research article the impact behaviour of silk...

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INTRODUCTIONFundamental research on silkworms tends to focus on increasingour understanding of the material and biochemical properties of theirsilk fibres (Porter and Vollrath, 2009). More applied silkwormresearch tends to focus on methods to best extract the silk from thecocoons of the domesticated silkworm Bombyx mori or from wildcocoons (Gheysens et al., 2011; Kundu et al., 2012), or indeed onturning those silks into useful textiles or other products. In contrast,the structure of the cocoon itself has largely been ignored, althoughrecent research shows that cocoons can be considered as hierarchicalcomposites composed of silk fibres and sericin bonds, whichconfers a number of unique properties to the cocoon (Chen et al.,2012a; Chen et al., 2012b; Chen et al., 2012c).

Cocoon properties may be of great interest in the biomimeticdevelopment of flexible, damage-resistant, lightweight composites.For example, many silkworms have silk cocoons with a laminatedstructure (see examples of B. mori, Antheraea pernyi andOpodiphthera eucalypti cocoons in Fig.1). Although the cocoons ofeach species have their own individual features, they all have a multi-layer structure with fewer fibres connecting layers than aligned in theindividual layers. The interlayer bonding is much weaker than theintralayer bonding. The porosity of the cocoon layers decreases frominner to outer layers (Chen et al., 2012b). This structure shares amorphological similarity with conventional laminated composites, inwhich the fibre prepregs are stacked and bonded by resin matrixbetween the layers. Furthermore, cocoon structures (and thereforecocoon properties) are optimised for combinations of differentbiological functions across the species range against a range ofdifferent threats and environmental challenges. Importantly, theanimal uses a very limited number of material components, usuallyonly silk fibre and sericin. Some cocoons also have additional features,such as extra calcium oxalate crystals on the cocoon surface in A.pernyi cocoons or the incorporation of hairs and spines (Chen et al.,2012a). In addition, some cocoons might display rather large holes,

e.g. the cocoon walls of O. eucalypti (Fig.1, insets), which will berelevant for discussions later in this paper. As the predominantnonwoven structures in a number of silk cocoons have a similarmicrostructure to other stochastic fibrous materials (such as paper,nonwoven textiles and electrospun polymer mats), the bioengineeringdesign principles evolved in silkworm cocoons make them excellentnatural prototypes and models for the study of structural composites(Chen et al., 2010b).

However, in order to fully utilise the biomimetic potential of thecocoons, we need to better understand the natural (native)relationships between their structure and function, which have been‘optimised’ over millions of years of evolution. All cocoons appearto be multifunctional and possible functions include camouflage(Danks, 2004), thermoregulation (Lyon and Cartar, 1996) andhumidity control (Blossman-Myer and Burggren, 2010). However,despite surprisingly little experimental data, the main function ofall cocoons is likely to be the mechanical protection of the enclosedpupae from predators (Scarbrough et al., 1972; Waldbauer, 1967),similar to the protection against both general and specialisedpredators provided by the silken cocoons enclosing spider egg sacs(Hieber, 1992). Clearly, the exact way in which the cocoon offersprotection depends on the nature of its main predators.

There seem to be three main strategies that predators employ topenetrate a cocoon. (1) Penetration of the cocoon wall by drilling.This strategy is employed by ichneumonid wasps, which lay eggsin or on the pupae that develop into larvae that parasitise the pupae(Marsh, 1937). (2) Creating a hole in the cocoon by removing silkby tearing and shearing movements. This strategy is employed bymice and other small mammals (Scarbrough et al., 1972). (3)Creating a hole in the cocoon by breaking individual fibres and thecocoon wall by making an indentation in the cocoon. This strategyis employed by birds, which either use their beaks to compress thecocoon walls or, like woodpeckers, attempt to directly hack holesin the cocoons (Waldbauer, 1967).

SUMMARYSilk cocoons, constructed by silkmoths (Lepidoptera), are protective structural composites. Some cocoons appear to haveevolved towards structural and material optimisation in order to sustain impact strikes from predators and hinder parasiteingress. This study investigates the protective properties of silk cocoons with different morphologies by evaluating their impactresistance and damage tolerance. Finite element analysis was used to analyse empirical observations of the quasi-static impactresponse of the silk cocoons, and to evaluate the separate benefits of the structures and materials through the deformation anddamage mechanism. We use design principles from composite engineering in order to understand the structure–property–function relationship of silkworm cocoons. Understanding the highly evolved survival strategies of the organisms building naturalcocoons will hopefully lead to inspiration that in turn could lead to improved composite design.

Key words: silk, composite, silk moth, finite element analysis, deformation.

Received 6 November 2012; Accepted 1 March 2013

The Journal of Experimental Biology 216, 2648-2657© 2013. Published by The Company of Biologists Ltddoi:10.1242/jeb.082545

RESEARCH ARTICLEThe impact behaviour of silk cocoons

Fujia Chen, Thomas Hesselberg, David Porter* and Fritz VollrathDepartment of Zoology, University of Oxford, South Park Road, Oxford OX1 3PS, UK

*Author for correspondence ([email protected])

THE JOURNAL OF EXPERIMENTAL BIOLOGY

2649The impact behaviour of silk cocoons

All three strategies involve impact strikes on the outer cocoonwall. Defences against these strategies would include the abilityto either resist the impact with little damage, or to tolerate thedamage by maintaining the structure. As a cocoon acts as aprotective structure for the pupa, it should evolve to haveengineering benefits such as impact resistance and damagetolerance by combining the structure and material properties. Inthe present study, we focus on how cocoons might have evolvedcounter-measures against the third predator strategy (creating ahole) using an engineering approach. We describe how cocoonsdeform during quasi-static localised indentation, and we analysethese observations with the help of a simple finite element analysis(FEA) model designed to simulate this behaviour and highlightkey features of the cocoon deformation and failure mechanisms.This combination of experiment and simulation providesimportant insights into the defensive strategy of silkworms,whose cocoons have structural and materials properties that appearoptimised for achieving a high impact resistance and damagetolerance.

Importantly, FEA has previously been extremely useful to betterunderstand the form and function relationships of spider webs(Hesselberg and Vollrath, 2012; Ko and Jovicic, 2004; Lin et al.,1995). Indeed, one might go as far as to say that without thisengineering approach such insights would have been impossible(Vollrath, 2000). After all, FEA requires detailed statements of themechanical properties of all component parts, as well as (for truthing)solid empirical data on the behaviour of the composite itself in

addition to a good understanding of the biological and abiotic(environmental) frame parameter under which the structure operatesand for which it has evolved. While spider’s webs are lightweight,airborne net structures that fish for aerial prey, silkworm cocoonsare complex, rather solid composite constructions that house adelicate inhabitant. Yet in both cases FEA provides key insightsinto structure–property–function relationships.

MATERIALS AND METHODSStudy animals

The cocoons used in this study were obtained through commercialtrade. Bombyx mori (Linnaeus 1758) (family Bombycidae) cocoonswere acquired from ICIPE (Nairobi, Kenya). Antheraea pernyi(Guérin-Méneville 1855) and Opodiphthera eucalypti (Scott 1864)(both family Saturniidae) cocoons from Korea and Australia werepurchased through Worldwide Butterflies (Sherbourne, UK). All thecocoons were spun in free space without attaching cocoon walls tothe substrates. In order to keep the intact structure of the cocoons,samples were frozen at −5°C for 24h to kill the pupae inside beforethe emerging adults tunnelled through the cocoon and broke thestructure.

The cocoons were then cut into two halves to release the pupaewithout contaminating the cocoon materials. This was done to isolatethe effects of the material properties of the cocoon from anypotentially confounding effects of the pupae. The geometry of thecocoons replicated in the models was measured using a MitutoyoIP65 micrometer (Andover, UK).

Inner layer

1 cm 200 µm 200 µm 200 µm

Outer layer Layers

Fig.1. The morphologies of the layer structure of the cocoons of Bombyx mori (first row), Antheraea pernyi (second row) and Opodiphthera eucalypti (thirdrow). The first column shows photographs of the cocoon morphology, while SEM photographs of the outer and inner layer structure are shown in columnstwo and three. Porosity is found to decrease from inner to outer layers. Inset of A. pernyi cocoon: calcium oxalate crystals found on outer cocoon surface.Inset of O. eucalypti cocoon: fabricated hole structure found on cocoon surface. The final column shows SEM photographs of cross-sections of layerstructures of the cocoons.


2650 The Journal of Experimental Biology 216 (14)

Tensile experimentsThe tensile strength and modulus of the cocoon materials weremeasured with a crosshead speed of 2mmmin–1 in an Instron 5542(Instron, High Wycombe, UK). Test specimens were individuallycut from the cocoon wall with a sharp blade into dogbone-shapedsamples having a width of 5mm and a length of 15mm.Opodiphthera eucalypti cocoon samples were cut to avoid thefabricated holes on the cocoon wall. The gauge length of samplesin the tensile test was 5mm. The samples were aligned using arectangular guiding tool from the Instron instrument. Three samplesof each cocoon species were tested.

Indentation experimentsEach half of the cocoon samples was affixed (with superglue) atits cut edge onto a glass slide. The central points of the sampleswere measured and marked to be the compressive points.Opodiphthera eucalypti cocoon samples were cut to avoid thefabricated holes on the cocoon wall. The tests were carried out ina Zwick/Roell Z0.5 test machine (Ulm, Germany) underdisplacement control at a loading rate of 5mmmin–1. Theindentation load was applied through a steel rod with a round flatend (1.56mm diameter). The unloading was performed at a speedof 15mmmin–1. The samples flexed back but did not recovercompletely their un-deformed shape. The cocoon samples respondto form a concave area under the indentor. The shapes of cocoonscrushed during the indentation until the indentor reached the slideunderneath the sample were recorded.

Finite element modelFor the finite element modelling, we performed simulations of thequasi-static response of cocoons in order to understand the failuremodes caused by the local indentation described above. In previouswork we have shown that models based upon open-cell foamstructures describe the mechanical properties of silk cocoons (Chenet al., 2010b). Here we therefore use the finite element softwareABAQUS/CAE 6.8-4 (Dassault Systèmes, Vélizy-Villacoublay,France) to simulate the indentation behaviour of the cocoons in thisstudy, as previous work on simulating deformation in foam materialswas carried out using ABAQUS (Gilchrist and Mills, 2001; Li etal., 2000; Rizov et al., 2005).

An axisymmetrical idealisation was used for the geometry of thethree cocoon types. The mesh consisted of 94,400 finite elementswith two elements through the wall thickness (Fig.2). All degreesof freedom at the boundary of the specimen bottom were constrained,simulating a rigid fixed support. The indenter was modelled as aforce applied to a circular area on the upper surface of the cocoonin the program. All degrees of freedom of the indenter wereconstrained, except in the vertical direction.

RESULTSMaterial properties

Four types of silk cocoon were categorised according to their differentmechanical behaviours in a previous paper (Chen et al., 2012c): (1)‘lattice’ cocoons, with a loose scaffold structure, (2) ‘weak’ cocoons,with high porosity and weak interlayer bonding properties, (3)‘brittle’ cocoons, with low porosity, strong interlayer bonding andbrittle mechanical properties, and (4) ‘tough’ cocoons, with mediumporosity, interlayer bonding and tough mechanical properties. Herea typical cocoon was selected from each of the latter (2–4) threenonwoven cocoon categories in order to investigate their failuremechanisms. Bombyx mori cocoons have high porosity: the inter-fibrebonding breaks gradually with the increasing strain, leading to areducing modulus; the stress drops when the breakage of the structurereaches a percolation point, then the unbonded fibres unravel fromthe structure. Opodiphthera eucalypti cocoons, in comparison, havelow porosity and strong bonding between the fibres; a crack startsfrom the sericin binding matrix and propagates to the fibres; thestructure fails when the fibres break perpendicular to the tensile load,which is seen in the stress–strain curves as a dramatic drop of thestress (Fig.3). The A. pernyi cocoon has a medium porosity comparedwith the other two cocoons: it exhibits yielding below 20% strain,which absorbs the energy to produce a tough behaviour; the structurefails when more than half of the sericin binder matrix fragments; thefibres then pull out from the structure, which is seen as a stress tailin stress–strain curves.

We have previously shown that B. mori cocoons have a gradedlayer structure, where the innermost layer exhibits a strong but brittlebehaviour, while the outermost layer is usually the weakest layer(Chen et al., 2012b). This is due to the gradual increase of porosityand the decrease of the number of sericin binding points from theinnermost to the outermost layer. In this paper, a similar behaviourof A. pernyi cocoons is shown. The fibres break at the innermostlayer and disentangle in the outer layers. The graded morphology

Fig.2. The finite element analysis geometry model of half of a Bombyx moricocoon.

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Fig.3. The mechanical tensile behaviour and breaking mechanism ofcutouts of three typical nonwoven cocoons [for a large set of datahighlighting intraspecific variance, see Chen et al. (Chen et al., 2012c)].The insets show SEM photographs of the microstructural failure in thecutouts, with scale bar lengths of 0.5 mm for the top inset and 1.0 mm forthe two lower insets.



observed from the scanning electron micrographs in Fig.1 confirmsthe same mechanism as in the B. mori cocoons. Opodiphtheraeucalypti cocoons show a clean failure in the structure because oftheir low porosity, even in the outermost layer. However, the sericinbonds still start at the outermost layer and then propagate into theinner layers. We conclude that all three nonwoven cocoons testedhave a graded layer structures in which the mechanical strengthincreases from the outer to the inner layers.

Indentation experimentsTypical load–indentation behaviour and load–deflection curves forthe three cocoon types are shown in Figs4 and 5, respectively, withdeflection given as a fraction of the maximum strain until theindenter reached the glass plate and with load shown on the samescale for all the cocoons for comparison. The B. mori cocoonload–deflection curve shows a gradual decrease in stiffness beforethe stress reaches a plateau level with the emission of a noise(cracking sounds) (Fig.5), which are attributed to the extensivesericin breakage and delamination in the cocoon sample (Fig.6).The damage process is also reflected in the fluctuations in the loadresponse. Bombyx mori cocoons have the largest delamination areasamong the three cocoons and nearly all the interconnectivitybetween layers in the concave area is broken (Fig.6). The B. moriresponse is relatively consistent, and the five curves shown in Fig.5reflect the full range of responses, which are attributed here torelatively consistent size and shape of the cultivated cocoons,compared with the other wild cocoons.

The indentation behaviour of A. pernyi and O. eucalypti cocoonshas much more variation that that of B. mori cocoons (Fig.5). Thisis attributed to their inconsistent geometrical shapes and sizes arisingfrom them being spun in the wild, in contrast to the cultivated B.mori cocoons. Generally, both cocoons also have nonlinearbehaviour (Fig.5). The onset of inter-laminar delamination of thecocoons is again associated with the gradual decrease of thestiffness in the load–deflection curves. After that, the cocoons areextensively damaged, which can be seen from the pronouncedfluctuations in the load–deflection curves. Antheraea pernyi cocoonshave extensive sericin breakage and some delamination after

indentation tests. In contrast, general fibre and layer breakages arefound in O. eucalypti cocoons with less damage propagation andlarge-scale failure found close to the indentation area. Theindentation terminates with a clear penetration of fibre and layerbreakage in O. eucalypti cocoons (Fig.6).

One of each of the three experimental tests from both A. pernyiand O. eucalypti cocoons were selected for finite element modelling.Their specific geometrical data were collected for FEA calculations,and their experimental curves were used for comparison with thesimulation results.

FEA: constitutive model for materialsAn open-cell foam model was used to describe the tensile propertiesof cocoon walls based upon the similarity of cocoon morphologywith that of cellular materials (Chen et al., 2010b). The compressionbehaviour of cocoon shells can be described by a comparable open-cell foam model using the appropriate deformation geometry of thecell walls under compression (Chen et al., 2010b). To complicatethings further, the inter-laminar debonding contributes to themechanical properties of cocoon walls and thereby must be included

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Fig.4. Photographs of the quasi-static impact tests of three cocoonsshowing their deformation: (A) Bombyx mori; (B) Opodiphthera eucalypti;(C) Antheraea pernyi.

Fig.5. Load–deflection curves of impact tests of cocoon samples from (A)Bombyx mori, (B) Antheraea pernyi and (C) Opodiphthera eucalypti. Thesolid lines are specific cocoon measurements, and the dashed lines for A. pernyi show the higher and lower limits for the wide range of cocoongeometries.


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in the deformation and failure mechanisms, particularly where shear(hence bending) deformation is involved through the wall thickness(Chen et al., 2010b).

The plastic compressibility of foams results from the collapse ofthe cell walls due to buckling, breaking or yielding (Rizov et al.,2005). A localised progressive crushing mechanism for foams isdescribed by Li et al. (Li et al., 2000), where the plastic deformationis usually localised into the weakest cell layer and the strain increasesrapidly in this layer and then triggers the next layer to crush. Thisprocess is very similar to the bond fission and delaminationprocesses of cocoon damage. Because such foam compressionsimulations have previously been calculated and modelled usingABAQUS (Li et al., 2000), we expected to find an appropriateconstitutive model in the software that would implicitly includedamage occurring in the plasticity of the irreversible process ofcocoon indentation

A number of different constitutive plasticity models in ABAQUSwere tested for their ability to reproduce the experimental tensilestress–strain relationships. The (generally hyperelastic) constitutivemodels were selected for testing by experienced ABAQUS usersand literature examples. The selection was made by a combinationof best visual fit to material test data, and also computationalefficiency of simulations, as some models gave very slowconvergence. The most appropriate deformation plasticity modelavailable in our version of ABAQUS is the Ramberg–Osgoodplasticity model, which describes the strain response to an appliedstress through a yield process:

where σ is the stress, ε is the strain, E is the Young’s modulus, αis the yield offset parameter, σ0 is the yield stress, n is the hardeningexponent and α(σ0/E) is the yield offset strain.

All these parameters come from fitting experimental tensilestress–strain data, as shown in Fig.7 and Table1. As this is adeformation plasticity model, which is actually an elastic modelmodified to include yielding behaviour, it does not include therapid drop in stress at the percolation damage point in eachexperimental curve. This model is chosen to simply suggest themechanism for initiation of the cocoon collapse in areas wherethe modulus reduces significantly under load without includingthe damage propagation.

ε = σ + σ σσ

⎛⎝⎜

⎞⎠⎟E

aE

, (1)n

0

0

The Journal of Experimental Biology 216 (14)

FEA simulation results for shape changes of cocoon samplesFig.8 shows the evolution of the stress on the outer surface of thecocoons at three increasing indentation loads and also the stressthrough the thickness of the cocoon wall in a cross-section throughthe long axis, with red being the highest stress and blue the lowest.Three different sets of indentation loads were selected to show thecocoon deformations evolved from elastic, initial yield and plasticstages. The cocoon sample has a highly deformed zone, which islocalised around the indenter, while other parts of the cocoonundergo far less deformation. The highest tensile stress isconcentrated on the outer surface of the minor axis of the cocoon.

Indentation: comparison between experiments andsimulations

Most of our experiments and simulations of cocoon indentationwere carried out on B. mori cocoons and hence we concentrate

Fig.6. SEM pictures of cocoonmicrostructures showing damagemechanisms after penetration. Above:delamination. Bottom: breakage of thefibre and sericin. (A)Bombyx mori.(B)Antheraea pernyi. (C)Opodiphtheraeucalypti. Bombyx mori and A. pernyicocoons show sericin breakage amongthe fibres, while O. eucalypti cocoonhas fibre breakage and penetration inthe structure.

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Fig.7. Stress–strain curves for cocoon samples tested and simulated inuniaxial tension from the deformation plasticity model.



Concave stress

Applied load: 16.73 NMax. strain: 3.3%



Applied load: 29.18 NMax. strain: 4%

Applied load: 11.99 NMax. strain: 4%





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Fig.8. Evolution of cocoon indentations deduced from the numerical modelling. Three applied loads were selected from the load–deflection curves of eachcocoon. The stress level in the concave and the strain level in the cross-section of the cocoon minor axis are shown. The simulation calculates themaximum strain in the cocoon structure.

Table1. Parameters of the plasticity constitutive model used in the finite element analysis simulations

Thickness (mm) Young’s modulus (MPa) Poisson’s ratio Yield stress (MPa) Exponent Yield offset

Bombyx mori 0.61 500 0.1 43.524 11.579 0.2842Antheraea pernyi 0.43 730 0.1 77.461 4.8584 0.377Opodiphthera eucalypti 0.25 850 0.1 127.97 10.225 0.3985


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on these results in order to deduce general trends. The measuredand simulated static indentation responses of B. mori cocoonsamples are shown in Fig.9. Simulation can generally reproducethe concave shapes of the cocoons seen in experiments at smalldeflections. However, with high deflection, the shape deformationin the simulations tends to concentrate too much around theindenter. In the experiments, the indenter gives a broader craterarea of deformation of the cocoon, thereby giving a lower craterheight.

Different constitutive models for the cocoon wall material weretried, including hyper-elastic models and even simple rubber models,on the B. mori cocoon FEA (data not shown). The general concaveshape of the cocoon indentation crater can be reproduced almostuniversally, but clearly with poor predictions of the load, whichsuggests that the general cocoon response behaviour is generic andindependent of the material properties. The geometric shape of thecocoon appears to have more effect on its indentation behaviour.

The measured and the simulated static indentation load responseswith the same cocoon geometries of B. mori are given in Fig.10,but using different sets of material parameters in the constitutivemodel. For the B. mori material data shown in Fig.10, the initialelastic slope of the simulated load–indentation curve is in goodagreement with the experimental results. However, at largedeflections the numerical simulations do not reproduce the overall‘yielding’ profile; the finite element modelling and the experimentalstudy diverge at approximately 20% deflection. Using theconstitutive model parameters for A. pernyi simply shifts thesimulation to higher loads due to the higher modulus. The


simulations of A. pernyi and O. eucalypti cocoon also reproducethe experimental results before the materials yield (Fig.11).

Fig.12 shows the distribution of the stress and strain thatcorresponds to the divergent point between the experimental resultsand the numerical simulation at approximately 20% B. mori cocoondeflection. The inner surface of the cocoon centre, which is localizedunder the indenter, has a highly deformed zone. The outer surfaceof the edge of the bending concave crater (circled) also developsthe highest general strain, which is locally above 4% strain due tothe tensile force distribution on the outer surface. This happens tobe the breaking strain of sericin (Fig.13) (Chen et al., 2010a).

The experimental observations suggest that this divergence betweensimulation and experiments indicates that the model cannot predictthe initiation of damage. In the cocoon, the initiation of the damage

Fig.9. Comparison of cocoon shapes betweenexperiments (above) and numerical simulations usingthe Ramberg–Osgood plasticity model (bottom). PanelsA–F show the development of the indentation concavewith increasing penetration.

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Fig.10. Comparison between load–deflection curves predicted by the finiteelement modelling (FEM) of different materials data input and from theimpact test on Bombyx mori cocoons. The circle highlights the diversion ofthe simulation and experimental results.

Fig.11. Comparison between stress–strain curves deduced from the finiteelement modelling and from the impact test for (A) Antheraea pernyi and(B) Opodiphthera eucalypti. The solid lines are experimental results thathave the same cocoon geometry as the model simulation, and the dashedlines are from other experiments of other cocoon geometries of the samespecies.



is the sericin breakage between the layers at the surface of the cocoon(Chen et al., 2010b). To explore this hypothesis, a B. mori sericinmodel was used in the indentation simulations. This model uses thesericin properties (Fig.13) and has the same stress–strain behaviouras B. mori cocoon material at low strain, but is constrained to yieldat 4% strain as for pure sericin (Fig.14). The intention was to examinewhether the local stress–strain response in the cocoon walls isdominated by sericin failure.

The sericin model can reproduce the experimental results at lowstrain shown in Fig.10, but the simulations would not converge abovea deflection of approximately 30%, which corresponds to a local strainat the outer surface of 4.5% and suggests failure of the sericin bindermaterial. This suggests that the point at which the simulations divergefrom the experiments is the initiation of the sericin breakage, whichis an irreversible damage in the cocoon structure that is not includedin the constitutive model. The point at which the sericin damagethreshold is reached should correspond to delamination of the cocoonand loss of connectivity in the planar interfibre bonding. At this pointthe composite material cannot sustain load, and the stress is transferredin a cascade to ever-deeper layers of the cocoon structure to propagatethe damage process through the full cocoon thickness, resulting inno more increase in the indenter load.

DISCUSSIONThe present study demonstrates that the silk moth cocoons showadaptations to resist standardised impact forces in the laboratory,

which suggests that cocoons could similarly be adapted to resistimpact forces generated by predators in the wild. The moth larvaeappear to employ a number of different strategies while buildingthe cocoons to increase their impact resistance and damage toleranceby combining their macro-structural shape, micro-layer structureand properties, and component materials. These hierarchicalorganisation and complicated engineering properties are inherent totheir design.

The B. mori cocoon is the most comprehensively studied type ofsilkworm cocoon in terms of structure and properties (Chen et al.,2012a). So it was used as the main example for analysing impactresistance and damage tolerance in cocoons. Our experimental andmodelling results both suggest that the silk cocoon may indeed bemechanically suited to withstand impact force. This is because of:(1) the ellipsoid shape of the cocoon, (2) the component materialproperties, (3) the laminated layer structure and (4) the graded layerproperties. Both the experiments and models show that loading thecocoon centre leads to a concave shape of deformation (Fig.9). Theellipsoid shape of the cocoon allows a certain level of elasticdeformation of the cocoon wall, and then restricts the deformationto avoid propagation of damage. In contrast, FEA simulationssuggest the deformation process and the deformed shape of thecocoon is relatively independent of its material properties (Fig.10).The damage is localized at the edge of the bending concave craterwithout excessive propagation of breakage. The material propertiesaffect only the elastic deformation rather than the damage area. This

Fig.12. Distribution of the stress and straincorresponding to the maximum indentation loadobtained from Bombyx mori cocoon in the finiteelement analysis. Above: stress in the cocoon concave.Below: strain in the cocoon cross-section. The largestdeformation is found at the innermost side of thecocoon under the impacter. The circle highlights thelarge deformation found at the edge of the cocoonconcave crater.


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feature helps to keep an intact cocoon structure, and provides a goodsupport to avoid massive deformation onto the pupa inside thecocoon by using limited materials.

In biological structures, the component material properties usuallyclosely link with the structure, as they evolve together to fit thebiological functions (Vincent, 2012; Meyers et al., 2008; Vogel,2003). This is also found in the B. mori cocoon in its relationshipbetween component properties and laminated structure (Chen et al.,2012b). The damage of the B. mori cocoon can be described by twocoupled failure modes: sericin bonds cracking and delamination.FEA shows that sericin cracking is the first fracture event aroundthe edge of the cocoon concave during an impact process due to itsrelatively low breaking strain compared with the fibres (Figs12,13). After extensive breakage of sericin bonds, delamination (thecrack in the sericin bonds between layers) develops, inducingseparation of the individual layers, which has been observed fromour experimental results (Fig.6). This sacrificial breakage allowseach fibre layer to deform semi-independently rather thantransferring the stress through the layers. In contrast, silk fibres witha high strain to failure adapt within this individual layer structure(Fig.13). The fibre layer can have an elastic deformation withoutdamaging the fibre to maintain its own mechanical properties in thefibre directions. This gives maximum energy absorption andincreases the toughness of the structure.

The graded layer structure is another feature that may haveevolved to improve the impact resistance of the cocoon. This is basedon the FEA simulation results that the largest deformation of thecocoon happens at the innermost layer of the area under the impacter(Fig.12). After delamination damage, the individual layer would beable to deform independently, and the properties of each layer woulddetermine its own damage mechanism. We have learnt from ourprevious publication that the mechanical properties of cocoonlayers decrease from the inner to the outer direction (Chen et al.,2012b). This is also confirmed by tensile tests of the cocoons inthis project (Fig.3). FEA simulation, in contrast, shows that thedeformation of layers decreases from inner to outer layers (Fig.12).It has been pointed out by Zhao et al. (Zhao et al., 2005) that thismaterial–structure relationship may have evolved to adapt to thecocoon bending behaviour, which is part of the impact deformation,


as the inner layer would sustain more tensile force than the outerlayers.

The A. pernyi cocoon has a breakage mechanism similar to thatof the B. mori cocoon, where the damage initiates at the brittle sericinand leads to an extensive delamination between the layers (Fig.6).The separated layers deform to absorb the impact energy and therelatively strong inner layers provide stiffness and stress to thestructure. Given the species-specific geometry and identical loadingregimes, peak stress was lower in the A. pernyi cocoon because ofits bigger size, leading to less damage and higher impact resistance(Fig.5). Further, the calcium oxalates crystals found on the cocoonsurface (Chen et al., 2012a) may also help to improve the hardnessof the materials and therefore the impact resistance.

In comparison, the O. eucalypti cocoon seems to employ anotherstrategy to protect the pupa. It has a high stiffness material propertyfrom its fibre connectivity structure because of its low porosity(Figs1, 3). This reduces the ability to deform the structure anddamage of the materials, resulting in a high impact resistance. Apartfrom sericin cracking, fibre breakage is its significant energy-absorbing mechanism. It leads to a catastrophic penetration whenthe sericin crack propagates to the fibres and the failure reaches acritical extent (Fig.6). This mechanism localises the damage underthe impacter, avoids excessive damage and maintains the structureintegrity in other undamaged areas. In nature, O. eucalypti seemsto have tolerance of holes in the cocoon, as it fabricates woven holesaround its attachment in the cocoon construction (Fig.1). This maybe a compensating strategy for ventilation as it has very low porosityin the cocoon walls compared with other species (Chen et al., 2012c).These fabricated holes do not appear to interfere with the structureand mechanical properties of the rest of the cocoon wall, unlikeother nonwoven cocoons. In this case, it is not surprising that theO. eucalypti cocoon would employ a penetration-breaking mode inits cocoon impacting behaviour.

Stre

ss (M

Pa)

Silk fibre

Sericin O. eucalyptiA. pernyi

B. mori

400

300

200

100

00 20 40 60

Strain (%)

Stre

ss (M

Pa)

60

40

20

0 0.3 0.6 0.9

B. mori test dataB. mori cocoon material simulationB. mori sericin material simulation

0

Strain

Fig.13. Stress–strain curves of silk fibre, sericin and cocoons. Data for silkfibre and sericin were obtained from previous work (Chen et al., 2010b).

Fig.14. Stress–strain curves for the Bombyx mori cocoon experimental test(red), the cocoon material simulation (black) and the sericin materialsimulation (blue).



The impact behaviour of cocoon composites is very similar tothat of conventional composite laminates, where layers of alignedunidirectional carbon fibres stack with epoxy matrix bondingbetween the fibres (Chen and Hodgkinson, 2011). Materials andstructural design are the key tools for controlling energy absorptionand toughness of composites. These design principles in compositesengineering can be used to understand the design criteria of cocoonstructure by connecting the materials and structure with theirengineering functionality. On the one hand, comparative analysesof cocoons from a broader sample of wild species are essential totest whether the observed cocoon properties and structures are aresult of adaptations to predators employing different strategies topenetrate the cocoon walls. On the other hand, as a complicatedengineering product arisen from millions of years of evolution tofit their individual functions, silk cocoons may be able to providea wealth of examples of how to apply biomechanical engineeringprinciples in the design of synthetic structural composites.

AUTHOR CONTRIBUTIONSF.C. conceived the study, executed the experiments and the data analysis, andwrote the main body of the text. T.H. constructed the cocoon model andperformed the FEA simulations. D.P. developed the material models forsimulations from experimental data. F.V. provided the biological background forthe study and revised the text.

COMPETING INTERESTSNo competing interests declared.

FUNDINGThis work was supported by The Air Force Office of Scientific Research (grantnumber F49620-03-1-0111 to F.C.), the Intra-European Marie Curie Fellowship forCareer Development (project number 234818, to T.H.) and the EuropeanResearch Council (grant number SP2-GA-2008-233409 to D.P. and F.V.).

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