Effect of Loading Rate on Mechanical Properties and FractureMorphology of Spider SilkMatthew Hudspeth,† Xu Nie,‡ Weinong Chen,*,†,‡ and Randolph Lewis§

†School of Materials Engineering, Purdue University, West Lafayette, Indiana 47907, United States,‡School of Aeronautics and Astronautics, Purdue University, West Lafayette, Indiana 47907, United States§Department of Biology, Utah State University, Logan, Utah 84322, United States

ABSTRACT: Spider silks have been shown to haveimpressive mechanical properties. In order to assess the effectof extension rate, both quasi-static and high-rate tensileproperties were determined for single fibers of major (MA)and minor (MI) ampullate single silk from the orb weavingspider Nephila clavipes. Low rate tests have been performedusing a DMA Q800 at 10−3 s−1, while high rate analysis wasdone at 1700 s−1 utilizing a miniature Kolsky bar apparatus.Rate effects exhibited by both respective silk types areaddressed, and direct comparison of the tensile responsebetween the two fibers is made. The fibers showed major increases in toughness at the high extension rate. Mechanical propertiesof these organic silks are contrasted to currently employed ballistic fibers and examination of fiber fracture mechanisms areprobed via scanning electron microscope, revealing a globular rupture surface topography for both rate extremums.

■ INTRODUCTION

Spiders produce some of the most impressive natural fibers. Inparticular, orb weaving spiders can produce a variety of silkfibers possessing vastly different physical properties.1,2 Ofparticular interest are the two structural silks, which are derivedfrom the major (MA) and minor (MI) ampullate glands, andare used by the spider in order to effectively construct theframework for its nutrient gathering web. These silks have beenshown to possess striking mechanical properties, requiringroughly the same amount of energy to break as currentlyemployed high-performance fibers such as Kevlar.3 Due to theenergy dissipative capabilities of these architectural silks, muchwork has gone into compiling the amino acid sequence motifsfound in both the MA and MI fibers.4−6 With this knowledge,efforts have begun not only studying the silk itself, but are alsotrying to synthesize the MA fiber on a commercial level, withsome success being accomplished thus far.7

With such attention, structural spider silks have been testedin numerous quasi-static tension environments, generating wideinconsistencies between various reported silk properties bydiffering researchers and even inconsistency in single reportedtest sequences.8−12 Therefore, the variability exhibited by thespider’s dragline silk has received much consideration, and amultitude of external and internal factors have been postulatedas silk behavioral governing parameters. Some of thesemechanical response differences have been attributed to speciestype, temperature, humidity, food intake, size, use of anesthesiaduring silking, silking rate, and fiber load experienced duringthe silking session.12−19 While the latter are likely to be themost profound regulating constituents, it is important tounderstand as many variable factors as possible. For example,

raising spider size during the silking procedure can increasethread diameter and failure stress while simultaneouslydecreasing the initial elastic modulus.17,20−22 Additionally, alack of nutrients consumed by the spider can cause a decreasein the silk’s failure strain,13 and it has even been hypothesizedthat a deprivation of proteins necessary for silk productionspurred the evolutionary response of arachnids to developmultiple ampullates in efforts to create silks with differing basicamino acid structures.20

It is also important to note that the environmental conditionswherein the silk is tested can have an effect on the stress−strainresponse. For example, an inherent limiting factor of the MAsilk is its change in mechanical properties when exposed toextreme hydration.15 Termed supercontraction, this effectcauses the silk to mimic a rubber-like material during itswetted state,23 thereupon causing an almost 1000-fold loss insilk stiffness.3 In light of such aforementioned variabilities, it isalso possible that the mechanical response of these highlyamorphous fibers, estimated to be roughly 30% crystalline byvolume for the genus Araneus,24 is subject to differences inmechanical properties due to the rate of deformation used inthe tensile testing procedure. It is well-known that variousmaterials will exhibit a high degree of rate sensitivity, beingexemplified by the viscoelastic behavior common in highlyamorphous materials such as EPDM rubber25 or the children’stoy commonly called silly putty. Furthermore, because the MAand MI silks are of such great interest in structural and ballistic

Received: March 8, 2012Revised: May 31, 2012Published: July 10, 2012

Article

pubs.acs.org/Biomac

© 2012 American Chemical Society 2240 dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−2246

applications, it is imperative from a material characterizationstandpoint to understand the response of such a biopolymerwhen tested at increasing strain rates. Very little effort has beendirected at the sensitivity of spider silk to extension rate, andpublished data have shown highly variable effects.3,10,11 BothDenny10 and Gosline et al.3 analyzed the rate sensitivity of MAfibers at a variety of low strain rates, while Cunniff et al.11

analyzed strain rates experienced in ballistic impacts. Denny,who tested the orb weaver A. sericatus saw a 3-fold increase inrupture energy when varying the testing strain rate from 0.0005s−1 to 0.024 s−1, along with an increase in failure stress andelastic modulus. Gosline et al., who tested A. diadematus MAsilk, pushed the testing strain rate up to 30 s−1 via dropping anobject onto a horizontal silk element, rendering a impressive10-fold increase in rupture energy. Although demonstrativelyshowing the strain-rate dependence of the MA silk fiber, it isimportant to note that no effect of wave propagation is takeninto account, even though a pseudotransverse impactexperimental technique was implemented. Cunniff et al.,11

who tested MA silk from N. clavipes, varied the tensile strainrate in excess of 3000 s−1 in a transverse ballistic impactenvironment and yielded no rate sensitivity for both the initialelastic modulus and failure strain. Whether this lack of ratesensitivity exemplified by the latter work correctly depicts thetrue material response of the silk or is a function of the testingparameters is unknown. Regardless, the necessity to reach thisorder of magnitude in material deformation strain rate is mostimportant in developing understanding of silk impact behavior.Thus, a more veritable experimental analysis utilizing a robustand accurate determination of strain-rate dependence of singlesilk fibers spanning many orders of magnitude may shednecessary light on the potential capabilities of these profoundnatural materials.

■ EXPERIMENTAL SECTIONMaterials. Both the MA ampullate and MI ampullate silks were

elicited via forcible silking using a constant silking rate of 20 cm/sec.The former was extracted from one single spider, and the latter wasgathered from a compilation of several different spiders, all within thespecies N. clavipes. The silking procedure is described elsewhere,26,27

with both silk types being wrapped onto separate glass vial housings.These vials were then packaged into separate larger container systemsensuring no contact with the surface of each set of spider silk. Sampleswere then stored in a padded housing kept at a constant temperatureand relative humidity of 72.5 oF and 34%, respectively, until futurehandling.Methods. Silks were carefully removed from their vial housing and

attached to rectangular cardboard substrates, as shown in the subset ofFigure 1, possessing a centered hole with the desired testing gaugelength: 5 mm and 3 mm for quasi-static and high-rate tests,respectively. A slow curing epoxy adhesive was chosen for silkattachment in order to minimize temperature effects imposed on thespecimen ends. Due to the extremely low force level needed to breakboth silk types, quasi-static tests were performed on a TA Q800 DMAmachine via implementation of a displacement controlled runsequence. This device houses a vertical rod translating on air bearingsvia a noncontact, direct drive motor, enabling a precise forceproduction (±0.1 mN resolution). The system is also equipped withboth a force transducer capable of measuring load levels down to 10nN and a high-resolution optical encoder allowing for accuratedisplacement resolution in the range of 1 nm. Additionally, thistranslation sensor provides for a displacement feedback signal guidingthe drive motor. Fiber specimens of both silk types were sequentiallyloaded into the device and tested via strain-rate controlled sequenceemploying a rate of 10−3 s−1. System compliance was assumed

negligible due to the extremely low breaking force levels experiencedduring the testing procedure (∼10 mN).28

In efforts to achieve accurate high strain rate measurements of thetensile behavior of these exceedingly fine fibers, a miniature tensionKolsky bar, seen in Figure 1, has been adapted from a previous study,29

allowing for strain rates occurring in the range of 103 s−1. As comparedto a traditional Kolsky tension bar, this miniature setup neglects theuse of a transmission bar due to the large impedance mismatch existingbetween the fiber sample and both the incident and transmission bars.In effect, a high-resolution load cell replaces the transmission bar, andthe force history seen in the load cell is collected. Interestingly, due tothe extremely low force levels needed to fracture these silk specimens,several high frequency noise culprits arose, which if not attenuated,completely overwhelmed the desired force history. The mostdetrimental was found to be acoustic noise originating from thestriker tube hitting the end flange, thereby causing an auditory ringingvibration. This ringing oscillation history was then able to run thelength of the incident bar, similar to the propagating stress wave, andthen broadcast across the expanse between the bar end and load cell.Subsequently, this noise excited a vibratory load response from theforce transducer on the same order of magnitude as the rupture forceexhibited by the silk itself. In efforts to quell this acoustic vibration,thin aluminum plates were designed to provide a barrier within theexpanse, leaving only a very small aperture for the fiber to pass, whichis depicted in Figure 1. Implementation of these blocker plateseffectively reflected the majority of the broadcasted acoustic noise,thereby attenuating the auditory vibrations to a level deemed negligibleduring the testing procedure. It is important to note that aperturealignment was carefully executed during each testing routine in orderto ensure zero contact of the fiber by the aperture boundary.

A direct measurement of bar end translation has been adopted forthis study, and as seen in Figure 1, consists of a laser line focused by anoptical lens and then collected down onto a photo diode.Displacement history is determined via deflection of the incident barend protruding into the laser path line, thereby causing an increase inradiation intensity sensed by the laser detector during test progression.It is important to note that the strategic positioning of theaforementioned blocker plates resulted in a negligible effect on thelaser measurement system. Load cell and laser detector signals werecollected via oscilloscope and then synchronized from initial forcedetection for determination of strain and force histories experiencedby the fiber sample. A typical set of collected waveforms can be seen inFigure 2A. The incident pulse, following an initial ramp lastingapproximately 90 microseconds, reaches a constant plateau for 120microseconds, pointing toward a constant rate of deformation in thislatter regime. From the laser signal, which displays a monotonicuniform intensity distribution inside the translation field of interest,the displacement history of the bar end is linear after 90 microsecondsof the ramp initiation, which independently verifies a constant rate ofdeformation experienced by the sample. This is corroborated by Figure

Figure 1. Miniature Kolsky tension bar.

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462241

2B, wherein a detailed strain rate history is depicted in tandem withthe engineering stress experienced in the silk sample. A region ofconstant strain rate of 1700 s−1 is evident 100 microseconds after theonset of bar deformation and lasts until ultimate failure of thespecimen. There is no sign of slippage in the glue joints during thishigh rate testing, indicating that the chosen epoxy is satisfactory.For both diameter measurement and fracture surface analysis, fibers

were imaged using a high-resolution Scanning Electron Microscope(HRSEM). Silk samples were mounted on SEM stubs and coated withAuPd using a Hummer 6.2 sputter coater. Samples were thenintroduced into an FEI Nova HRSEM and imaged at a 5 mm workingdistance using either a 5 or 6 kV accelerating voltage. Fiber diametermeasurements yielded values of 5.23 ± 0.16 μm and 3.17 ± 0.10 μmfor the MA and MI silks, respectively.

■ RESULTS AND DISCUSSION

In efforts to gather a rate sensitivity baseline, quasi-statictension tests were performed on both single fiber MA and MIsilks at a rate of 10−3 s−1. At least 10 tests were repeated oneach silk, and the resultant stress−strain response can be foundin Figure 3. The results show both MA and MI silks behavingsimilarly, possessing a failure stress of 0.83 ± 0.08 GPa and 1.07± 0.12 GPa, respectively. The failure strain and initial elastic

modulus were 0.12 ± 0.022 and 12.06 ± 1.61 GPa for the MAsilk and 0.148 ± 0.032 and 8.93 ± 1.16 GPa for the MI silk,respectively. Finally, the energy density required to ruptureboth the MA and MI silks was determined to be 63.16 ± 16.30MJ/m3 and 88.77 ± 29.18 MJ/m3, respectively. These resultsare summarized in Table 1.Following quasi-static analysis, both the MA and MI silks

were tested at a dynamic rate of 1700 s−1 utilizing the miniaturetension Kolsky bar apparatus described above. At least 10 testswere performed on both silk types, and both sets of stress−strain curves are also depicted in Figure 3. Like the quasi-staticresults, at this greatly increased testing strain-rate, both MA andMI silks again behaved similarly, having a failure stress of 1.43± 0.11 GPa and 1.5 ± 0.35 GPa, respectively. Likewise, thefailure strain and initial elastic modulus had values of 0.19 ±0.042 and 34.39 ± 8.89 GPa for the MA silk and 0.162 ± 0.062and 35.52 ± 13.80 GPa for the MI silk, respectively. Finally, therupture energy density exhibited by the MA and MI silks was193.0 ± 53.4 and 168.5 ± 101.7 MJ/m3, respectively. Theseresults are also summarized in Table 1.The large scatter seen by the MI silk as opposed to the MA

fiber for both the quasi-static and high-rate tests is assumed to

Figure 2. Representative signal histories. (a) Typical Kolsky bar voltage signals. (b) Strain rate history experienced by single fiber.

Figure 3. Stress−strain curves from both MA and MI silks at low and high rates.

Table 1. Mechanical Properties of Both MA and MI Silks at Varying Strain Rates along with Fiber Properties of Two CurrentlyEmployed Ballistic Fibers

silk type gage length (mm) rate (s−1) failure stress (GPa) failure strain (%) initial modulus (GPa) failure energy MJ/m3 diameter (μm)

major 5 0.001 0.83 ± 0.08 12.0 ± 2.2 12.06 ± 1.61 63.16 ± 16.30 5.23 ± 0.163 1700 1.43 ± 0.11 19.0 ± 4.2 34.39 ± 8.89 193.0 ± 53.43

minor 5 0.001 1.07 ± 0.12 14.8 ± 3.2 8.93 ± 1.16 88.77 ± 29.18 3.17 ± 0.103 1700 1.5 ± 0.35 16.2 ± 6.2 35.52 ± 13.80 168.45 ± 101.67

KM2 10 600 4.38 ± 0.68 4.07 ± 0.94 152.45 ± 23.62 102.04 ± 35.69 12.31 ± 0.17dyneema 10 600 3.81 ± 0.29 2.65 ± 0.62 237.94 ± 28.47 67.33 ± 19.58 16.21 ± 0.74

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462242

have arisen from the variability in the tested silk itself. The MIsilk is a compilation of strands from several different spiderssilked at differing times, while the MA silk is a single strandfrom one spider derived during a singular silking session. It isaccepted that fibers silked from various individuals within thesame species can differ drastically in mechanical properties.13 Itis also possible that the periods wherein MI silk was drawncoincided with cycles of large fluctuation in applied forcerendered from the spider’s braking mechanism, which is notuncommon.12 It has been shown that silk tensile properties aregoverned by the force experienced during the silkingprocess,12,30 thus potentially rendering the MI silk mechanicalresponse relatively variable. In light of this force governingparameter, it is likely the MA silk tested for this studyoriginated during a relatively constant force region of theforcible silking procedure, resulting in the minimal amount ofscatter exhibited by both the quasi-static and high-rate stress−strain response of the MA silk. It is also important to note therelative similarities seen in mechanical properties from both theMA and MI silks. As opposed to the current work wherein fiberdiameter measurements are made via HRSEM, many previousstudies have used optical microscopy or laser diffraction,rendering error in diameter measurement up to 50%.8 Thisamount of error could easily account for previous worksconcluding that the MA silk is typically stronger and stiffer thanits MI counterpart. Upon closer inspection of the quasi-staticresults, a slight difference exists in the stress−strain evolutionbetween the MA and MI fiber, with the latter portraying adefinite yield being characteristic in structural spider silk testing,while the former depicts a less customary biphasic response.During the forcible silking procedure, it has been shown thatspiders will usually provide an extremely high friction-brakedrawing force in efforts to quell the loss of such precious lifelinematerial, which may be up to 60% of the fiber’s breaking load.12

At such a high stress-level, this drawing force may allow for anincrease in crystalline region alignment and thereby potentiallywipe out the MA silk’s typical yield nature.In order to better visualize the rate dependency of both fiber

types, low and high rate response have been overlaid and can beseen in Figure 4 for both the MA and MI silks. Clearly there isan increase in failure stress, initial elastic modulus, and ruptureenergy with an increased rate of strain. Indeed, directcomparison of resulting low and high rate mechanicalproperties shows a clear increase with a rise in strain rate asseen in Figure 5. Regarding failure stress, there is a 70% and40% increase for the MA and MI silks, respectively, while theinitial elastic modulus increases 3-fold and 4-fold, respectively.

Most impressive is the increase in rupture energy, resulting in a3-fold and 2-fold amplification for the MA and MI silks,respectively, upon increasing strain rate. Concerning failurestrain, the MA silk exhibits a 60% improvement in value, whilethe rate dependency of MI failure strain is unclear.

Comparison to High-Performance Fibers. In light of thenature of this study, it is worthwhile to discuss the similarcharacteristics exhibited by both of these structural spider silksand currently employed high performance fibers. Figure 6shows a stress−strain plot depicting a few representative MAand MI silks tested at 1700 s−1 along with several single fiberDyneema and KM2 fibers tested at 600 s−1. Immediately, fourfeatures become apparent. First, the elastic modulus and failurestrength of the high performance fibers are much greater thanthe two tested spider silks. The high-performance fiber-to-spider silk modulus and strength ratios are almost 10-fold and3-fold higher, respectively. The former results in a drasticdecrease in deflection exhibited by the high-performance fibersas compared to both spider silks during tensile loading and thelatter of course results in the high-performance fibers beingmuch stronger than both spider silks in the axial direction.Second, the elastic-plastic nonlinearity exhibited by both spidersilks renders a nonrupture deformation cycle susceptible topermanent deflection, as opposed to the linear elastic responseprevalent in both Kevlar and Dyneema fibers, wherein if loaded

Figure 4. Stress−strain curves of both MA and MI silk curves depicting rate sensitivity.

Figure 5. Effect of testing strain rate on: (A) failure energy, (B) failurestress (C) elastic modulus, and (D) failure strain.

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462243

to a stress level below their respective failure tolerances, theresulting plastic strain is minimal. Third, there exists a high levelof viscoelasticity exhibited by both MA and MI silks as opposedto the slightly viscoelastic response of the Kevlar and Dyneemafibers. This viscoelastic property of the spider fibers most likelyderives from the lesser crystallinity of both the MA and MIsilks, 30% crystalline by volume,24 as opposed to the 80−95%exhibited by high-performance fibers.31,32 Fourth, the failurestrain exhibited by both MA and MI silks is as much as 6 timesgreater than that of the high-performance fibers, accounting forthe enormously large rupture energy needed to break bothspider silks, which during this test is as much as 3 times greaterthan that of Kevlar, and has been reported to be as much as 10times greater for the Caerostris darwini spider found inMadascar, when tested in quasi-static tension.33 In light ofthis phenomenal energy dissipation characteristic, it isenlightening to employ the use of an important fibercomparison tool that has been previously established34 topredict the transverse impact performance of a fabric fromsingle fiber material response as shown in the following:

σερ ρ

=UE

2 (1)

with σ, ε, ρ, and (E/ρ)1/2 representing fiber failure stress, failurestrain, density, and elastic wave speed, respectively. (U)1/3 maythen be used to compare the possible velocity (V50) at which aspecific projectile will penetrate different armor systems.Although the increased failure energy characteristic of bothMA and MI silks is impressive, resulting in a (U)1/3 predictionfor the MA and MI silks of at least 780 m/s, the lack of axialstiffness cannot be outweighed from a deflection standpoint.During armor transverse impact, it is imperative that themagnitude of fabric deflection is as minute as possible in orderto ensure the wearer’s bodily deformation is minimized. Thedrastically reduced stiffness of the tested spider silks ascompared to the synthetic fiber renders the former materialmuch less adept at minimizing bodily harm due to fabricdeflection, even if it may be able to halt an oncoming projectile.It is also important to note that the previous determination ofU assumes a linear elastic stress−strain response, beingcommon in high-performance fiber testing, thus the previous(U)1/3 value may be overvalued as the elastic moduli of the silksreduce with increasing strain. Nonetheless, the remarkablecharacteristics of spider silk make it a superb structure foranalysis and may unveil key fundamental aspects needed tobetter engineer currently employed high-performance fabrics.

Origin of Viscoelastic Properties. It is likely that thepresence of this rate-sensitivity in the silk fibers has arisen dueto the results of 400 million years of evolution.1 In order tosurvive, efficient web architecture may have evolved via bothweb geometry constraints and innate single fiber materialcost.35 While some researchers have suggested that silk isoptimized due to the evolutionary time scale, thereby acutelylimiting possible improvements in biomimetic applications,36 itis much more likely that silk has been optimized for a variety ofconditions, rendering each silk type suboptimal in some specificapplications.2 Regardless, the cost of web production doesaffect the size and thread density of the web architecture,rendering depletion of silk material from the gland storehousesdetrimental to the spider’s foraging capabilities.37 In light of thecaloric expenditure needed for each web, it is reasonable toassume that thread development and web design havecoevolved over time, introducing mechanisms to prevent webdestruction.First, it is impractical for smaller sized spiders to produce

extremely large webs capable of halting prey much larger thanthe spider itself while still ensuring that the web will not beutterly destroyed by prey. Thus, it is more advantageous forsmaller spiders to build webs of reduced size, which can beconstructed with a reduced risk of destruction.38 Second, itwould be beneficial for a silk to exhibit mechanical propertiesdependent on strain rate, as this would allow for a prey size/mass sorting mechanism. Ultimately, in collecting prey with awide size and mass range, viscoelasticity would allow varyingeffects of different impacting energies of the incoming prey.While a larger prey, which can harm the web structure if caught,may strike the web with a range of velocities, the ultimatestrength of the web structure would preferably be lower thanneeded to capture large prey, preventing destruction of theweb. In contrast, smaller prey, which can also impact the web ina range of varying velocities, would still be effectively captured ifthe web rupture energy was consistently greater than thatneeded to halt the smaller prey. As a comparison, if the webfiber was not rate-sensitive (e.g., Kevlar fiber), the maximumamount of stopping energy of the web structure would beconstant. If a web was able to catch a smaller insect moving at afast speed, then it may too allow for slow moving large insectsto be caught, which as previously stated, could be inopportune.Thus, the strain rate sensitivity demonstrated here by both

MA and MI silk can provide for prey capture differentiation dueto a cutoff web rupture energy. As noted recently35 even iflarger prey were caught, it appears that only a local area ofdestruction will occur, which can be repaired by the spider. It isalso important to note the elastic-plastic response of the framesilk, as this deformation mechanism allows energy to bedissipated via heat during insect impact. In contrast, if thedeformation response was purely elastic, incoming prey beingstopped by the web would then experience a spring-back effectpossibly catapulting the prey out of the orb-web entrapment.10

Fracture Surfaces. Due to the lack of conclusive findingsregarding MA spider silk failure mechanisms under tensileloading, and because, to the authors’ knowledge, no analysis ofMI fracture surfaces has been published, both silk types werebroken in tension at two drastically different strain rates, andthe resulting surface topographies have been inspected. Forboth rate extremes tested, the customary fracture contoursconsist of a rough texture with a relatively constant peak andvalley distribution with no presence of a major defect causingultimate failure. This globule-like surface undulation behavior,

Figure 6. Stress−strain curves of representative spider silks and high-performance fibers.

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462244

which can be seen in Figure 7, has sparked debate over themode of fracture being either brittle or ductile with various

works alluding to the former11,39,40 and latter41 mechanisms ofaction. It is important to note that even though MA and MIsilks exhibit a high degree of extensibility, ductile fracture is notrequired, as is the case with Lycra, which fails in tension atstrains over 500% in a brittle fashion,42,43 albeit Lycra exhibits astrain hardening response.44 More importantly, in both MA andMI silks, the deformation sequence disperses the majority ofthe loading cycle energy via heat.10 In light of this and due tothe minimal damage seen on the typical fracture surfaces, thepoint of ultimate failure most likely does not drastically alter thetotal energy dissipated during loading regardless of whether theultimate failure is a more instantaneous brittle rupture or aprogressive ductile process. This is also corroborated by thecongruency exhibited by both the low- and high-rate resultingfracture topographies even though there is a very large increasein the energy needed to rupture both fiber types. Thus, theenergy dispersion mechanisms incurred during the tensileloading process are of much greater concern.It is important to note that a few fracture morphologies did

not exhibit the typical mosaic topography, rather they displayedboth axial splitting and fibrillation rupture morphologies, whichcan be seen in Figure 8A,B, respectively. The former fracture

mode was uncovered during the typical quasi-static testingexperience, while the latter was found during efforts to generatea kink-band surface defect, which is highly uncommon in spiderfiber.45 In order to promote the evolution of kinks bands, a MAsilk was folded on itself, and firm pressure was applied to thecorner zone with thumb and index finger application. Thissample was then gently pulled in tension and imaged viaHRSEM, rendering a most unusual fibrillated fracture surface asseen in Figure 8B. Clearly, there is the presence of a fibrillatedfailure topography. Both of these fracture mechanisms, axialsplitting and fibrillation, are commonly evidenced in high-performance fiber failure and are indicative of a highly fibrillarfiber architecture.42 It can be tentatively stated that if thepresence of fibrils does exist, they possess a high degree oflateral bonding, which would explain the lack of kink-bandsevidenced in all samples tested.45

■ CONCLUSIONS

MA and MI fibers have been subjected to quasi-static (10−3 s−1)and high rate (1700 s−1) tensile testing with results showing avery large increase in mechanical properties such as failurestress, initial elastic modulus, and rupture energy for both silktypes upon increased testing strain rate. The latter mentionedmaterial response (rupture energy), yields both silks severaltimes tougher than high-performance fibers such as Kevlar orDyneema. It is this deformation characteristic that hasprompted spider silk to be of such great interest and it ispostulated that this rate-sensitive mechanism has evolved inorder to allow the orb-web to act as a selective prey filtrationdevice. Analysis of fiber rupture surfaces have yieldedcommonly described globular topographies regardless of thetesting strain rate and various unusual fiber breakingmorphologies have alluded to a potential fibrillar micro-structure.

■ AUTHOR INFORMATION

Corresponding Author*E-mail: wchen@purdue.edu.

NotesThe authors declare no competing financial interest.

■ ACKNOWLEDGMENTS

This research was supported by the US ARMY PEO Soldierprogram. The first author would also like to thank the NDSEGfellowship for graduate research funding.

■ REFERENCES(1) Koover, Ecophysiology of Spiders; Springer-Verlag: Berlin-Heidelberg, 1987.(2) Vollrath, F. Int. J. Biol. Macromol. 1999, 24, 81−88.(3) Gosline, J. M.; Guerette, P. A.; Ortlepp, C. S.; Savage, K. N. J.Exp. Biol. 1999, 202, 3295−3303.(4) Xu, M.; Lewis, R. Biochemistry 1990, 87, 7120−7124.(5) Hinman, M. B.; Lewis, R. V. J. Biol. Chem. 1992, 267, 19320−19324.(6) Colgin, M.; Lewis, R. Protein Sci. 1998, 7, 667−672.(7) Hinman, M. B.; Jones, J. A.; Lewis, R. V. TIBTECH 2000, 18,374−379.(8) Zemlin, J. A Study of the Mechanical Behavior of Spider Silks;Collaborative Research, Inc: Waltham, MA, 1968(9) Work, R. W. Text. Res. J. 1976, 485−492.(10) Denny, M. Exp. Biol. 1976, 65, 483−506.

Figure 7. Typical silk fracture surfaces at both low and high rates. (A)MI silk at 1700/s, (B) MI silk at 0.001/s, (C) MA silk at 1700/s, and(D) MI silk at 0.001/s.

Figure 8. Atypical fracture surfaces seen during: (A) MI silk low ratetesting, and (B) MA silk fold-pull test.

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462245

(11) Cunniff, P. M.; Fossey, S. A.; Auerbach, M. A.; Song, J. W. SilkPolymers; ACS Symposium Series; American Chemical Society:Washington, DC, 1993; pp 234−251.(12) Ortlepp, C. S.; Gosline, J. M. Biomacromolecules 2004, 5, 727−731.(13) Madsen, B.; Shao, Z.; Vollrath, F. Int. J. Biol. Macromol. 1999,24, 301−306.(14) Vollrath, R.; Madsen, B.; Shao, Z. Proc. Biol. Sci. 2001, 268,2339−2346.(15) Work, R. W. Text. Res. J. 1977, 47, 650−662.(16) Vollrath, F.; Samu, F. Bull. Br. Arachnol. Soc. 1997, 10, 295−298.(17) Christiansen, A.; Baum, R.; Witt, P. N. J. Pharmacol. Exp. Ther.1962, 136, 31−37.(18) Madsen, B.; Vollrath, F. Naturwissenschaften 2000, 87, 148−153.(19) Cunniff, P. M.; Fossey, S. A.; Auerbach, M. A.; Song, J. W.;Kaplan, D. L.; Adams, W. W.; Eby, R. K.; Mahoney, D.; Vezie, D. L.Polym. Adv. Technol. 1994, 5, 401−410.(20) Craig, C. L. Am. Nat. 1987, 129, 47−68.(21) Vollrath, F.; Kohler, T. Proc. R. Soc. London, Ser. B: Biol. Sci.1996, 263, 387−391.(22) Garrido, M.; Elices, M.; Viney, C.; Perez-Rigueiro, J. Polymer2002, 43, 1537−1540.(23) Gosline, J.; Denny, M.; Demont, M. Lett. Nat. 1984, 309, 551−552.(24) Gosline, J. M.; DeMont, M. E.; Denny, M. W. Endeavour 1986,10, 37−43.(25) Nie, X.; Song, B.; Ge, Y.; Chen, W.; Weerasooriya, T. Exp. Mech.2009, 49, 451−458.(26) Work, R. W.; Emerson, P. D. J. Arachnol. 1982, 10, 1−10.(27) Stauffer, S.; Coguill, S.; Lewis, R. J. Arachnol. 1994, 22, 5−11.(28) Perez-Rigueiro, J.; Viney, C.; Llorca, J.; Elices, M. J. Appl. Polym.Sci. 1998, 70, 2439−2447.(29) Cheng, M.; Chen, W.; Weerasooriya, T. J. Eng. Mater. Technol.2005, 127, 197−203.(30) Perez-Rigueiro, J.; Elices, M.; Plaza, G.; Real, J. I.; Guinea, G. V.J. Exp. Biology. 2005, 208, 2633−2639.(31) Prevorsek, D. In High Technology Fibers, Part D; Lewin, M.,Preston, J., Eds.; Marcel Dekker, Inc.: New York, 1996; Vol. 3, pp 1−170.(32) Smith, A. P.; Ade, H. Appl. Phys. Lett. 1996, 69, 3833−3835.(33) Agnarsson, I.; Kuntner, M.; Blackledge, T. A. PLoS One 2010, 5,e11234.(34) Cunniff, P. Dimensionless Parameters for Optimization ofTextile-Based Body Armor Systems. In Proceedings of the 18thInternational Symposium on Ballistics, San Antonio, TX/Lancaster,PA, 1999.(35) Cranford, S. W.; Tarakanova, A.; Pugno, N. M.; Buehler, M. J.Nature 2012, 482, 72−76.(36) Elices, M.; Plaza, G. R.; Arnedo, M. A.; Perez-Rigueiro, J.;Torres, F. G.; Guinea, G. V. Biomacromolecules 2009, 10, 1904−1910.(37) Vollrath, F.; Downes, M.; Krackow, S. Physiol. Behav. 1997, 62,735−743.(38) Eberhard, W. G. J. Arachnol. 1988, 16, 295−302.(39) Perez-Rigueiro, J.; Elices, M.; Llorca, J.; Viney, C. Appl. Polym.Sci. 2001, 82, 2245−2251.(40) Poza, P.; Perez-Rigueiro, J.; Elices, M.; LLorca, J. Eng. Fract.Mech. 2002, 69, 1035−1048.(41) Perez-Rigueiro, J.; Elices, M.; Plaza, G. R.; Rueda, J.; Guinea, G.V. J. Polym. Sci., Part B: Polym. Phys. 2007, 45, 786−793.(42) Elices, M., Llorca, J., Eds. Fiber Fracture; Elsevier: New York,2002.(43) Hearle, J. Atlas of Fibre Fracture and Damage to Textiles, 2nd ed.;Woodhead Publishing Limited: Boca Raton, FL, 1998.(44) Hicks, J.; Elija, M.; Ultee, A. J.; Drougas, J. Science 1965, 147,373−379.(45) Mahoney, D. V.; Vezie, D. L.; Eby, R. K.; Adams, W. W.;Kaplan, D. Silk Polymers; American Chemical Society, 1993; Vol. 544,Chapter 19, pp 196−210.

Biomacromolecules Article

dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−22462246