Finite Element Modeling of the Cyclic Wetting Mechanism in the Active Part of Wheat Awns
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Many plant tissues and organs are capable of moving due to changes in the humidity of the environment, such as the opening of the seed capsule of the ice plant and the opening of the pine cone. These are fascinating examples for the materials engineer, as these tissues are non-living and move solely through the differential swelling of anisotropic tissues and in principle may serve as examples for the bio-inspired design of artificial actuators. In this paper, we model the microstructure of the wild wheat awn (Triticum turgidum ssp. dicoccoides) by finite elements, especially focusing on the specific microscopic features of the active part of the awn. Based on earlier experimental findings, cell walls are modeled as multilayered cylindrical tubes with alternating cellulose fiber orientation in successive layers. It is shown that swelling upon hydration of this system leads to the formation of gaps between the layers, which could act as valves, thus enabling the entry of water into the cell wall. This supports the hypothesis that this plywood-like arrangement of cellulose fibrils enhances the effect of ambient humidity by accelerated water or vapor diffusion along the gaps. The finite element model shows that a certain distribution of axially and tangentially oriented fibers is necessary to generate sufficient tensile stresses within the cell wall to open nanometer-sized gaps between cell wall layers.
Awns and appendages attached to seeds play an important role in dispersing the seed from the mother plant to the germination site [1, 2, 3]. Throughout millennia nature evolved various wings, hairs, and hooks for controlling the route of dispersal to a safe site. The seed has to be designed in such a way as to optimize its ability to find proper conditions for germination. Therefore, seeds bearing active awns are more abundant in structured soils, i.e. soils containing pores and aggregates of different sizes . Seeds with hygroscopically active awns are able to propel themselves below the ground by coiling and uncoiling of their awns . The mechanism of hygroscopic movement is a consequence of wetting and drying of tissue, which results in different anisotropic swelling in different regions of the tissue. Humidity-driven movement is not only shown in wheat awns, it is also reported for various other species [5, 6, 7, 8, 9]. This movement is interesting for the (bio)materials engineer as the movement occurs without an active metabolism and as such is controlled solely by the architectural arrangement of the different swellable tissues.
In a previous study on the structure of the active part of the wheat awns, Elbaum et al.  speculated that the alternating orientation of cellulose in successive cell wall layers might enhance vapor (or water) diffusion if gaps opened between every second layer in the plywood structure. This somewhat counter intuitive mechanism, that swelling may lead to opening pores, was inspired by the idea that swelling of the layer in circumferential direction would be strongly reduced in the layers where the cellulose runs circumferentially, but not in layers where the cellulose runs axially. However, a quantitative estimate whether this effect is actually possible was not given in this experimental study.
The present work endeavors to study the proposed mechanism of humidity-driven movement and to find out whether, and under which conditions, an opening of gaps between cell wall layers is possible through swelling. The wheat awn is modeled using finite elements based on the structure reported in the earlier electron microscopic study . The focus is on a mechanical description of the wetting mechanism. The interface between the various cell wall layers is monitored depending on their relative thickness and their cellulose orientation. Finally the composite material properties of such a cell are used to model the motion of the entire awn, which is validated by comparison with experimental results of awn bending as a function of humidity.
2.1 Macroscopic Modeling
The aim of the macroscopic modeling is the determination of the expansion coefficient α due to moisture swelling. The expansion coefficient was obtained by means of finite element analysis by imposing the curvature of the finite element model to be equal to the curvature of the awn (Fig. 1a) measured experimentally under varying humidity conditions. The geometry of a representative cross-section of the awn for the finite element model came from scanning acoustical microscopy (SAM) images . Based on the gray level, three distinct regions were manually identified: the active part, the intermediate gap, and the resistance part (Fig. 1b). The elastic moduli were taken from a previous study on the wheat awn, where Elbaum et al. determined Open image in new window for the active part and Open image in new window for the resistance part by nano-indentation . The elastic modulus for the intermediate gap could not be measured directly, thus it was obtained by interpolation between the data of the resistance part and active part based on gray scale intensity of the SAM images. Local mean gray levels from SAM images were taken from all three regions, hence a linear interpolation provides Open image in new window for the intermediate gap region. The active part and the intermediate gap are composed of an alternating sequence of strongly anisotropic layers due to the direction of the fibrils. However, the ensemble properties are more or less isotropic for this very special arrangement. In the resistance part, on the other hand, all these fibrils are uniformly oriented in axial direction , thus for this part a special case of orthotropy—transversally isotropic material properties [20, 21]—were chosen.
A two-dimensional model of the cross-section was built of generalized plane strain elements (CPEG8) using the finite element software Abaqus . The swelling due to a humidity change of 10 % was mimicked by thermal expansion caused by a positive temperature step of ΔT = 1 K. The expansion was assumed isotropic in the active part, orthotropic in the resistance part and no expansion in the gap. Thus, the wheat awn deforms to a circular shape with constant curvature when the individual parts of the cross-section expand or contract.
2.2 Microscopic Modeling
The single cylindrical cell of the active part was modeled as a plywood architecture with the finite element software Abaqus . Based on scanning electron microscopy images , the inner radius ri was set to 5 μm and the outer radius ro to 7 μm. The cylindrical cell was assumed to be composed of ten concentric rings with radial thickness of 0.2 μm each. Each individual ring was set to contain two sublayers of material with axial and tangential cellulose orientation (Fig. 3c), and transversely isotropic material properties were assigned to both sublayers.
It should be noted that the finite element model of the full assembly provides not only the elastic moduli of the composite and the Poisson’s ratios of the total cylindrical cell depending on the composition of axially and tangentially oriented material and the in-plane elastic modulus Ep, but also the distribution of stresses inside the rings, including the radial stress components.
The macroscopic modeling of the wheat awn provides a thermal expansion coefficient α of 0.025 K−1 for a positive temperature step of ΔT = 1 K, which mimics swelling due to a humidity change of 10 %. The expansion coefficient α is used for microscopic modeling of the wheat awn. For the sake of clarity the following nomenclature is used: The fraction of axially oriented material of an individual ring can be varied from 0 to 100 %. The total fraction of axially oriented material ϕ describes the composition of the entire cell and can also be varied from 0 to 100 %.
However, one should keep in mind that for combinations with σR,max > 0 (Fig. 8a) at least one interface senses tensile stresses. For determining combinations that sense tensile stresses at each interface Fig. 8b shows the minimal value of the local maximum radial stress σR,max* (Fig. 7) at the interfaces as a function of Open image in new window. It is seen that the fraction of crossover is further shifted towards higher values of Open image in new window. Most interestingly, all four curves almost overlap, meaning that there is hardly any influence of the in-plane elastic modulus.
It should also be mentioned that the numerical values of the shear modulus Gt does not have any influence, neither on the composition of the cell nor on the elastic modulus EA, and variations of νp and νtp show only minor influence on the calculated parameters.
The microscopic finite element modeling of the active part provides valuable information on the possible mechanism of humidity-driven movement of the wheat awn. Although it is clear that differential swelling in different regions of a tissue leads to bending, one issue that is not often addressed is a question of kinetics and how water (vapor) can penetrate deep into the tissues. In a previous study on the wheat awn, Elbaum et al.  proposed that water transport into the active part of the awn is enhanced due to swelling itself, where tensile stresses at the interface between consecutive layers result in the formation of gaps, thus acting as valves, enabling a faster entry of water into the cell wall. The present study has investigated this model numerically and gives deeper insight into mechanisms of how the complex structure of the cell wall can lead to relatively fast motion or actuation. The selection of proper modeling parameters is done under two constraints: (a) All interfaces between two rings must open and (b) the total elastic modulus EA should be in the range of experimental data given in Ref. , see Sect. 1. As shown in Fig. 8b, only cells with volume fractions greater than about 65 % experience tensile rather than compressive stresses at each interface position, indicating that the gaps will open. This value is quite independent of Ep, however, the elastic modulus EA of the entire cell depends on Ep (Fig. 9a). Therefore, Ep = 5.0 kN mm−2 seems to be reasonable, which results in an overall elastic modulus EA of about 15 kN mm−2. This combination fulfills constraint (a), but is slightly larger than the experimental value Open image in new window for the active part determined by nano-indentation . However, it should be taken into account that nano-indentation provides an indentation modulus under the assumption of isotropic material behavior. Furthermore, when comparing experimental and calculated values, one should keep in mind possible effects of porosity and cleavage due to the penetration of a sharp-edged diamond pyramid in a rather soft fiber composite material. Moreover, one should consider that the elastic modulus depends on the water content which changes during movement. The mechanical response of the cell wall is also likely to depend on the environmental humidity [23, 24], although—to simplify the analysis in the current paper—a constant modulus was assumed.
5 Summary and Conclusions
In the present study the microstructure of the wild wheat awn (Triticum turgidum ssp. dicoccoides) is modeled by finite elements, especially focusing on the specific microscopic features of the active part. Depending on its composition the nano-scaled plywood architecture of the active part senses tensile stresses at the interfaces of individual rings of arranged fibrils. These stresses result in the formation of gaps, thus acting as valves, to allow faster entry of water into the cell wall. This is a somewhat counter-intuitive mechanism, where swelling of the plywood-like fibril arrangement of tissue leads to the formation of pores. It may therefore play a role in enhancing the rate at which changes in ambient humidity lead to swelling of the tissue, thus enabling the actuation of the awn under moderate humidity changes. The finite element model shows that only selected distributions of axially and tangentially oriented fibers are able to generate tensile stresses within the cell wall, which lead to the opening of nanometer-sized gaps. Constant distributions and linearly increasing distributions fail to generate the effect of constant opening over the entire cross-section of the cell. The overall elastic modulus is in reasonable agreement with experimental data from nano-indentation probing on wheat awns of the same species. The homogeneous properties of the tissue are also consistent with simple calculations of awn curvatures at the macroscopic scale with changes in humidity.
The present study has shown that a very special layering of the cells constituting the wheat awns is required to serve two purposes: (a) Provide sufficient stiffness to guarantee to work as an efficient actuator and (b) act as a humidity-driven valve to enable a sufficient amount of water intake. The presented concept involving experimental techniques in combination with numerical methods has proven successful for the quantification of experimentally inaccessible values in natural tissue.
The next logical step is to take the findings for the material behavior on the cell scale to the next hierarchical level of the entire wheat awn by again employing the finite element method in combination with the existing experimental evidence.
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