretic and magnetic)
swimming characteristics. Our ultimate purpose is to finalize a mathematical modelling that simulates
the swimming characteristics of multiple spermatozoa and amphitrichous bacteria under dielectrophoretic
effects in novel microchannel geometries. We want to finalize the program until April 2018, since it is the
deadline of Scientific and Technological Research Council of Turkey’s 2209-A, Supporting Program for the
Research Projects of Undergraduate Students and on June 10-13, we are going to present the outcomes
of our research in The ASME 2018 16th International Conference on Nanochannels, Microchannels and
Minichannels (ICNMM2018) in Dubrovnik, Croatia.
Boundary Element Formulation of Flagellar Microorganisms Çam

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