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H I G H L I G H T S G R A P H I C A L A B S T R A C T
a r t i c l e i n f o a b s t r a c t
Article history: Mycelium, the root structure of fungi, grows naturally as a biodegradable filamentous material. This unique ma-
Received 22 May 2018 terial has highly heterogeneous microstructure with pronounced spatial variability in density and exhibits
Received in revised form 22 September 2018 strongly non-linear mechanical behavior. In this work we explore the material response in compression, under
Accepted 27 September 2018
cyclic deformation, and develop an experimentally-validated multiscale model for its mechanical behavior. The
Available online 29 September 2018
deformation localizes in stochastically distributed sub-domains which eventually percolate to form macroscopic
Keywords:
bands of high density material. This is reflected in the stress-strain curve as strain softening. Cycling at fixed mac-
Mycelium roscopic strain leads to deformation history dependence similar to the Mullins effect. To capture this behavior, we
Fibrous materials use a two-scale model. At the micro-scale, a random fiber network is used, while at the macroscale the spatial
Mullins effect density fluctuations are captured using a stochastic continuum model. The density-dependent local constitutive
Cyclic loading behavior is defined by the microscale model. An empirical damage model is incorporated to account for the ex-
Constitutive modeling perimentally observed cyclic softening behavior of mycelium. The model is further validated by comparison with
a separate set of experimental results. The model can be used to explore the effect of mesoscale density fluctua-
tions on the overall mechanical behavior and to design mycelium-based products with desired mechanical
performance.
© 2018 Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
https://doi.org/10.1016/j.matdes.2018.09.046
0264-1275/© 2018 Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
550 M.R. Islam et al. / Materials and Design 160 (2018) 549–556
multiscale structure of mycelium to meet targeted global properties for ρs = 59 kg/m3. Unloading is performed immediately after loading,
specific applications. with the same strain rate (6.25 × 10−3 s−1). Mycelium softens cyclically,
i.e. a smaller stress is required in subsequent cycles to compress the ma-
2. Experimental details and results terial to the same strain level. However, once the strain exceeds the pre-
viously imposed maximum strain level, the loading curve converges to
The mycelium samples used in this work were provided by what would have been obtained from a monotonic compression of a vir-
Ecovative Design, LLC. The samples were prepared as follows: the gin sample (Fig. 2(b)). Part of these experimental results is used in
mycelium vegetative tissue is first inoculated in a filter patch bag Section 4 for model calibration, while the reminder of the data set is
with nutrition (calcium and carbohydrate) and water. After an initial used for validation.
growth phase (around 4 days), the substrate is ground into small
pieces to redistribute the growth evenly throughout the material. 3. Multiscale model for mycelium
This step also prevents preferential colonized growth of mycelium
in the vicinity of nutrition sites. Next, the material is packed into The multiscale model developed for mycelium is presented in this
rectangular molds (6″ × 6Δ″ × 1″) and additional nutrition is added section. At the microscale, we consider representative volume elements
to promote further growth. Mycelium is allowed to grow for around of the hyphae network and characterize their mechanical behavior as a
six additional days in the molds. As a last step, the samples were heat function of the effective network density. A hyperelastic model with
treated to stop hyphae growth. density-dependent parameters is fitted to these results. This is then
Microscopic imaging was carried out to characterize the microstruc- used as constitutive representation in a stochastic mesoscale continuum
ture of mycelium, using a VERSA 3D Dual Beam Scanning Electron Mi- model which accounts for density fluctuations on a scale much larger
croscope (SEM). SEM images were processed using ImageJ [24] to than that of the microscale network models. Hence, the continuum
evaluate various parameters such as the fiber diameter, segment length, model is heterogeneous in terms of all parameters of the hyperelastic
orientation and pore size. The mean hypha diameter, segment length description, which fluctuate spatially as a function of density. A damage
and pore size were 1.3 ± 0.66 μm, 6.5 ± 4.7 μm and 5.8 ± 4.1 μm, re- phenomenological model is introduced in the continuum representa-
spectively. Furthermore, it was observed that fibers (hyphae) have no tion in order to capture the Mullins effect (Fig. 2). An alternative to
preferential orientation. The mass density of the samples was also mea- this procedure would be to allow damage (e.g. fiber failure) to evolve
sured to evaluate the effect of density on mechanical properties. on the microscale in each representative volume element and import
Cuboid specimens of dimensions - 20 mm × 20 mm × 16 mm are cut that information in the upper scale continuum model. We avoid taking
for compression testing using a bandsaw. An EnduraTec Elf 3200 me- this route due to the limited data available at this time about the condi-
chanical testing machine (BOSE, Eden Prairie, MN) with displacement tions in which individual hyphae rupture or lose their load carrying
control was used for mechanical testing in ambient conditions (25°C capacity.
and ~50% relative humidity). A constant strain rate of 6.25 × 10−3 s−1 Fig. 3 shows this procedure schematically. The distribution of myce-
was used for all tests during both loading and unloading. Cyclic loading lium density on the mesoscale has been characterized in our previous
tests with no hold/relaxation between cycles were performed under work [1]. This distribution is mapped to a histogram of 10 specific den-
compression. sity values. Microscale network models, in which each fiber is explicitly
Fig. 2(a) illustrates the generic stress-strain response of mycelium represented, are constructed for each of these densities. The average re-
under compression. The test is performed with a sample of effective sponse to uniaxial compression of multiple replicas of a given density is
density ρs = 34 kg/m3. The stress-strain measures used in this work fitted with a hyperelastic model. Further, a stochastic continuum model
are the nominal stress (computed as the total applied force divided by is constructed and each mesoscale sub-domain is assigned the constitu-
the initial cross-sectional area of the sample), S, and the stretch ratio, tive model associated with the local density. We present next each of
λ. The response is linear elastic at small strains, with constant Young's these modeling steps.
modulus E = 1.3 MPa. Starting in the range 0.97 N λ N 0.92 the material
undergoes gradual softening due to strain localization and the initiation 3.1. Microscale model
of collapse band formation. A pronounced hysteretic response is ob-
served upon unloading. Samples of higher density (ρs = 59 kg/m3) ex- The random fiber network model used at the microscale is a Voronoi
hibit similar behavior (Fig. 2(a)), although the small strain modulus and network. A set of randomly distributed seed points are used to construct
the stress at the onset of localization are larger. Fig. 2(b) shows the the tessellation of the domain in which the network is defined, and fi-
stress-strain curves for five compressive loading-unloading cycles per- bers are placed along the edges of the resulting polyhedral cells to ob-
formed at two different maximum strain levels for a sample of density tain a random fiber network. In this algorithm, the network density is
Fig. 2. Experimental stress-strain response of mycelium under compression- (a) single compression cycle for mycelium of densities ρs = 34 kg/m3 and ρs = 59 kg/m3, and (b) five
successive compression cycles performed on same sample at two different maximum stretches (λ = 0.9 and λ = 0.79 respectively) for a mycelium of density ρs = 59 kg/m3.
552 M.R. Islam et al. / Materials and Design 160 (2018) 549–556
controlled by the density of seed points. We adjust the distribution of The fiber segment length in the model (lc) varies from 4 to 8 μm (ex-
seed points so as to mimic closely the pore size distribution of mycelium perimental, lc ≈ 6.5 μm) depending on the network density (ρm). All fil-
observed microscopically. Fig. 4 compares pore size probability distribu- aments in the network model are assumed to have identical cross-
tion functions of experimental samples and microscale model. It is section with outer diameter d0=1.3 μm (experimental, do ≈ 1.3 μm)
noted that the experimental pore size distribution corresponds to the and wall thickness (tw = 100 nm [5]). The base material of the filament
two dimensional (2D) projection of mycelium network as observed in is chitin which has density, ρf = 1430 kg/m3. We used an elastic-plastic
SEM images of finite (and known) depth of focus. As such, the pore material model based on literature data for chitin nanofilament net-
size of the microscale model was also evaluated for thin sections of works (the structural constituent of the hypha wall) following ref. [8],
same thickness to ensure proper comparison with experimental values. with the elastic modulus, Poisson ratio and yield strength as 2.5 GPa,
The network mass density, ρm, is defined as: 0.3 and 45 MPa respectively. Beyond the yield point, the material behav-
ior is assumed to follow linear strain hardening with a stiffness ratio of
X
N 0.02 between elastic and plastic regime. The generated network is
1
ρm ¼ 3
ρf A li ð1Þ discretized using shear-deformable Timoshenko beams. The minimum
L i¼1 element aspect ratio is 5.
Fiber to fiber contact is incorporated using surface based contact
where L is the size of the 3D domain, ρf is the density of a hypha wall, A constraints using the general contact algorithm in Abaqus [25]. The con-
is the cross-section area of a typical tubular hypha, N is the number of tact behavior normal to fiber surfaces is implemented with zero pene-
filaments in the network and li is the length of the ith filament. tration condition (‘hard’ contact algorithm in Abaqus). The relative
sliding between fibers is represented as Coulomb friction with a coeffi-
cient of friction, μf = 0.3, as suggested in refs. [26, 27]. The hypha net-
work is deformed in uniaxial compression by introducing two rigid
surfaces at the top and bottom boundaries while imposing equal and
opposite displacement boundary conditions on these surfaces. The lat-
eral faces of the model are kept traction free and all other degrees of
freedom are free. Finite element simulations are performed using the
general purpose finite element solver Abaqus/Explicit (version 6.13-1)
[25].
It has been discussed in the literature that fiber networks exhibit
strong size effects [28] depending on the fiber elastic properties. Specifi-
cally, for fibers which are rather rigid in bending, the scale of homogene-
ity (i.e. scale at which the response becomes independent of model size)
is equal to few fiber segment lengths (lc). If fibers are soft in bending,
which is the case for mycelium, the scale of homogeneity increases grad-
ually as the bending stiffness of filaments decreases. In the current work,
a large model size (L≥12lc) is selected to exclude the network size effect.
The compressive stress-strain responses of samples with four
representative network densities are illustrated in Fig. 5. At small
Fig. 4. Comparison of pore size distribution functions for experimental samples and compressive strains (λ ≤ 0.95), the curves show a linear elastic re-
microscale model. sponse where deformation is largely dominated by fiber bending.
M.R. Islam et al. / Materials and Design 160 (2018) 549–556 553
Fig. 6. Deformed configurations of a micro-scale network model (ρm = 16.9 kg/m3) with von Mises stress contours corresponding to applied stretch ratio values of (a) λ = 0.99, (b) λ =
0.95 and (c) λ = 0.85.
554 M.R. Islam et al. / Materials and Design 160 (2018) 549–556
∂W 2 X N
μ i αi
SL ¼ ¼ λL − J α i βi ð4Þ
∂λL λ α
L i¼1 i
where the coefficients (μi, αi and βi) need to be determined by fitting the
stress-strain curves obtained from the microscale model. Material coeffi-
cients are determined by a nonlinear least-squares fit methods based on
Marquard-Levenberg algorithm [30] by minimizing relative error in
stress. A fit of expression (4) with three terms in the sum, N = 3, provides
a good approximation of the stress-strain response of various network
densities with relative error b5% for all densities. Fig. 4 shows the fits ob-
Fig. 7. Representative mesoscale density distribution for a sample of average density ρs =
34 kg/m3. The black line represents the actual distribution and the vertical bars indicate
tained using Eq. (4) for four representative network densities. To repre-
the corresponding approximation. sent the entire density distribution as shown in Fig. 7, ten similar
network densities (corresponding to the vertical bars in Fig. 7) are consid-
ered and the resulting material parameters are shown in Table A1. The
The mechanical behavior of models of all ten densities defining the dis-
hyperelastic formulation discussed here is implemented using the
crete distribution in Fig. 7 is evaluated using microscale models.
HYPERFOAM material model available in the commercial finite element
package Abaqus.
3.3. Constitutive representation of microscale model behavior
1.01,m = 0.005, β=0.1) are used. The multiscale model is able to pre-
dict the highly non-linear behavior of mycelium accurately, except for
the residual strain. In the absence of accurate elastic-plastic properties
for individual hyphae, the residual strain or permanent set cannot be
captured. Further, the predicted unloading and reloading curves are
identical, whereas the respective paths are slightly different in exper-
iment. This is most likely due to viscoelastic recovery of mycelium
after unloading. Since no viscoelastic component is included in the
model, the model cannot account for such recovery as seen in exper-
iment. This difference is considered unimportant for the purpose of
the developed model.
5. Conclusion
Appendix A
Hyperelastic model parameters, as defined by Eq. (3), are summarized for ten network densities in Table A1. These parameter sets are used to
define the constitutive behavior of each sub-domain of the continuum mesoscale model according to the density distribution of Eq. (2). The values
of μi are in MPa, while αi and βi are dimensionless.
Table A1
Summary of hyperelastic model parameters for ten different network densities.1,2
ρm (kg/m3) μ1 α1 μ2 α2 μ3 α3 β
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