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Directed Motility of Hygroresponsive Biomimetic Actuators

Lidong Zhang, Stanislav Chizhik, Yunze Wen, and Panče Naumov*

The capability of cellulose microfibrils to elicit directionality by anisotropically typical shapes of plant seed pods shown in
Figure 1a–d, occurs by anisotropic defor-
restricting the deformation of amorphous biogenic matrices is central to the
mation (bending, twisting, or uncoiling) of
motility of many plants as motoric and shape-restoring elements. Herein, an their parts upon drying. The mechanical
approach is described to control directionality of artificial composite actuators reconfiguration of these seemingly com-
that mimic the hygroinduced motion of composite plant tissues such as the plex structures can be in principle reduced
opening of seed pods, winding of plant tendrils, and burial of seed awns. The to deformation of a combination of simple
bilayer architectures. In an attempt to
actuators are designed as bilayer structures where single or double networks
mimic these natural systems, artificial
of buried parallel glass fibers reinforce the composite. By anisotropically mechanically active materials have been
restricting the expansion along certain directions they also effectively direct developed that are capable of twisting,
the mechanical reconfiguration, thereby determining the mechanical effect. bending, curling, or rotation in response
A mathematical model is developed to quantify the kinematic response of to light, heat, spatial, and temporal gra-
fiber-reinforced actuators. Within a broader context, the results of this study dients in humidity, chemical potential, or
electric and/or magnetic fields.[6–18] These
provide means for control over mechanical deformation of artificial dynamic
materials are normally based on photo-
elements that mimic the oriented fibrous architectures in biogenic motoric responsive, thermoresponsive, chemore-
elements. sponsive, electroactive, or hygrosensitive
smart polymers.[19–31]
However, precise external spatiotem-
poral control over the dynamics and kinematics of such bio-
1. Introduction
mimetic materials continues to posit a considerable challenge.
The kinematic principles of motile hierarchical architectures With photomechanical actuators that are capable of externally
that have evolved through the process of natural evolution controllable mechanical motion in response to light, gener-
resemble some man-made devices.[1] The analogy between ally one of two approaches to external control of motility is
these biogenic structures and the mechanical devices used in adopted.[8,32] In the molecular approach, prolate-shaped photo-
contemporary engineering extends beyond the mere metaphor, receptor molecules are linked to or embedded into a flexible
as the biological systems have inspired the design of energy- polymer or liquid-crystalline matrix as motion directors.[8] In
effective biomimetic dynamic elements, for instance, within the alternative, macroscopic approach, control over the defor-
the realm of the emerging field of engineered soft robotics. mation is exerted by introducing photoresponsive structural
The underlying biophysical mechanism of motility in climbing elements, for instance, macro/nanosized particles or rods with
plants such as coiling and overwinding of plant tendrils, cir- controllable distribution and/or relative orientation.[3] However,
cumnutation (daily sweeping of young shoots), and thigmotro- these strategies cannot directly be translated to hygroresponsive
pism (slow motion during growth where a plant moves toward actuators due to the fundamentally different interaction of the
a support in response to touch) is an anisotropic expansion/con- matter with light on one hand, which depends on the optical
traction of biogenic bilayer structures in response to changes in and electronic properties of the materials, and humidity on the
either the turgor pressure or the environmental humidity.[2–5] other, which is controlled by diffusion.
Opening of ripe seed pods to release seedlings, such as the four Here we report a simple, yet universal approach to prepare
composite hygroresponsive actuating elements with high direc-
tionality. To mimic various tropisms of plant tissues, such as
Dr. L. Zhang, Y. Wen, Prof. P. Naumov the directional motion of plant tendrils and seed awns, where
New York University Abu Dhabi the directionality is accomplished by the action of cellulose
PO Box 129188, Abu Dhabi, United Arab Emirates microfibrils, glass fibers (GFs) were incorporated as directing
E-mail: pance.naumov@nyu.edu
and reinforcing elements into agarose (AG) as a natural
Dr. S. Chizhik
Institute of Solid State Chemistry hygroresponsive matrix. It is demonstrated that the motility of
and Mechanochemistry the composite actuators can be preprogrammed and fine-tuned
Siberian Branch of Russian Academy of Sciences by the alignment of the GFs. A general mathematical model
ul. Kutateladze 18, Novosibirsk 630128, Russia applicable to linearly reinforced actuators that predict the type
Dr. S. Chizhik of motion depending on the orientation of the directing fibrils
Novosibirsk State University
ul. Pirogova 2, Novosibirsk 630090, Russia
is developed and is used to explain the kinematics of these
actuators. A small-scale application of the actuators is also
DOI: 10.1002/adfm.201503922 demonstrated with a device that is capable of harnessing the

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Figure 1. Natural and artificial hygroresponsive architectures. a) Elongated and curled seed pods from four tree/plant species in their closed (wet)
state. b) Sketch of the seed pods shown in panel (a) with arrows indicating the deformation that occurs upon drying. c) Dried and opened seed pods
from the same tree/plant species as shown in panel (a). d) Sketch showing the structures of the opened seed pods. Note that while the first pod (from
left) has opened by twisting of the two halves with identical handedness, the second pod has opened by uncoiling which has brought to misfit strain
between the two halves. The third and the fourth pod have opened by bending of the two or the three parts, respectively. All four structures can be
approximated by simple bilayer structures. e) GFs with diameter 5–10 µm prealigned onto a microscopic glass slide. f) Preparation of a biomimetic
fiber-reinforced bilayer structures that mimic biogenic-reinforced bilayers (AG/TGF@AG is shown as example). GFs were aligned and coated with AG.
After drying, a second layer of AG was cast on the composite to create a bilayer-like structure. g) Orientation of the GFs in the reinforced layer of the
actuators: single nets of longitudinal (LGF@AG), transverse (TGF@AG) and oblique (OGF@AG) GFs, and double nets of skewed (SGF@AG) and
perpendicular (PGF@AG) fibers.

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chemical potential of a humidity gradient as elastic energy to
generate electricity.
2. Results and Dicussion
2.1. Preparation of the Actuators
Nets of parallel GFs were embedded into AG by layering a
solution of AG over fibers that were prealigned on a micro-
scope glass (Figure 1e,f; Rhodamine B was added to the solu-
tion to facilitate visualization of the otherwise colorless films).
The GFs (Figure 1e) were selected as flexible reinforcing ele-
ments to build a network with remarkably high tensile strength
and excellent handling and knotting characteristics.[33–35] AG
was used as a soft hydrogel matrix that is capable of rapidly
exchanging water with the surroundings to induce deforma-
tion by anisotropic swelling.[36–41] The GFs were oriented as
single nets of longitudinal (LGF@AG), transverse (TGF@AG),
and oblique (OGF@AG) fibers, or as double nets of skewed
(SGF@AG) and perpendicular (PGF@AG) fibers (the orienta-
tion is given relative to the long axis of the film, L; Figure 1g).
To prepare the bilayer structures, after the composite layer
(GF@AG) had dried, a second layer of pure AG was cast on top
of the first layer. After the bilayer films dried off, rectangular,
60 µm-thick stripes were cut out. The films were flexible and
free-standing (Figure 1f and Figures S1–S3 in the Supporting
Information show optical and scanning electron microscopy
images of the films and the fibers).
2.2. Kinematic Analysis
When exposed to humidity by approaching to a water droplet,
the strips having a single net of GFs aligned ||L (AG/LGF@AG)
bent due to swelling by adsorption of water vapor (Figure 2a).
The side exposed to humidity determined the deforma-
tion. Unlike films of pure AG, which always bent away
from the droplet regardless of which side of the film was
exposed (Figure 2b), the AG/LGF@AG film bent only when
it was exposed to humidity from the AG face, whereupon it
deflected off the source of humidity and toward the LGF@AG
side (Movie S1, Supporting Information). The deformation
was unidirectional as exposure of the LGF@AG layer of the
film to humidity did not cause bending. When the film was
retracted from the water droplet, it was partially dehydrated,
whereby it recovered its original shape. This process is
reversible and resembles the change in shape of pinecone
scales that bend to peduncle upon hydration and then recover
their original shape upon dehydration.[3–5] In the pinecone
scales, the cellulose microfibrils that form a bilayer reorient
during water adsorption and desorption to drive asymmetric
and reversible expansion and contraction of the scales. In the
AG/LGF@AG bilayer, the GFs that run ||L restrict the expan-
sion of the GF@AG layer when it is hydrated. Thus, only the
layer of pure AG is unrestrained to swell. This anisotropy
directs the bending exclusively toward the LGF@AG side,
since the bending toward the AG side is arrested by the rigid
LGF@AG layer. This result implies that the differences in
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stiffness counterbalance the elastic forces of swelling on the
AG and LGF@AG faces of the actuator to cause anisotropic
bending.
Assuming that the resistance to external pressure could be
taken as a measure of the stiffness of the AG/LGF@AG film
in response to swelling by hydration, its mechanical properties
were tested in a three-point bending geometry (Figure 2d). As
shown in Figure 2e,f, the bending forces on both sides of strips
of pure AG are identical, whereas stronger force is required to
stretch a film of AG/LGF@AG on the LGF@AG face (bending
toward the AG face) relative to the AG face (bending toward
the LGF/AG face). This result confirms that, indeed, the GFs
restrict and direct the bending of the LGF@AG layer. There-
fore, the directionality of bending of the AG/LGF@AG com-
posite is due to the embedded GFs that cause anisotropic
mechanical response to swelling. In accord with this result, at
a fixed size of the AG/LGF@AG film and with identical rela-
tive humidity of the surroundings, the bending degree depends
on the density of GFs, the number of parallel GFs per dis-
tance normal to their direction (Figure 2c and Movie S1, Sup-
porting Information). Increased density of GFs corresponds
to stronger reinforcement and smaller angle of bending. This
result parallels the stiffness of the film in the mechanical three-
point deformation tests, where stiffer and denser architectures
require stronger force to bend (Figure 2g). Embedding the GFs
at density of 5 mm–1 nearly doubled the mechanical stress rel-
ative to the pure AG film with more than 100% strain at the
point of rupture (Figure S4b, Supporting Information). After
the AG layer was torn apart, the GFs were broken (Figure S4c,
Supporting Information).
2.3. Directing the Motion by Orientated Reinforcing Elements
Since the GFs should behave as mechanically reinforcing
1D elements, the orientation of the GFs was expected to
affect the elastic tensors and hence, to direct the deformation
of the film strips. To test this hypothesis, strips were cut out
that contained a network of parallel GFs perpendicular to the
long axis (⊥L, TGF@AG; Figure 1g). Since these dynamic
elements are reinforced normal to their longer side, the
hydration-induced expansion along a was not restricted, and
they bent away from the source of humidity when exposed
to humidity on either face (Figure 3a,e and Movie S2, Sup-
porting Information). In line with the loss of directionality
(relative to AG/LGF@AG), the bending force in the mechan-
ical tests was identical on both sides of the strip (Figure 3g).
The bending was reversible; after the source of humidity was
removed the film recovered its original shape (Movie S3,
Supporting Information).
The lack of bending directionality in AG/TGF@AG
prompted us to investigate the effect of aspect ratio on the
mechanical response. While keeping the absolute width
a of the strip constant, the aspect ratio was decreased to
L/a ≈ 1 by reducing the length L (square shaped film). As
shown in Figure 3b, this resulted in stochastic response to
humidity. When it responded, the film was capable of curling
either perpendicular or along the direction of the GFs. This
result demonstrates the interplay between the aspect ratio
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Figure 2. Kinematics of a hygroresponsive actuator with parallel reinforcing fibers (AG/LGF@AG). a) When exposed to humidity emanating from
a water droplet, the film bends only when exposed on the AG face, but remains straight when exposed on the LGF@AG face. b) A film of pure AG
bends to the same extent when exposed to humidity regardless of the exposed side. The two faces of the film are marked “A” and “B” for distinction.
c) The bending degree depends on the density of GFs (expressed as number of GFs per width a of the film). The size of all films used in the humidity-
induced bending tests was 1 cm × 3 mm × 60 µm. d) Schematic of the three-point bending experiment designed to measure the bending force that
can be induced on either side of the bilayer. e) Three-point bending tests showing that the bending forces on both sides of films of pure AG are nearly
identical. f) The force on the LGF@AG layer (bending toward the side of the LGF@AG layer) in an AG/LGF@AG bilayer is stronger than the force on
the AG layer (bending toward the side of the AG layer). g) Effect on the density of the GFs of the bending force required for three-point bending of the
AG/LGF@AG film.

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Figure 3. Kinematics of hygroresponsive actuators with perpendicular and oblique reinforcement. a) Cartoon showing the direction of exposure to
humidity on the deformation of an actuator having perpendicular reinforcing GFs (AG/TGF@AG) running ⊥L. For high aspect ratios, the bending is
bidirectional but it always occurs along the long side. b) Decreasing the aspect ratio to unity results in stochastic, nondirectional mechanical response.
c) Further shortening of the film effectively affords structure identical to AG/LGF@AG (GFs ||L) and correspondingly, results in unidirectional bending.
d) Sketch of the deformation of AG/OGF@AG actuator having GFs at 45° to the long axis of the ribbon, L. The strip can twist into helices of opposite
handedness. e) Bending of AG/TGF@AG film exposed to humidity. f) Bending of AG/OGF@AG film exposed to humidity. g,h) Bending force, measured
in three-point bending geometry, of AG/TGF@AG and AG/OGF@AG strips. The dimensions of the ribbons in all cases were 1 cm × 3 mm × 60 µm.

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and direction of the reinforcing architectures—the direction-
ality can be controlled by introducing anisotropy in the elastic
response only with actuators having aspect ratios >1. The obser-
vation aligns well with the natural shape of common biogenic
dynamic elements such as leaves and awns, which are always
naturally elongated (Figure 1a–d). As shown in Figure 3c
and in line with these conclusions, further reduction of the
length (L) effectively switches the film from AG/TGF@AG to
AG/LGF@AG; hence, similar to AG/LGF@AG, the film reac-
quires directionality of motion.
The control of directionality by orienting directing structural
elements within the flexible matrix and by combining bending
and curling elicits more complex kinematic patterns that
cannot be attained when using simple bilayer structures.[42–44]
Alignment of the GFs at an angle of 45° with respect to
L (AG/OGF@AG, Figure 1g) restricted the hydration-induced
expansion along the direction of the GFs in the OGF@AG layer
and resulted in either left-handed or right-handed coiling of the
strip into a helix upon exposure to a weak flow of humid air
(Figure 3d and Movie S4, Supporting Information). When the
AG/OGF@AG strip (5 mm wide, 100 µm thick) was placed on
a moist substrate with the OGF@AG layer in contact with the
surface, it coiled into a helix that had the OGF@AG layer on
the outer and the AG layer on the inner surface (Movie S5, Sup-
porting Information). The reason behind this response is that
the restricted swelling along the short axis (a) relative to the long
axis (L) introduced anisotropy in swelling. However, when the
strip was placed with its AG layer in contact with the surface,
it did not form a helix but tended to curl along the shorter axis
instead. This behavior corresponds to more isotropic swelling,
where the film can curl both along the long and short axes.
Decreasing of the thickness to ≈40 µm and the width to ≈3 mm
effectively restricts the curling along the short axis and results
in left-handed or right-handed twisting motion (Movie S5, Sup-
porting Information). As in previous cases, AG/OGF@AG shows
different response (handedness) when exposed to humidity
on different sides, regardless of the fact that the response
does not correlate with the direction of applied external force
(Figure 3h). The rate of twisting of the strip depends on its
thickness. An ≈100 µm-thick OGF@AG film underwent slow
twisting when exposed to humidity. Decreasing the thickness to
≈60 µm resulted in a remarkable enhancement of the curling
and decrease of the helical pitch; the strip quickly curled into
a helical multilayer tube (Figure 3f and Movie S4, Supporting
Information). Therefore, both the sensitivity to humidity and the
response time of the hygroresponsive strips can be improved by
reducing their thickness, providing additional means for control
over the mechanical response of hygroactuated devices.
Since the hydrogels are elastically reinforced by glass fibers
that aid the recovery of the original shape after the internal
bending moment has vanished, these bilayer structures can
be used to perform work. A simple helical structure was pre-
pared by coiling a 3 mm (width) × 60 µm (thickness) ribbon of
AG/OGF@AG around a glass rod (Ø3 mm). The ribbon was
dried during 2 h at 70 °C and affixed to a solid support at one
end. A metal ring was attached at the free-hanging end of the
helical strip (Figure 4a). When humid air (35 °C) was supplied
from one side, the strip quickly uncoiled due to asymmetric
expansion caused by swelling, thereby lowering the height of
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the ring. After the supply of humid air was terminated, the
helix recoiled again by shrinking due to dehydration, and the
ring was hoisted to its original position. This helical dynamic
element of AG/OGF@AG acts as a humidity-driven unidirec-
tional twisting actuator (Movie S6, Supporting Information).
However, unlike the nonpretreated strips, the coiling (dehydra-
tion) is much slower than the uncoiling (hydration).
To design a controllable, bidirectional twisting actuator, two
helices made of OGF@AG of identical chirality were joined
together by a metal ring (Figure 4b and Movie S7, Supporting
Information). When humid air was supplied to the upper half
of this device, the upper strip uncoiled, forcing the lower strip
to simultaneously coil at the same rate. By redirecting the flow
of humid air from the upper to the lower half of the device, the
lower strip uncoiled, thus causing coiling of the upper half. This
bidirectional twisting actuator that resembles the coiling and
overwinding of cucumber tendrils[2] provides a remote control
over the direction of rotation of the joint ring solely by humid air
where the direction of rotation can be switched simply by shifting
of the source of humidity. In a similar biomimetic application,
a ribbon of AG/LGF@AG was used to simulate the behavior of
some seeds that profit from the periodic changes in humidity by
deformation for self-burial in arid areas. The seeds of Erodium
for instance are effective drillers that burrow themselves into the
soil for germination by coiling/uncoiling cycles driven by periodic
changes in aerial humidity.[45,46] As shown in Figure 4c and Movie
S8 (Supporting Information), a ribbon of AG/LGF@AG attached
to a small wooden cone coils upon hydration and uncoils by spon-
taneous dehydration. The coiling/uncoiling cycles can be repeated
by periodic exposure to humidity, and this action causes the
wooden cone to drill into a bed of silica beads in a manner that
resembles closely the drilling mechanism of Erodium awns.[45,46]
To further understand the role of GFs in modulation of the
motion of humidity-driven polymer actuators, we designed more
complex architectures where two networks of GFs were paved
in perpendicular (AG/PGF@AG) or skewed (criss-crossed)
(AG/SGF@AG) alignment to each other and embedded in one
of the AG layers (Figure 1g). The second layer was pure AG.
In the case of the AG/PGF@AG actuator, the hydration-induced
expansion is restrained within the PGF@AG layer (GFs aligned
both ||L and ⊥L), but is unrestricted in the AG layer. As a result,
the actuator exhibited only unidirectional hygroinduced bending
(Figure 4d and Movie S9, Supporting Information). The three-
point bending measurements (Figure 4f) reflect a great differ-
ence between the forces that are required to bend the element
on the two faces as a result of the strong reinforcement of the
GF layer, particularly in the direction ||L, which limits its expan-
sion. By analogy with a single layer of GFs with a skewed align-
ment, it was anticipated that the actuator AG/SGF@AG having
two layers of criss-crossed GFs would coil or twist in response
to humidity. However, the experiments showed exclusively
unidirectional motion (Figure 4e and Movie S10, Supporting
Information). This result could be explained by the alignment
of the GFs. The two networks of GFs restrict the expansion of
the SGF@AG layer equally but in opposite directions, while the
swelling of the AG layer is unrestricted, which eventually leads
to bending of the actuator to the side of the SGF@AG layer. The
mechanical tests confirmed that a stronger force is required to
bend the actuator toward the AG layer (Figure 4g).
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Figure 4. Biomimetic dynamic elements and hygroinduced motility of framework-reinforced actuators. a) Unidirectional humidity-driven twisting of
OGF@AG actuator lifts a metal ring as cargo. b) Bidirectional twisting actuator composed of two helical strips of identical handedness connected by a
metal ring. Alternative exposure of one half of the actuator to humidity forces simultaneous coiling of the other half. The direction of ring rotation can
be switched by vertical shuffling of the humidity source. c) Humidity-driven self-drilling actuator of AG/OGF@AG that simulates the drilling action of
seeds of Erodium. d,e) Monodirectional bending actuators AG/PGF@AG and AG/SGF@AG with buried perpendicular and criss-crossed alignment of
reinforcing GFs. f,g) Bending force of AG/PGF@AG and AG/SGF@AG strips measured in three-point bending geometry. The thickness of the helices
and ribbons used in (a,b,c) is 60 µm. The dimensions of ribbons in (d,e) are 1 cm × 3 mm × 60 µm.

2.4. Conversion of Humidity Gradient to Electricity
To demonstrate the performance of the actuator for conversion
of the energy stored within the humidity gradient to mechan-
ical work, a film (10 mg) of AG/LGF@AG was coupled with a
flex sensor using a silk thread (this setup separates the sensor
from humid environment thus avoiding the detrimental effects
of humidity on the sensor). A 9 µm-thick polyvinylidene fluo-
ride (PVDF)-based bending sensor weighing 5 mg was used as
a piezoelectric transducer that converts the mechanical force
to electrical power (Figure 5a). Periodic exposure to humidity
of the film triggered reversible bending. The signals were
delivered to a generator through the silk thread, thus inducing
reversible bending of the generator and generating an alter-
nating current to pass through a 10 MΩ resistor. The peak
output was ≈0.8 V (Figure 5b). The output voltage depends
on the bending degree of the PVDF piezoelectric transducer,
which is determined by the degree of bending of the film of
LGF@AG. The hygroinduced bending of the film of LGF@AG
can be quantitatively assessed from the output voltage. By har-
vesting the energy of the humidity gradient, this device gen-
erates average power output 2.99 nW and power density of
299 µW kg–1 (per mass of the film actuator) (Figure 5c) that is
comparable to the reported value of 56 µW kg–1.[16] The accu-
mulated energy delivered to the resistor raises up to 500 nJ
within 3 min (Figure 5d). This simple device provides a proof
to the concept that the bilayer composite actuator is not only
capable of measuring aerial humidity, but it also holds poten-
tial for real-world applications within the context of alternative
energy transduction.

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Figure 5. Miniature humidity-driven power plant. a) Sketch of a device for humidity-to-electricity conversion. A strip of AG/LGF@AG that acts as humidity-
powered actuator is combined with piezoelectric transducer made of PVDF thin film. The humidity-triggered bending moment of the actuator provides
impetus to the generator, resulting in generation of electrical energy. b) Output voltage produced by the combined PVDF-based generator across a 10 MΩ
resistor. c) Instantaneous power calculated from real-time output voltage values. d) Cumulative electrical energy delivered to the resistor with time.

2.5. Mathematical Model for Mechanical Reconfiguration
of Fiber-Reinforced Bilayers
The type of deformation, intensity of the effect, and most impor-
tantly, the directionality of the bending are determined by the
orientation of the microfibers. To explain these effects, we set a
mathematical model for mechanical reconfiguration (reshaping)
of actuators reinforced by an array of unidirectional fibers. In
the first approximation, it can be assumed that the deformation
of the reinforced ribbon occurs by simultaneous deformation
of both layers along the direction of the fibers. This situation is
equivalent to equal local longitudinal deformations of the fibers
and the surrounding matrix, that is, in absence of sliding of the
fibers within the matrix. In such an idealized system, the model
assumes glass fibers of diameter d buried at definite depth zg
in an AG strip of thickness h and width a. Initially, the AG
matrix has Young’s modulus E0 and Poisson’s modulus p. Since
Young’s modulus of the glass fibers Eg is substantially larger
than E0 it is also assumed that any stresses in the fibers caused
by deformation of the matrix in the direction transversal to the
fibers or shearing of the matrix are negligible. In effect, the only
nonzero stress in the fibers will be that caused by their longitu-
dinal deformation.
The reinforcing effect of the fibers can be included in the
model by considering a composite structure where a layer
of reinforcing material that has an effective stiffness tensor
is incorporated into the AG matrix. If we set the x axis in the
direction of the fibers in the reinforcing layer and assume that
the only nonzero stress component of the fibers in response to
the deformation is along the fiber direction (σxx) that arises in
response to the longitudinal deformation of the composite only
(εxx), it follows that the effective stiffness tensor of the GF layer
has only one nonzero component, c1111. Its value can be esti-
mated as follows. In the layer of cross-section d × a there are n
fibers with cross-section πd2/4 each. Thus, the mean stiffness of
this layer is
nπ d (1)
c 1111 = Eg ≡ c0
4a
It should be noted that Equation (1) is only a rough estima-
tion. Due to the contact with the (hard) fibers, a relatively softer
material such as AG should effectively become more rigid in
response to shear and transversal stresses in a region around
the fiber, with d being the characteristic width of that region.
This implies that d in Equation (1) should be somewhat larger
than the fiber diameter; this detail, however, does not affect the
qualitative conclusions. Provided that the fibers are oriented
along its long axis x, such as is the case with LGF@AG, the
stiffness tensor described above can be used to describe the
stresses and deformations in a composite ribbon.
If the reinforcing layer is pivoted at an angle around the z
axis (the axis normal to the ribbon surface) the tensor should be
transformed to reflect the orientation of the fibers in the local
coordinates of the ribbon. This is achieved by setting
′
c ijkl = aip a jq akr als c ipqrs (2)
where aij is the rotation matrix and summation over pairs of
repeating indices is assumed. Rotation about z by angle α is
represented as (3)

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⎛ cos (α ) − sin (α ) 0 ⎞
⎜ ⎟
a ij = ⎜ sin (α ) cos (α ) 0 ⎟ (3)
⎜⎝ 0 0 1 ⎟⎠
If the layer is rotated by a right angle, like in TGF@AG, the
only nonzero component of c′ijkl is c′2222 = c0, corresponding to
orientation of the fibers along y. A notable feature of this case
is that the deformation along the long axis of the ribbon does
not induce longitudinal stress in the GF layer. On the contrary,
being related to its Poisson modulus, the transversal deforma-
tion of the matrix induces stress in the fibers, which should
appear as effective change of the Poisson modulus of the entire
composite. As a result, it is anticipated that the reinforcing
effect in case of TGF@AG will be much less pronounced if pre-
sent at all. In this case, the GF layer can influence the longitu-
dinal stiffness of the ribbon indirectly, by affecting the effective
Poisson modulus.
Furthermore, if the layer is rotated by π/4, such as is the case of
OGF@AG, there will be six symmetrically independent nonzero
components: c′1111 = c′2222 = c′1212 = c′1122 = c′1112 = c′2212 = c0/4.
The most important feature of this tensor is the nonzero c′1112
(as well as c′1211, to which it is symmetry related). The longi-
tudinal deformation of the composite ribbon along the x axis
causes shearing stress σxy in the GF layer which generates
torsional moment in the AG matrix. Moreover, the shear defor-
mation εxy in the ribbon, which appears as a result of the tor-
sional moment, causes longitudinal stress σxx in the GF layer,
and modifies the bending moment in the matrix. The outcome
is a helix-like deformation of the ribbon.
The bilayers having net-like arrangement of GFs can each
be considered as being composed of two layers of unidirec-
tional GFs with different orientations. Thus, the stiffness
tensor of PGF@AG can be represented as a sum of the ten-
sors of LGF@AG and TGF@AG and its mechanical response
displays features that are characteristic to both LGF@AG and
TGF@AG. The nonzero components of this stiffness tensor
are c′1111 = c′2222 = c0. SGF@AG can formally be considered
a superposition of two layers of OGF@AG that are offset by
rotation by ±π/4. Its stiffness tensor has only the components
c′1111 = c′2222 = c′1212 = c′1122 = c0/2, while c′1112 and c′2212 are
absent. This result explains the loss of ability of SGF@AG to
twist in response to bending moments. In all other aspects but
the magnitude of the mechanical response, this hybrid behaves
similarly to PGF@AG because the rhombus-like net can be
obtained by taking the square net (PGF@AG) over a π/4 rotation.
2.6. Characteristics of the Main Deformation Components
of Ribbons and the Reinforcing Effect
The effects within this model require calculation of the energy
of deformation of the ribbon by assuming that the deformation
can be represented as a combination of εxx, εyy, and εxy (note
that although εzz is included, its value is determined by the con-
dition of the plane stress state, σzz = 0, and is thus irrelevant
for the model). All deformation components are assumed to
be linear functions of the z coordinate. This set of parameters
is sufficient to describe combination of uniform deformation,
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twisting and bending of a thin ribbon (L  a  h). The two
most important parameters of the deformation are the twist ϑ,
defined as the rate of change of rotation around the x axis
∂ϕ yz ∂ε xy
ϑ≡ = (4)
∂x ∂z
and the curvature k, which is identical to the reciprocal curva-
ture radius R −1 and is equal to the rate of change of rotation
around the y axis
∂ϕ zx ∂ε xx
k≡ = (5)
∂x ∂z
The nonuniform stiffness of the composite ribbon caused by
the presence of the GF@AG layer changes its bending and tor-
sion stiffness. If the ribbon is solely deformed by external torsion
or bending moments, the change in sign of the moment will only
alternate the signs of the stress and deformation tensors provided
that a linear relation between them is maintained (i.e., the elas-
ticity is linear). It follows that the signs but not the magnitude of
the twist ϑ and the curvature k depend on the sign of the corre-
sponding moments. From the sections of the force-displacement
curves shown in Figures 2e,g, Figure 3g,h, and Figure 4f,g with
positive slope that correspond to the elastic part of the tensile
action, it is seen that the central deflection of the ribbons does
not depend on the ribbon face to which the force is applied. This
evidence shows that the bending stiffness of the reinforced rib-
bons is insensitive to the bending direction. The magnitude of the
reinforcement effect, which can be estimated from Figure 2e,g,
indicates that the bending stiffness of the ribbon with glass fibers
of GF density 7 mm–1 is about 2.5 times that of pure AG.
2.7. Correlation with the Humidity-Induced Deformation
In contrast to the deformations caused by external forces
described above, a qualitatively different picture was observed
experimentally with deformation of the films induced by
humidity. Nevertheless, the fact that we observe different
bending by exposing different faces of the composite ribbons
to vapors does not contradict the previous statement that the
bending should not depend on the bending direction in case of
external bending moment. The asymmetric response is intrinsic
to the nature of the bending force in this case. When an external
moment is applied, the orientation of the sample does not
determine the moment as it is applied externally. However, if
the moment appears as an internal response to some external
conditions, its magnitude can depend on the sample orientation
relative to the external stimulus (e.g., the source of humidity).
In other words, the evolution of a (deformation) moment is the
response of a nonuniform structure to nonuniform conditions.
Thus, if the magnitude of the moment depends on the exposed
ribbon face, a different bending response can be anticipated.
The process of water absorption occurs as a sequence of
three processes. First, water is adsorbed onto the surface that
faces the source of humidity (the water droplet). Second, the
water diffuses across the sample thickness and into the bulk.
Finally, the water is desorbed from the face opposite to the
Adv. Funct. Mater. 2016, 26, 1040–1053
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source of humidity. After some time, this dynamic system
eventually reaches one of the two possible stationary states.
Depending on the relation between the rates of diffusion,
adsorption, and desorption, the concentration of the absorbed
water eventually becomes uniform across sample thickness, or
alternatively, a constant gradient of water concentration may
be established across the depth of the adsorbent. It is obvious
that in the former case both faces will respond in identical way
because identical distribution of water is ideally established on
the two faces. Since only the second case provides the anisot-
ropy required for macroscopic deformation, a gradient in water
content must be established across the sample depth.
2.8. Equilibrium Shape of the Reinforced Ribbons Exposed
to Humidity
The mechanical equilibrium that ultimately determines the
ribbon shape can be calculated by minimizing the energy in
respect to the deformation tensor. This allows the equilibrium
shape of the ribbon for various GF architectures to be pre-
dicted. The energy is calculated as
h z g + d/ 2
a a
2 ∫ ij ij ∫
W= σ AGε AG d z + σ ijGFε ijGF d z
2
z g − d/ 2
0 h
FULL PAPER
The first equation in this set describes uniform expansion
along the ribbon axis exx and uniform bending within the xz
plane with curvature k. The second equation is the uniform
deformation along the y axis only. Note that the bending along
the short ribbon axis is not accounted for here, because under
high curvatures k observed in the experiments it is highly
unlikely for dynamic elements like the ones used (a >> h)
to bend simultaneously in both directions; instead, the rib-
bons will bend mainly in one direction. Indeed, in line with
the results from the experiments, the preferred direction for
bending is the longer axis or the one that corresponds to lower
stiffness.
The third expression in Equation (9) is a combination of the
uniform shear exy and the uniform twist ϑ, and the fourth is a
result of the plane stress condition. The last equation is a rea-
sonable approximation that summarizes a number of condi-
tions (zero net shear forces on the outer boundaries relative to
both components in this equation, εxz = 0 in most part of the
twisted plate if a >> h, and εyz being negligible relative to εxy
because the twist along the short ribbon axis is negligible due
to much higher twist stiffness for L >> a). The five unknown
parameters in Equation (9) (exx, eyy, exy, k, and ϑ) can be defined
by minimization of the energy given by Equation (6) which can
now be expressed in terms of the deformations as
(6)
aE 0 ⎛ 1

2 ⎝ (1 − p 2 ) ⎣⎢( ) ( yy )
⎡ ε xx
AG 2 + ε AG 2 + 2 pε AGε AG ⎤dz
where the superscripts of the tensor components indicate the cor-
W= ⎜ ∫ xx yy
⎦⎥
0
responding material of the composite (note that the stress com- (10)
ponents labeled with GF do not refer to the stress of the glass h z g + d/ 2 ⎞
1
1+ p ∫ ∫ C ijkl ε ij ε kl dz ⎟⎟
fibers but to the mean effective stress of the GF layer). As the + ε xy
2 dz + ξ

portion of the total volume taken up by the fibers is negligible, 0 z g − d/ 2 ⎠

Equation (6) does not account for the corresponding decrease of
the AG volume in the first term. As the glass fibers are not sensi- where Cijkl = c′ijkl/c0 is a dimensionless stiffness tensor of the
tive to humidity, their deformation equals to the deformation of GF layer, which is fully defined by the combination of orienta-
the ribbon relative to its initial state (before deformation) tions of the fibers in the local coordinate system of the ribbon,
and ξ = c0/E0 is a dimensionless parameter defining the mag-
ε ijGF = ε ij (7) nitude of the reinforcement effect (ξ = 0 corresponds to the
plain AG ribbon). Minimization of Equation (10) according to
To calculate the energy, we should use the deformation of the the condition
AG matrix relative to its local equilibrium state, corresponding
to the local water content ∂W ∂W ∂W ∂W ∂W (11)
= = = = =0
∂e xx ∂e yy ∂e xy ∂k ∂ξ
z
ε ijAG = ε ij − δ ij ε 0 (8)
h affords equilibrium values of the five unknown variables as
functions of six parameters of the problem (ε0, h, d, zg, p, ξ).
Where δij is the Kronecker delta, ε0 is the linear expansion of As it can be concluded from the format of the above equations,
AG due to change of water content on the side of the ribbon all deformation components are linear, uniform functions in
exposed to humidity (the side for which z = h). The deformation respect to the parameter ε0. In addition, all dependencies on
tensor εij of the ribbon-like plate that is uniformly deformed, z can be expressed as functions of a dimensionless coordi-
twisted, and bent along its long axis can be defined by nate, z/h. Thereby, the most interesting results of the solution,
the curvature k, and the torsion ϑ, can be expressed as the
ε xx = e xx + kz following functions
ε yy = e yy
ε xy = e xy + ϑ z ε0 ⎛ d zg ⎞
(9) k= F , , p, ξ ⎟
h ⎜⎝ h h ⎠
p
ε zz = −
1− p
(ε xx + ε yy ) (12)
ε0 ⎛ d zg ⎞
ϑ= G , , p, ξ ⎟
ε xz = ε yz = 0 h ⎜⎝ h h ⎠

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 www.afm-journal.de
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FULL PAPER

Figure 6. Model of the deformation of fibril-reinforced flexible bilayer actuator. Variation of a) curvature of AG/LGF@AG, b) curvature of AG/PGF@AG,
c) curvature of AG/OGF@AG, d) torsion of AG/OGF@AG, e) curvature of AG/SGF@AG, and f) the helix angle of AG/OGF@AG with the reinforce-
ment parameter ξ and the relative (zg/h) depth of the glass fibers (GFs) within the actuator.

The problem can be solved arithmetically; however, the func-
tions F and G are cumbersome. In Figure 6, these functions are
plotted against the relative depth of the GF layer in the ribbon
zg/h and the reinforcement parameter ξ. The plots are calcu-
lated for d/h = 0.1 and p = 0.3.
2.9. Correlation of the Model with the Experimental
Observations
As shown in Figure 6a,b, the model predicts very similar
results for AG/LGF@AG and AG/PGF@AG. If the GF layer
is located on the face opposite to the one exposed to humidity
(zg = 0), then the curvature is scarcely affected by the reinforce-
ment, regardless of the stiffness of the layer. There is no effect
even when the GF layer lies in the middle of the ribbon depth,
as expected from its proximity with the neutral plane (a geo-
metrical set of points that defines a layer which retains its size
during the deformation). The strongest effect is predicted for
the case when the GF layer lies near to the surface exposed to
humidity (zg = h). The curvature decreases with increased stiff-
ness of the GF layer ξ, and at characteristic values ξ > 10 it
could even change its sign. As the AG/LGF@AG film did not
demonstrate any significant curvature when its reinforced face
was exposed to humidity, ξ was estimated to ≈10. This value
is exceedingly large, and would imply Eg ≈ 1000E0, which is a
clearly an overestimated value relative to the experimental data,
Eg ≈ 30E0 (Eg ≈ 70 GPa, E0 ≈ 2.4 GPa).
There are at least two possible explanations for this discrep-
ancy. First, the water adsorption by AG could affect the stress. As
the GF layer hinders free expansion of AG induced by the action
of humidity on the reinforced face, it also causes compressive
stress in the area beneath the surface. If the compressive stress
suppresses the water adsorption, less water will be adsorbed and
the respective moment is expected to decrease. In effect, the rein-
forcement will be amplified. However, it should be noted that the
experiments described above are not directly comparable with
the model. For example, while Figure 2c demonstrates nearly

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twofold decrease in curvature by increasing the stiffness of the
GF layer by increasing the GF density from 1 to 7 mm–1 when
humidity is applied to the AG face, the present model (Figure 6a)
shows negligible curvature decrease. This effect cannot readily
be accounted for by the above hypothesis of stress-dependent
water adsorption because the development of stress on the face
opposite to the one exposed to humidity is unlikely.
A second possible explanation for the discrepancy is that the
initial assumption of zero curvature along the shorter side of
the ribbon is incorrect. As the overall effective bending stiffness
increases with the stiffness of the GF layer (i.e., with the fiber
density), the ribbon becomes more prone to curving along the
shorter (less resisting) side. Modeling of large and simulta-
neous bending of reinforced plates in both directions is a theo-
retically involved exercise, for which there is no simple solu-
tion. Nevertheless, a relatively simple behavior outcome can
be predicted. When bending in one direction prevails, the thin
plate becomes effectively thicker in the other direction, thereby
greatly increasing the stiffness for bending in that direction.
This hypothesis is in line with the experimental results. More-
over, in case of GF density of 5 and 7 mm–1, Figure 2c shows
irregularities in the curvature, in support of the tendency of the
ribbon to bend along the short dimension.
It should be noted that the behavior of the AG/TGF@AG
film is not included in Figure 6 because its curvature does not
depend on the reinforcement parameters; the film bends similar
to that of pure AG. However, in view of the second hypothesis
above, it is expected that the stiffness of the GF layer will affect
the curvature. This is a reasonable assumption because the
higher the TGF layer stiffness is, the higher the bending stiff-
ness related to the shorter dimension of the ribbon will become.
In turn, the system better resembles the present model, that is,
the bending along the long ribbon axis is facilitated by smaller
bending along the width and poses less hindrance.
The results of the modeling of the bending of AG/SGF@AG
demonstrate an interesting increase in curvature when humidity
is applied to the AG face of the ribbon (Figure 6e). This effect is
a result of the expansion upon water absorption. The expansion
along the shorter side causes nearly identical contraction in the
perpendicular direction of the SGF layer because of the special
feature of the stiffness tensor, where c′1122 is identical with c′1111
and c′2222. The behavior of the dynamic element can be visualized
as an anisotropic 2D elastic band: if the band is stretched along
one of the directions along the rhombus diagonal, it will shrink
equally along the other direction. This ultimately results in expan-
sion of the humidity-exposed side of the ribbon and shrinking of
the opposite side (SGF side) along the ribbon axis, and will evi-
dently increases the bending moment and the final curvature.
Finally, the effect of exposing the SGF side of the actuator to
humidity is hardly distinguishable from that of AG/PGF@AG.
Among the geometries of the GF reinforcing architectures,
the directionality of the AG/OGF@AG structure (Figure 1c)
appears to be the most peculiar case. The model in this case
predicts simultaneous bending and twisting (Figure 6c,d),
which should result in coiling into a helix. Thus, the model is
capable of predicting the asymmetric twisting response. The
exposed side, however, should determine the twisting direction;
applying humidity on opposite sides of the ribbon should result
in coiling in opposite directions. Moreover, the exposed face
Adv. Funct. Mater. 2016, 26, 1040–1053 © 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
www.afm-journal.de
FULL PAPER
also determines the degree of twisting; exposing the OGF side
to humidity should result in stronger coiling than when the AG
side is exposed. The degree of helical coiling can be conveni-
ently represented by the helix angle, which is defined by
ϑ
tg (ϕ ) = (13)
k
Accordingly, a helix angle close to zero corresponds to an
almost unwound helix (analogous to stretched, nearly flattened
spring), while helical angle of π/2 represents a very tight helix.
The variation of the helical angle with the model parameters is
shown in Figure 6f.
Exposure to the humidity of the OGF side results in forma-
tion of tight helices with helical angles close to π/4, whereas
exposure of the opposite case brings about angles less than the
limit of 15°. At least qualitatively, these results agree with the
experiments. However, the asymmetry in the coiling magni-
tude may indicate that the coiling could be alleviated by curling
along the short axis of the ribbon. The current model for defor-
mation of reinforced actuating ribbons could also be applied
for correlation with the results of the three-point bending tests
described above (see the Supporting Information).
3. Conclusions
In summary, composite bilayer actuators based on natural
hydrogel reinforced by a variety of patterns of microfibers
were designed and prepared. These composite structures are
capable of versatile actuation modes that are analogous to the
motility of some dynamic tissues in biological systems. They
are capable of converting humidity-triggered anisotropic expan-
sion/contraction into large macroscopic deformations that
appear as reversible bending, curling, and twisting through a
mechanism that involves anisotropic restriction of the hygroin-
duced expansion by the fibers and results in an asymmetric
swelling of the bilayer. This approach allows control over
the type of deformation and the intensity of hygroinduced
mechanical response. The composite bilayers can be further
processed into simple actuating devices that perform work by
transporting cargo or be combined with a piezoelectric gener-
ator into energy transducers that convert the potential energy
of humidity into electricity. The output voltage can be con-
trolled by adjusting the bending degree of the composite bilayer
through variation of the density of the GFs in the GF@AG layer.
While these simple devices demonstrate the potentials of the
composition actuator for energy conversion, any real-world
applications in continuous mode would require mechanical
gearing of large number of actuators or fabrication of actuating
elements where the mechanical effect induced by humidity is
offset by another stimulus (e.g., heat) to induce switching of
the dynamic element between at least two states. Mathematical
model was developed that explains the response of linearly
reinforced bilayer structures. This approach also provides a
proof of concept to the mechanisms of kinematic control of
directionality of mechanical deformation and reinforcement in
biogenic dynamic elements that is readily accomplished by ori-
ented fibrous architectures in amorphous matrices.
wileyonlinelibrary.com 1051
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FULL PAPER
4. Experimental Section
Preparation of the Actuators: A precleaned glass slide
(2.5 × 7.5 cm) was paved with parallel GF strings with a diameter of
5−10 µm. A solution of AG (Powder was purchased from Sigma-Aldrich)
in dimethylformamide (DMF) containing 0.1 wt% Rhodamine B to
visualize the colorless film was casted onto the surface of the GFs at
25 °C. After drying (5 h), an identical volume of AG/DMF solution was
casted onto the surface of the first layer. After solidification (25 °C, 6 h),
the composite was dried in a vacuum oven at 50 °C overnight. The
raspberry red film was retrieved using a blade and was cut in various
shapes. A series of samples with varying alignments of the GFs were
cut out with a thickness of ≈60 µm (Figure 1g). These actuators can be
considered a bilayer structure with one layer being of pure AG and the
other layer containing GFs.
Testing of the Humidity-Driven Bending, Curling, and Twisting:
A water droplet (≈1.5 cm in diameter) was placed on a hot plate
(≈50 °C) and allowed to thermally equilibrate for 5 min (Movies S1 and
S2, Supporting Information). The film (1 cm × 3 mm × 60 µm) was
brought close to the droplet. Both sides were exposed to the vapor
emanating from the droplet and the response was recorded. The curling
and twisting required higher relative humidity. A 100 mL two-neck round
flask filled with 50 mL water at 50 °C was used as source of humidity.
Produced humid gas at very low flow rate was purged over the water and
used to induce deformation of the films which were held at ≈1 cm from
the outlet (Movies S3 and S4, Supporting Information). The response
was recorded using an iPhone 4 (Apple Tech) for further analysis.
Scanning Electron Microscopy: Scanning electron microscopy
micrographs were taken with a Quanta FEG 450 electron microscope
with primary electron energy of 5 kV. The films were directly attached
to adhesive carbon tape. The micrographs were recorded at room
temperature at pressure of 8.8 × 10–7 Pa.
Three-Point Bending Testing: A small tensile tester MTII/Fullam
Semtester (MTI instruments) was utilized for the three-point bending
testing at 24 °C with load cell accuracy of up to ±0.2% of the full-scale
load range (0−225 N). Various films that were 3 mm wide, 60 µm thick,
and over 2 cm long were tested by bending with applying pressure on
either face at a rate of 10 mm min–1. The film was freely standing on the
sample supporting stage.
Tensile Testing: In the tensile tests at 24 °C, a sample with rectangular
shape (2 cm × 0.5 cm × 60 µm; Figure S4, Supporting Information) was
held by the grips of a screw-driven device using the tensile tester. The stress
was recorded while stretching the film until it failed. To study the effect of
humidity on the mechanical strength, the film was exposed to humidity
during varying time intervals before it was mechanically tested. The load cell
and extensometer were calibrated prior to use. The load was applied at a
crosshead speed 10 mm min–1 and the load range was 0–225 N. The tests
complied with the rules specified by the international standard norms.
Supporting Information
Supporting Information is available from the Wiley Online Library or
from the author.
Acknowledgements
L.Z. contributed to all aspects of this study. S.C. developed the
mathematical model. Y.W contributed to the synthesis of the actuators.
P.N. conceived the study. The manuscript was written through
contributions of all authors. All authors have given approval to the final
version of the manuscript. This work was supported by funding from
NYU Abu Dhabi and was partially carried out using Core Technology
Platform resources at NYU Abu Dhabi. S.C. thanks the Russian
Foundation for Basic Research (RFBR) for the financial support (Project
No. 14-03-00902). P.N. thanks NYUAD for the Research Enhancement
1052 wileyonlinelibrary.com © 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
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Fund (project “Smart Biomimetic Superhydrophobic Self-Cleaning
Materials”). We thank Dr. Nikolas Giakoumidis for his help with design
of the device for energy conversion and Dr. Patrick Commins for reading
the manuscript and language corrections.
Received: September 16, 2015
Revised: October 28, 2015
Published online: December 29, 2015
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