3.2.2 Morphing structures in plants Examples of morphing structures are abundant in nature.

Morphing structure is defined as macroscopic shape change here. Shape change of a biological species is a part of sequential event in a response to environmental change for a given biological species, which is composed of sensing and actuation. Fig. 5.1 shows a good example of such sequential events of sensing and rapid actuation (morphing) of a Venus fly trap leaves. In this section we will review the actuation which results in shape change while the sensing part will be reviewed in the next section.
Sensing hair

epidermis

+ K H2O

Parenchyma cells

vein

epidermis

+ H

expand (a) (b) (c) (d) Fig. 5.1 Venus Fly Trap action in catching a flying insect, (a) insect touches the antenna located in the middle of leaf, (b) rapid closure of the leaves trap the insect, (c) cross section view before the leaf motion (d) after the leaf motion(Taya, 2007). In the following, we will review five cases of morphing structures inherent in biology, (1) Venus fly trap, (2) Mimosa pudica, (3) tendril coiling, (4) twing of vines, (5) folding and unfolding of flowers and leaves, (6) insects eclosions ,(7) wing structures of eagles, bats and insects, and (8) plasmodal slime. After these examples, we will discus on some bioinspired morphing structures applied to aerospace structures. It is noted that the energy dissipations used in these actuations are minimum which is realized by the mode of shape changes, i.e., bending at localized joints, coiling for which limited shear stress is used. This demonstrates the fundamental principle of actuations associated in biological species, minimum Gibbs energy. 5.1.1. Examples of morphing structures in Nature (1) Venus fly trap The Venus Fly Trap leaf, Fig. 5.1, is designed to sense and trap flying insects by rapidly closing the leaf-like trap when triggered by sensing antennae located in the center of the leaf. The microscopic mechanism of the Venus Fly Trap leaf is based on controlled ion fluxes creating osmotic movement of water molecules toward the outer-most surface of the leaf, resulting in the expansion of the outer surface and bending. Leaves retain a flat shape as long as the resistance offered by upper and lower epidermis layers is equivalent, and pressure is evenly spread throughout the internal layer. But leaves fold when the outer epidermal cell layer suddenly expands while the inner does not. This ability to expand rests with the osmotic pressure created by an ATP-driven proton pump located on the plasma membrane, expels protons, creates both a very negative membrane potential (-

120 to 250 mV) and acidic external pH (Hodick and Sievers 1989; Stahlberg and Van Volkenburgh, 1999). Let us review the work of recent studies focusing on the mechanisms of morphing of Venus fly trap in the following. Forterre et al (2005) studied the motion of Venus fly trap lopes experimentally recording the shape change of lopes using high speed camera and observed the snap from concave outword to convex outward geometry of lopes. From this observation, they calculated strains along x- and y-directions, see Fig. 5.2(a). By using the model of poroelastic shell model which simulates the leaf, they proposed snap through bucking, some of such results are shown in Fig. 5.2(b). To explain the rapid snap through motion of the lopes, they used the poroelastic shell arriving at the time of such snap through , t=L2/(kE) (5.1)

where is viscosity of fluid that occupies the lope cells, L is the size of lope, k is the mean curvature and E is the Youngs modulus of dehydrolayed lope. Based on this formula, they predicted the speed of snap through as 0.1 second which coincides with that observed. The speed of the actuation of Venus flytrap lopes is proportional to square of the lope thickness based on the model proposed by Forterre et al (2005) which is challenged recently by Volkov et al (2008) who did a series of testing using Venus flytrap lopes of different thicknesses, claiming that the formula by Forterre is not valid.

Fig. 5.2 (a) measured strains along x-direction and along y-direction,(b) smooth snapping transition in leaf closure of Venus flytrap where mean curvature (km =(kx + ky)/2) is plotted as a function of kxn which is defined as 1-T where = L4k2/h2 with L is length, k is the initial mean curvature, h is thickness of leaf of Venus fly trap, T is nodimensional time (Forterre et al, 2005).

Volkov et al (2008), performed a well-defined experiment on Venus fly trap lopes by applying change where use of two Ag/AgCl electrodes, the positive electrode located at the midrib and the negative at one of the lopes. They first applied electrical stimulation(14C, 1.5 V) and measured the speed of the closure of the lopes in terms of ratio of opening (d) to the maximum opening(dmax) as a function of time in second, Fig. 5.3(a) which indicates very fast speed of the lope closure, within 0.3 second. In order to examine the condition under which the closure takes place, they conducted another test where charge input is primary input and the lope opening distance (d) was measured as a function of change, Fig. 5.3(b). Fig. 5.3(b) illustrates clearly that the lopes can accumulate the charge until 14mC, just after that the closure of lopes started and completed within 0.3 second.

Fig. 5. 3 Effects of applying charge on the opening of the Venus fly trap lopes(d), (a) relation between the ratio of d to maximum d(dmax) and elapsed time in second under initial charge of 14C applied to the lopes, (b) relation between applied charge and raio of lope opening to its maximum, d/dmax(Volkov et al, 2008). The experiments by Volkov et al using 200 Venus flytrap plants with different sizes of leave ranging from 1 cm to 5 cm reveal no dependence of the closing time on size of the leaf L. This contradicts with Eq. (5.1) which predicts a dramatic increase in the closing time for large Venus flytrap plants. Volkov et al also claims that the motion of Venus flytrap is smooth, not like snap through buckling which seems to be supported by the work by Nakano (2003), see Fig.5. 6.

(2) Mimosa pudica If leaves and/or petiole of Mimosa pudica are touched by a foreign object, the petiole falls downward in a second or so. This phenomena of Mimosa pudica has attracted strong attentions of many plant scientists, for example, Snow(1924) and Shibaoka(1966;1969). Shibaoka (1969) reviewed extensively the actuation mechanism of action plants including Mimosa pudica where he cited other researchers work as well as his own work. In Shibaoka (1969) review the motor cells play key role in which the stimulus exhibit the contractile vacuoles, not due to increase in the permeability of the plasma membrane, and

the contractile of the vacuoles are related to mechano-chemcial reactions with ATPATPase system. The propagation of action potentials are along vascular tissues (particularly phloem and neighboring tissues). Once such action potentials arrive at the motor cells underneath the pulvinus, Toriyama (1955) observed that potassium ion escaped from the motor cells to draw water out of the motor cells by osmosis, leading to collapse and folding down of the pulvinus. Later, Torimaya and Sato (1968) observed under microscope that main vacuole containing fibers and tannin vacuole which containing large amount of potassium ions can reduce their size so that the fibers are also contracted. Toriyama and Jaffe (1972) discovered that calcium held in the tannin vascuoles before the pulvinus movement appear to migrate to the central vascuole where the fibers may contact. This is similar to the contraction of animal muscle fiber where calcium plays a key role on the contractions of protein actomyosin (Simon, 1992).Jaffe (1973) speculated that the contractual motion of the midrib of Venus flytrap is actomyosin-like ATPase which is similar to the contractual motion of other action plants, pea tendril (Jeffe and Glaston, 1966; 1968) and Mimosa pudica (Lyubumova et al, 1964). Nakano (2003) studied the motion of Mimosa pudica by using high speed camera and measured the angle() between petiole and main pulvinus as a function of time (T) in second, see Fig. 5.4 from which the initial angle of 740 is changed to final angle of 210 within 2 seconds. They also measured the motor cell size change before and after touching of petiole of Mimosa pudica, Fig. 5.5 where the diameters of the motor cells above and below vascular bundles are recorded with darker blue for larger size and light blue to no color for smaller sized motor cells. Comparing Fig. 5.5 (a) and (b), we can conclude that the motor cells below the vascular bundles (located in the center of petiole) lost its osmotic pressure or equivalently its water which is considered to be contractile vacuoles as reviewed by Shibaoka (1969) in the earlier paragraph. However, the exact mechanism of triggering the shrinkage of motor cells in terms of loss of potassium ions from the motor cells( uptaking again water in the motor cells in the lower part in the long run) is not clear.

Fig. 5.4 Sequence of photos for movement of petiole of Mimosa pudica after leaves are touched where the angles () between petiole and main pulvinus as a function of time (T) recorded (Nakano, 2003)

(a)

(b)

Fig. 5.5 Motor cell diameters before (a) and after (b) the leaves of Mimosa pudica are touched where darker blue colored motor cells for larger diameters of the cells, and light blue to white colored cells are for smaller cell size(Nakano, 2003). The speed of petiole motion to change the angle from initially large to smaller angle is compared with that of the closure of Venus flytrap leaves, Fig. 5.6 where closing leaves of Venus flytrap is slightly faster than that of petiole of Mimosa pudica, but they are within 1 second or so. .

Fig. 5.6 Angle ratio change (t)/max of two different action plants, Mimosa pudica petiole and Venus Fig. 7 reveals the speed flytrap leavesthat where max is of the initial angle, and (t) is the angle at time t (Nakano,2003)

(3) of tendril coiling. Shape change in moving tendrils of various climbing plants (cucumbers, grapes, passion flowers, pumpkins and gourds) in search for stable support has been studied since Darwin (1865). In "The Movements and Habits of Climbing Plants," Darwin proposes that the helical formation is due to the asymmetric growth rate between dorsal and ventral sides of the tendril, i.e., the former rate exceeding the latter rate. Rainer (2002) examined the motion of cucumber tendrils which are associated with two coilings: primary (contact) coiling to sense stable support surface using tactile sensors and secondary (free) coiling to draw the stem of the plant closer to the support through the formation of a series of right and left handed helices, see Fig. 5.7. Jaffe (1977) and Jaffe and Glastone (1966) studied the contact coiling behavior of Alaskan pea with the aim of determining what environmental parameters give rise to larger coiling. It is the free coiling that attracted many researchers beyond botanists, in order to determine why left-handed and right-handed helices form with a reversal in between them, see Fig. 5.8.

Fig. 5.7 Sequence of tendril morphing in order to contact a secure object, then grabbing it by primary coiling, then moving the main body of the plant toward the secure object(Rainer, 2002)

Fig.5.8 Coiled tendril of Luffa cylindrica with the appearance of multiple reversals along the length(Eberle et al, 2009)

Junker (1977) studied the change in auxin (growth hormone) concentration located in dorsal and ventral domains of Passiflora quadrangularis and discovered that there was not a significant change during coiling. Instead, he hinted that action potentials and acid growth along the free coiling direction may be the main mechanism. Carrington and Esnard (1989) examined the coiling of two tendril-bearing plants, water melon (Citrullus lanatus), and passion fruit (Passiflora edulis). They observed that the contacted side of the tendril decreased the length while the non-contact side increased during primary coiling. They concluded that the mechanism of signal transduction from the contact site to the growth of motor cells and/or wall property changes are still a mystery. Thus, it is still not clear if asymmetrical motor cell growth or asymmetrical arrangement of tissues is mainly responsible for free coiling Mathematical models in explaining the above free coiling have been proposed. Keller (1980) proposed an elastic strain energy concept applied to thin elastic rod with boundary condition at support and derived that the helical shape can be predicted by the minimization of the Gibbs mechanical energy. Keller focused two cases, (i) tendril has free-end, (ii) tendril tip is constraint, such fixed with the contact coiling around the support. The solution of the minimization of Gibbs free energy for case (i) provides the helical shape of the tendril with free end, while the solutions of the second case leads to free coiling with reversals. Goriely and Tabor(1998) treated a tendril as thin elastic rod with intrinsic curvature and used linear and nonlinear stability analysis of such thin rod under various tension and concluded that the free coiling with a reversal can be predicted by their model. Following this work, Domokos and Healey studied the case of finite length with initial curvature and clamped ends, and predicted multiple reversals in free coiling of tendrils. Thomson et al (2005) studied the tendril-bearing plant, Luffa cylindrical, and measured the Youngs modulus of the tendril to find that the average value is 33 MPa which was used in their finite element

Experimentally measured strain

0.5

Experimentally measured strain

0.5

-0.5

a) Tendril 1
-1 0 0.2 0.4 0.6 0.8 1

-0.5

b) Tendril 2
-1 0 0.2 0.4 0.6 0.8 1

Normalized position (x)

Normalized position (x)

Fig. 5.9 Measured strains in dorsal (open circles) and ventral domains(filled triangles) of Luff cylindrical. It is noted that the dorsal strains are positive while the ventral strains are negative , and both increases with position toward the tip of the tendril( Eberle et al, 2009).

analysis (FEA). In the FEA input data set, they used the equivalent thermal strain to simulate the growth rate of tendril dorsal and ventral parts which are set in terms of thermal expansion coefficient, i.e. dorsal side being 0.001/C and ventral side being zero. Upon application of torsional perturbation around the tendril axis, they could produce the helical formation with reversal point. Following Thomson et al work, Eberle et al (2009) modified the FEA to study growth of another species of tendril-bearing plant: Adenia lobata. Using a set of marker painted sites, they measured total strain along the tendril axis for Adenia lobata and implemented this in their FEA. Fig. Fig 5.9 shows the strains in the dorsal and ventral domains along the axial direction (x). This figure shows clearly the asymmetry growth of tendril, expansion of dorsal domain and shrinkage of ventral domain. Providing the growth distribution between dorsal and ventral domains with those measured, would result in only bending of the tendril. They applied small rotation (0.05 radians per unit length) of the dorsal-ventral boundary interface about the tendril axis, arriving at helical shape in the FEA modeling (4) twining of vines Silk (1989) and her co-workers (1991;2005) studied twining of vines whereby a vine grows into helices around a support. This mechanism is different from tendril coiling because the vine does not coil freely in air but is continuously in contact with the support that it encircles. Silk and her colleagues used a non-orthogonal coordinate system to predict radial and circumferential growth using empirical data obtained from various cross sections. They proved that axial force (Ft) in climbing morning glory is balanced with normal force (pn) exerted on the surface of cylindrical support, where friction and shear force are assumed to be neglected. The balance equation between Ft and pn are given by

Ft + pn =0

(5.2)

where is the curvature of climbing morning glory. They found experimentally the order of Ft being 50 to 200 g, which is proportional to the height of climbing vine. Silk and Holbrook (2005) studied theoretically and experimentally the effects of the friction force which was neglected in their earlier work (1991). In order to account frictional force (pt), they used an well-known formula, pt= pn (5.3)

where is coefficient of friction. By using the governing equations of Costello (1978) developed for climbing rope, they obtained the axial force, Ft, given by Ft = A es (5.4)

where A is the tension at the top of the vine, is friction coefficient, is curvature, s is the arc length along the vine. They used Ipomoea purpurea vine in their experimental work, to demonstrate very large frictional force active between the above vine and support where the friction coefficient can be as large as 3.0. It can be concluded from this study that the gravitational force due to older vines located in lower part of the climbing vine can be supported by younger vine located at the top with only few turns. It is noted that the climbing vine is very weak under compression force, resulting in immediate detachment of the vine from the support (5)Unfolding and folding of leaves and flower pedals

Hydration and dehydration is a key function for all plants, adjusting environmental change that surrounds plants. Typical plant has many fibrous elements among which motor cells are located, accommodating water (ionic water, too) during uptaking water from roots, or in rainy season while in dryier environment, such motor cells dehydrate. Plant structure is fully supported mechanically with hydration, which is called as nastic structure.

Certain plants like the so-called Kentucky bluegrass Poa pratense (a European weed), many other grasses and Tradescantia species are able to roll their leaves in order to prevent excessive dehydration. Large, bulliform cells in the upper epidermis trigger this response. Since these cells have a very thin impregnating coat (cuticle) they (1) loose water more rapidly than others, (2) shrink the surface area of the upper leaf and (3) roll the leaf blade around the midvein; a measure which protects the upper surface from loosing further water to the atmosphere. The interesting side effect of this nastic movement is the rolling and unfolding of leaf area. A similar design is found in the appendages of horsetail spores. Fig. 5.10 shows how a Kentuckey blue grass leaf can fold by using the upper and lower motor cells where expansion of upper cells and shrinkage of the lower cells would result in bending of the leaf convex downward (or concave upward) , while the shrinkage of the upper cells and expansion of the lower cells can provide the opposite morphing, i.e. convex upward. It is noted that use of hinge motion to achieve folding and unfolding is very energy-efficient as the energy (or swelling and de-swelling of motor cells) is dissipated only at those hinges. One example of the use of fibrous motors in plants is the opening of seed containers like legume pods to release the seeds. Pod walls are made of two opposed fibrous hydration layers that have a 90 -degree angle to each other. Dehydration of the maturing pod walls leads to a torsional twist that rips the pod apart and with some luck may even spread the seeds in different directions (Figure 5.11). Although torsion was used for an advanced version of medieval catapults, called ballista, no human-made design is currently known to use such a motor. Botanists studied and correctly explained these dead, fibrous hydration motors as dimorph actuators consisting of two swelling layers [Jost 1933]. The movements were modeled with cellulose laminates in the form of joined paper strips having a different orientation of the cellulose fibrils (Figure 5.12). . The case of twisted shape of Fig. 5.11 may be explained by the mechanism of Fig. 5.12 (c). One should not forget that these paper models differ from natures designs in that they are glued together when they are flat and dehydrated and that they bend and twisted when hydrated. Of course, the opposite is the case in seed containers, which develop as straight structures when hydrated and green, while tension and torsion arise with the severe dehydration of the ripening seeds. This difference aside, these models are extremely useful to mimic and hence fully comprehend existing natural fibrous motors. They also elegantly demonstrate the countless possibilities for multifunctional biomimetic designs where fibers can serve both as structural elements and as motors. One can safely predict that the biomimetic use of fibrous hydration will not stop with the development of blotting paper. Bio-inspired design of fibers with larger relative volume increase and force development than the original cellulose fibers would be a useful step on the way.

Fig. 5.10. How a leaf of Kentucky bluegrass Poa pratense (a European weed) can fold to exhibit large morphing using the concept of expansion and shrinkage of motor cells, (a) zoom up of the upper part of the leaf with expanded motor cells, (b)-(e) sequence of expansion, entire leaf showing folded in morphology by kinking at several hinges.

Fig. 5.11 Dehydrated and twisted (upper picture) and smooth hydrated halves (lower picture) from the same seedpod of Lathyrus japonicus, a legume. The wall is made of two hydration layers with the fibers pointing in different directions (angle 90 degrees). When dehydrating, this torsion motor rips the pod apart and releases the seeds. Fig. 5.12 Shape change mechanism by hydration and dehydration of various laminate made of two different textured laminae, where blue colored textured sheet is hydrated to deform to curved shapes shown on right

Kishimoto et al (2006) examined various folding and unfolding patterns inherent in biological species, both plant leaves and flower booms and insect ecosion process. They categorized the folding/unfolding patterns into four types, depending on volume change, deployment only, and both deployment and storage: Type A: large volume change with deployment only Type B: not much volume change with deployment only Type C: large volume change with both deployment and storage Type D: not much volume change with both deployment and storage Examples of type A are bloom of dandelion and development of new leaves, while those of type B are bloom of morning glory and eclosion of insects, and those of type D are many : bloom of bindweed , open-close movement of sensitive and insectivorous plants, flap-stowage of beetles hind wings and flap-stowage of bats wings. Fig. 5.13 and Fig. 5.14 (a)-(c) are examples of type A development where flowers of dandelion(a), and sunflower(b) are composed of tubular and lligulate corolla which are used to deploy their folded pedals sequentially. Fig. 5. 14(d) is an example of type B development of plant flower bloom where morning glory opens only in the morning without reversing it. Fig. 1 2 3 4 5 6 7

7 2 3 4 5 6

5.14 is an example of type D development of plant where bindweed flower(e) can opens daytime while it can close the flower during nights, thus exhibiting reversible movement. The petals of both morning glory and bindweed flowers stored as helical wound configuration, shown in Fig. 5.14(f). Fig. 5.13 Sequential development of bipinnately compound leaves of alegument plant upper left to mid-left inserts, then fully opend leaves, in that order of sequential development (Kishimoto and Natori, 2006

(a) dandelion (f) helically-wound buds: (b) sunflower

(d) morning (c) poppy

(e) bindweed

Fig. 5.14 Examples of folding and unfolding of plant flower blooms, (a) dandelion, (b) sunflower, (c) poppy, (d) morning glory, (e) bindweed, (f) helically wound buds, morning glory (left), bindweed (right) (Kishimoto and Natori, 2006).