How the Venus flytrap snaps: a poroelastic buckling

Y. Forterre
IUSTI CNRS UMR 6595, Universit de Provence, 5 rue Enrico Fermi, 13453 Marseille Cedex 13, France

J. Skotheim & L. Mahadevan

DEAS, Harvard University, Pierce Hall, 29, Oxford Street, Cambridge, MA 02138, USA

J. Dumais
DOEB, Harvard University Biological Laboratories, 16 Divinity Avenue, Cambridge MA 02138, USA

ABSTRACT: We present a mechanical study of the snapping closure of the carnivorous plant Venus flytrap
(Dionaea muscipula), which exhibits one of the fastest motion in the vegetable kingdom (typically 100 ms). Using
high-speed video measurements and non-invasive microscopy techniques, we propose that the fast closure of the
Venus flytrap results from a snap-buckling instability, which is damped by the flow of water through the tissues.
A simple model for the snapping of a poroelastic shell and experiments on the mechanical properties of the leaf
tissue are completely consistent with this picture.

1 INTRODUCTION

Plants, unlike animals, are not known to move quickly.

Yet rapid movements in plants are essential for func-
tions such as seed/sporangium dispersal (exploding
fruits in Impatiens and Squirting cucumber), pollen
emplacement (Catasetum orchids, Stylidiumtrigger-
plants), defense (Mimosa pudica) and nutrition (Venus
flytrap, Aldrovanda vesiculosa, bladderwort). Of these
spectacular examples that have long since Darwin
fascinated scientists (Darwin 1875), the Venus fly-
trap (Fig. 1), whose leaves snap together in a frac-
tion of second to capture insects, has long been
a paradigm for study. The closure is initiated by
the mechanical stimulation of trigger hairs acting
as mechano-transducers. Previous studies (Burdon-
Sanderson 1882, Stuhlman & Darder 1950, Hodieck &
Sievers 1989, Juniper et al. 1989) have focused on the
biochemical response of the trigger hairs to stimuli
and quantified the propagation of an action poten-
tial in the leaves. Yet the mechanism by which this
non-muscular engine works remains poorly under-
stood. The most frequently proposed explanations for
the movement are a rapid loss of turgor pressure
in motor cells (Hill & Findlay 1981) or an irre-
versible loosening of the cell wall (Williams & Bennet
1982). However, the validity of both mechanisms has
recently been questioned (Hodick & Sievers 1989,
Morillon et al. 2001) on the grounds that these cel-
lular mechanisms alone cannot explain the rapidity
of closure of the entire leaf on a macroscopic scale
Figure 1. Pictures showing the carnivorous plant Venus
flytrap in the open (a) and closed (b) states.
leading to the suggestion (Hodick & Sievers 1989,
Vincent 2001) that elastic deformations could be
important.
In this paper, we focus on the mechanical aspect
of Venus flytrap closure and try to elucidate the
mechanisms responsible for the macroscopic motion
observed.
2 EXPERIMENT
2.1 Dynamics of closure
We have first studied the dynamics of the trap by
painting sub-millimetric UV-fluorescent dots on the
external face of the leaves and filming flytraps snap-
ping at 400 frames/s under a UV light. A stereoscopic
set-up allows to reconstruct the leaf geometry and the
change therein using triangulation. The first obser-
vation is that the leaf is curved outward (convex) in

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Copyright 2005 Taylor & Francis Group plc, London, UK

Figure 2. a) Spatially averaged mean curvature m as a func-
tion of time. Inset: 3D stereoscopic reconstruction of the leaf
in the open and closed states. b) Spatially averaged gaussian
curvature g as a function of time. The plant is triggered at
t = 0. The closure dynamics is characterized by three phases
(IIII) (see text). The solid line corresponds to the poroelastic
model (see 5.3).
the open state and curved inward (concave) in the
closed state (Fig. 2a). The leaf shape can be naturally
characterized in terms of its spatially averaged mean
curvature, m , and its spatially averaged gaussian cur-
vature, g . The snapping motion itself is characterized
by three phases (Fig. 2a): a slow initial phase (20% of
total displacement in 1/3 s); a rapid intermediate phase
(60% of total displacement in 1/10 s); and finally a sec-
ond slow phase (20% of total displacement in 1/3 s).
Most of the leaf displacement occurs in the interme-
diate phase, during which the leaf geometry changes
from convex to concave (Fig. 2b) shows g as a func-
tion of time. We see that g is not constant and also that
g changes slowly and then rapidly as it passes through
a minimum. As changes in g correspond to stretch-
ing the mid-plane of the leaf (Love 1944), the first
observation implies that closure involves the storage
and release of elastic energy; while the second obser-
vation implies that closure is characterized by a slow
storage of elastic energy followed by a rapid release.
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Copyright 2005 Taylor & Francis Group plc, London, UK
Figure 3. a) Measured strain field of the outer surface due
to closure (averaged over 6 different leaves), where pos-
itive strains correspond to extension and negative strains
correspond to contraction of the surface in the principal
directions as shown. b) Typical local strain measured on the
outer surface of the leaf inside the dashed region, super-
posed on a micrograph of the leaf surface. The polar plot
shows the local strain in the direction , (l/l)(), defined
by (l/l)() = 1 cos( 0 ) + 2 sin( 0 ) where 1 and
2 are the principal values of the strain tensor and 0 is the
angle of the principal axes with respect to the reference frame
of coordinates. Scale bar: 0.1 mm.
2.2 Strain measurements
To understand the origin of these curvature changes,
we measure the local strains by recording the position
of fiducial markers on the entire outer surface of the
leaf before and after closure (Green et al. 1991). Our
measurements of the strain (Fig. 3) are consistent with
earlier point-wise measurements (Hodick & Sievers
1989) but go beyond these by characterizing the spatial
structure of the strain field over the entire leaf. Figure
3a shows that the maximum strain perpendicular to the
midrib (x-direction) is six times the maximum strain
parallel to the midrib (y-direction). Furthermore, we
find that the strains on the inner surface of the leaf are
1%, implying that closure is triggered primarily by
differential strains in the x-direction.
Figure 4. Cutting the closed leaf along the dotted lines
shows the natural curvatures in the x-direction (right) and
the y-direction (left). Scale bar: 1 cm.

2.3 Natural curvature changes

To corroborate this picture we cut recently closed
leaves to determine the residual strains in it. Cutting
the leaf in the x-direction eliminates the constrain-
ing effect of curvature in the y-direction and allows
it to recover its natural curvature in the x-direction,
xn , as seen in (Fig. 4). Similarly, cutting the leaf in
the y-direction allows us to observe the natural cur-
vature in the y-direction, yn . We see that xn reverses
sign during closure, while yn does not. This is con-
sistent with previous observations (Hodick & Sievers
1989) and provides quantitative evidence that a change
in xn drives leaf closure. Support for a mechanistic
basis for this anisotropic deformation comes from a
microscopic examination of the leaf surface (Fig. 3b)
where we see that the cells on the outer surface are
highly elongated in shape, with their long axis oriented
along the x-axis. Since the cylindrical cell wall is rein-
forced azimuthally by microfibrils (Hodick & Sievers
1989), it follows that any changes in turgor would lead
to deformations that are primarily in the x-direction,
consistent with our macroscopic observations that xn
changes much more than yn .
3 MECHANISM OF CLOSURE
Although the anisotropic curvature changes occurs via
physiological processes on the cellular level which
still remain poorly understood, we now argue that
the macroscopic mechanism of closure is determined
solely by leaf geometry. For a doubly-curved leaf, i.e.
one that is curved in two orthogonal directions, bend-
ing and stretching modes of deformations are coupled
(Love 1944), i.e. bending the leaf causes its mid-
plane to be stretched. If the coupling is weak, the leaf
can change its shape from open to closed by vary-
ing its gaussian curvature and stretch without a large
Figure 5. Smooth-snapping transition in leaf closure. We
plot the dimensionless mean curvature Km = (Kx + Ky )/2 as
a function of the control parameter Kxn . The different stages
in the schematics correspond to Kxn values of 0.95, 1.05,
1.15 and 1.25.
energetic cost. In such a situation the leaf deforms
smoothly to accommodate the change in xn . If the cou-
pling is strong, the leaf will not deform much owing to
large energetic cost of stretching its mid-plane, until
eventually the change in xn becomes so large that the
leaf snaps shut rapidly (see Fig. 5).
4 ELASTIC MODEL
To quantify the smooth/snapping transition, we model
the leaf as a thin weakly-curved elastic shell (thick-
ness h, size L, Young modulus E) of paraboloid shape
given by f = (x x2 /2) + (y y2 /2), where x and y are
the spatially homogeneous principal curvatures. Con-
sistent with our experimental observations, we take the
natural curvature in the y-direction to be a constant
(equal to that in the x-direction before snapping). The
elastic energy u of the shell is then written as the sum
of a bending term (Mansfield 1989) and a stretching
term:
where U = u/CL2 h3 E (C is a constant), Kx = x /,
Ky = y / and Kxn = xn / are dimensionless. The
geometrical dimensionless parameter L4 2 /h2

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Figure 6. Speed of closure and delay between triggering and
snapping. a) Maximum angular velocity plotted against .
b) The time between triggering the leaf and snapping, rapid
closure plotted against (note the semi-logarithmic scale).
Similar symbols correspond to different leaves of the same
plant.
quantifies the coupling between bending and stretch-
ing deformations. Note that we use a simplified
expression for the stretching elastic energy of the
shell that neglects the role of Poisson contraction and
extension (Mansfield 1989). The shape of the leaf
is obtained by minimization of U with respect to
Kxn , which is the control parameter that is actively
changed by the plant during closure. In Figure 5 we
see that U (Kxn ) has a single minimum when < c
(weak bending-stretching coupling), but has two min-
ima when > c (strong bending-stretching coupling)
for some values of Kxn .
Since the amount of mid-plane stretching required
for the leaf to close increases with , the mechanical
barrier to snapping is determined by this geometrical
parameter. Thus we expect that large highly curved
leaves will release more energy and snap more rapidly
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Copyright 2005 Taylor & Francis Group plc, London, UK
than small weakly curved leaves. In order to test this,
we measured the speed of the closure as a function of
the geometrical parameter for many different leaves
and plants. (Fig. 6a) shows a clear positive correla-
tion between the maximum speed of the snap and .
Interestingly, the time delay between the beginning of
the motion and the snap increases with the parameter
as shown in (Fig. 6b), just as the maximum speed
of snapping does. This is probably because the delay
reflects the time required to cross the stretching barrier,
which increased with . For a typical leaf L 1 cm,
0.1 cm1 , h 0.1 cm so 1 c , i.e. the leaves
are poised at the transition between smooth closing and
snapping. Since the plant is clearly best served by (i)
minimizing the delay between triggering and closure,
(ii) snapping rapidly rather than closing smoothly, this
choice of may not be a coincidence.
5 TIME SCALES AND POROELASTICITY
5.1 Poroelastic time
The actual speed of snapping, or equivalently the leaf
closure time is a critical parameter for trap function,
and we now turn to the mechanism that determines
it. The store elastic energy must be rapidly dissipated
once the trap is closed to prevent any inertial ringing
that would allow the prey to escape. Since the time
scale of the fundamental bending mode of the leaf
b (L2 h1 )(/E)1/2 0.0010.01 s is much less than
the observed time scale of the motion 0.11 s, and
external dissipation due to motion through air is neg-
ligible, the damping must occur internally. Since the
leaf is highly hydrated, a natural candidate for damp-
ing is provided by the flow of water, an interstitial
fluid, through the surrounding elastic tissue. The cur-
vature change during closure induces a transient flow
perpendicular to the leaf surface. At the continuum
level this water diffusion is described by poroelastic-
ity and the typical time scale of diffusion across the
leaf is given by the poroelastic time scale P h2 /kE
(Biot 1944, Skotheim & Mahadevan 2003), where k is
the hydraulic permeability of the leaf tissue, is the
interstitial fluid viscosity, and E is the drained bulk
modulus of the tissue. Measurements of the Youngs
modulus give E 10 MPa. It is much more difficult
to evaluate the hydraulic permeability of the leaf tis-
sue, which is poorly documented (Steudle 1989). We
simply note that in order to find a poroelastic time
consistent with the snapping time, i.e. P 0.1 s, we
need to take k/ 1012 m2 Pa1 s1 . This is equiva-
lent to a pore size k 1/2 30 nm, which is a realistic
value considering the leaf anatomy.
5.2 Mechanical response of the leaf tissue
In order to test the previous order of magnitudes for the
inertial time scale and the poroelastic time scale, we

2 h2 /2 kE is the poroelastic time. This
Figure 7. Time response of a strip of the leaf to impulsive
(a) and step (b) loads.
directly measured the response time of the leaf tissue
to a step load (Fig. 7). A thin strip of a closed leaf is
clamped at one end and free at the other. In the case
of an impulsive load applied at the free end, we see
a short ringing transient of period 10 ms (Fig. 7a),
consistent with our estimate for the inertial (bending)
mode and much faster than the time of closure. On
the other hand if the strip is released suddenly after
being statically deflected at the other end for a while,
we get a very different response. In Figure 7b, we see
that after a short inertial transient the unloading is best
described by a single exponential with a time constant
p 0.10.4 s, which is of the same order of magnitude
than the snapping time.
This mechanical response of the leaf tissue is
consistent with the behavior of a poroelastic solid
(Ced erbaum et al, 2000) and supports our simple
poroelastic picture, which is likely to be the dom-
inant mechanism operating during the dynamics of
snapping.
5.3 Poroelastic dynamics model
Following these results, we model the dynamics of
snapping by treating the leaf tissue as a poroelastic
material. When the leaf snaps shut, the stored elastic
energy given by Equation 1 is dissipated via the vis-
cous flow within the leaf tissue. The mid-plane mean
curvature of an impermeable poroelastic plate with
curvatures x (t) and y (t), Youngs modulus E, Pois-
sons ratio = 0 for the elastic skeleton, and fluid vol-
ume fraction
, generates a pressure in the interstitial stood. However, once this change occurs, the geometry
fluid given by (Skotheim & Mahadevan 2003):
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Copyright 2005 Taylor & Francis Group plc, London, UK
where P
expression arises from the solution of a Darcy-type
diffusion equation for the fluid pressure, which in turn
gives rise to a moment resisting the bending:
where z is the coordinate perpendicular to the leaf
surface. Fluid motion through the tissue leads to the
dissipation rate:
Balancing the elastic power with the viscous dissipa-
tion rate yields:
where A = 196/4 . Here we scale time T = t/p and
scale the curvatures and elastic energy U as in the
previous section. We assume that Kx and Ky follow
the path of steepest descent in the energy potential.
In the absence of microscopic physiological informa-
tion for the change in dimensionless natural curva-
ture upon x-direction changes, we choose the form
Kxn = 1 (1ebT ) (we check that other functional
forms do not change the qualitative dynamics of snap-
ping). Figure 2 shows the prediction of the above
poroelastic model using a = 3, b = 0.05, P = 1/94 s
and = 1. We see that the model qualitatively captures
the three phases of snapping.
6 CONCLUSION
In this article, we have shown that the fast closure of the
Venus flytrap is composed of two component: an active
biochemical component and a passive elastic compo-
nent. Upon stimulation, the plant actively changes
one of its principal natural curvatures, xn , the micro-
scopic mechanism for which remains poorly under-
of the doubly-curved leaf provides the mechanism by
which elastic energy is both stored and released, while
the hydrated nature of the leaf induces the rapid damp-
ing that is equally crucial to efficient prey capture. A
single geometrical parameter determines the nature
of closure: if c 1 the leaf closes smoothly, while
if > c the leaf snaps rapidly. This ingenious solu-
tion to the problem of scaling up movements and
speed from the cellular to the organ level by natures
consummate hydraulic engineers, plants, shows how
controlling elastic instabilities in geometrically slen-
der objects provides an alternative to the more common
muscle-powered movements in animals.
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