Effect of Loading Rate on Mechanical Properties and Fracture

Jul 10, 2012 - properties were determined for single fibers of major (MA) and minor (MI) ampullate single silk from the orb weaving spider Nephila cla...
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Effect of Loading Rate on Mechanical Properties and Fracture Morphology of Spider Silk Matthew 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 have impressive mechanical properties. In order to assess the effect of extension rate, both quasi-static and high-rate tensile properties were determined for single fibers of major (MA) and minor (MI) ampullate single silk from the orb weaving spider Nephila clavipes. Low rate tests have been performed using a DMA Q800 at 10−3 s−1, while high rate analysis was done at 1700 s−1 utilizing a miniature Kolsky bar apparatus. Rate effects exhibited by both respective silk types are addressed, and direct comparison of the tensile response between the two fibers is made. The fibers showed major increases in toughness at the high extension rate. Mechanical properties of these organic silks are contrasted to currently employed ballistic fibers and examination of fiber fracture mechanisms are probed via scanning electron microscope, revealing a globular rupture surface topography for both rate extremums.

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INTRODUCTION Spiders produce some of the most impressive natural fibers. In particular, orb weaving spiders can produce a variety of silk fibers possessing vastly different physical properties.1,2 Of particular interest are the two structural silks, which are derived from the major (MA) and minor (MI) ampullate glands, and are used by the spider in order to effectively construct the framework for its nutrient gathering web. These silks have been shown to possess striking mechanical properties, requiring roughly the same amount of energy to break as currently employed high-performance fibers such as Kevlar.3 Due to the energy dissipative capabilities of these architectural silks, much work has gone into compiling the amino acid sequence motifs found in both the MA and MI fibers.4−6 With this knowledge, efforts have begun not only studying the silk itself, but are also trying to synthesize the MA fiber on a commercial level, with some success being accomplished thus far.7 With such attention, structural spider silks have been tested in numerous quasi-static tension environments, generating wide inconsistencies between various reported silk properties by differing researchers and even inconsistency in single reported test sequences.8−12 Therefore, the variability exhibited by the spider’s dragline silk has received much consideration, and a multitude of external and internal factors have been postulated as silk behavioral governing parameters. Some of these mechanical response differences have been attributed to species type, temperature, humidity, food intake, size, use of anesthesia during silking, silking rate, and fiber load experienced during the silking session.12−19 While the latter are likely to be the most profound regulating constituents, it is important to understand as many variable factors as possible. For example, © 2012 American Chemical Society

raising spider size during the silking procedure can increase thread diameter and failure stress while simultaneously decreasing the initial elastic modulus.17,20−22 Additionally, a lack of nutrients consumed by the spider can cause a decrease in the silk’s failure strain,13 and it has even been hypothesized that a deprivation of proteins necessary for silk production spurred the evolutionary response of arachnids to develop multiple ampullates in efforts to create silks with differing basic amino acid structures.20 It is also important to note that the environmental conditions wherein the silk is tested can have an effect on the stress−strain response. For example, an inherent limiting factor of the MA silk is its change in mechanical properties when exposed to extreme hydration.15 Termed supercontraction, this effect causes the silk to mimic a rubber-like material during its wetted state,23 thereupon causing an almost 1000-fold loss in silk stiffness.3 In light of such aforementioned variabilities, it is also possible that the mechanical response of these highly amorphous fibers, estimated to be roughly 30% crystalline by volume for the genus Araneus,24 is subject to differences in mechanical properties due to the rate of deformation used in the tensile testing procedure. It is well-known that various materials will exhibit a high degree of rate sensitivity, being exemplified by the viscoelastic behavior common in highly amorphous materials such as EPDM rubber25 or the children’s toy commonly called silly putty. Furthermore, because the MA and MI silks are of such great interest in structural and ballistic Received: March 8, 2012 Revised: May 31, 2012 Published: July 10, 2012 2240

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applications, it is imperative from a material characterization standpoint to understand the response of such a biopolymer when tested at increasing strain rates. Very little effort has been directed at the sensitivity of spider silk to extension rate, and published data have shown highly variable effects.3,10,11 Both Denny10 and Gosline et al.3 analyzed the rate sensitivity of MA fibers 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 in rupture energy when varying the testing strain rate from 0.0005 s−1 to 0.024 s−1, along with an increase in failure stress and elastic modulus. Gosline et al., who tested A. diadematus MA silk, pushed the testing strain rate up to 30 s−1 via dropping an object onto a horizontal silk element, rendering a impressive 10-fold increase in rupture energy. Although demonstratively showing the strain-rate dependence of the MA silk fiber, it is important to note that no effect of wave propagation is taken into account, even though a pseudotransverse impact experimental technique was implemented. Cunniff et al.,11 who tested MA silk from N. clavipes, varied the tensile strain rate in excess of 3000 s−1 in a transverse ballistic impact environment and yielded no rate sensitivity for both the initial elastic modulus and failure strain. Whether this lack of rate sensitivity exemplified by the latter work correctly depicts the true material response of the silk or is a function of the testing parameters is unknown. Regardless, the necessity to reach this order of magnitude in material deformation strain rate is most important in developing understanding of silk impact behavior. Thus, a more veritable experimental analysis utilizing a robust and accurate determination of strain-rate dependence of single silk fibers spanning many orders of magnitude may shed necessary light on the potential capabilities of these profound natural materials.

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Figure 1. Miniature Kolsky tension bar. negligible due to the extremely low breaking force levels experienced during the testing procedure (∼10 mN).28 In efforts to achieve accurate high strain rate measurements of the tensile behavior of these exceedingly fine fibers, a miniature tension Kolsky 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 compared to a traditional Kolsky tension bar, this miniature setup neglects the use of a transmission bar due to the large impedance mismatch existing between the fiber sample and both the incident and transmission bars. In effect, a high-resolution load cell replaces the transmission bar, and the force history seen in the load cell is collected. Interestingly, due to the 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 most detrimental was found to be acoustic noise originating from the striker tube hitting the end flange, thereby causing an auditory ringing vibration. This ringing oscillation history was then able to run the length of the incident bar, similar to the propagating stress wave, and then broadcast across the expanse between the bar end and load cell. Subsequently, this noise excited a vibratory load response from the force transducer on the same order of magnitude as the rupture force exhibited by the silk itself. In efforts to quell this acoustic vibration, thin aluminum plates were designed to provide a barrier within the expanse, leaving only a very small aperture for the fiber to pass, which is depicted in Figure 1. Implementation of these blocker plates effectively reflected the majority of the broadcasted acoustic noise, thereby attenuating the auditory vibrations to a level deemed negligible during the testing procedure. It is important to note that aperture alignment was carefully executed during each testing routine in order to ensure zero contact of the fiber by the aperture boundary. A direct measurement of bar end translation has been adopted for this study, and as seen in Figure 1, consists of a laser line focused by an optical lens and then collected down onto a photo diode. Displacement history is determined via deflection of the incident bar end protruding into the laser path line, thereby causing an increase in radiation intensity sensed by the laser detector during test progression. It is important to note that the strategic positioning of the aforementioned blocker plates resulted in a negligible effect on the laser measurement system. Load cell and laser detector signals were collected via oscilloscope and then synchronized from initial force detection for determination of strain and force histories experienced by the fiber sample. A typical set of collected waveforms can be seen in Figure 2A. The incident pulse, following an initial ramp lasting approximately 90 microseconds, reaches a constant plateau for 120 microseconds, pointing toward a constant rate of deformation in this latter regime. From the laser signal, which displays a monotonic uniform intensity distribution inside the translation field of interest, the displacement history of the bar end is linear after 90 microseconds of the ramp initiation, which independently verifies a constant rate of deformation experienced by the sample. This is corroborated by Figure

EXPERIMENTAL SECTION

Materials. 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 was gathered from a compilation of several different spiders, all within the species 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 systems ensuring no contact with the surface of each set of spider silk. Samples were then stored in a padded housing kept at a constant temperature and relative humidity of 72.5 oF and 34%, respectively, until future handling. Methods. Silks were carefully removed from their vial housing and attached to rectangular cardboard substrates, as shown in the subset of Figure 1, possessing a centered hole with the desired testing gauge length: 5 mm and 3 mm for quasi-static and high-rate tests, respectively. A slow curing epoxy adhesive was chosen for silk attachment in order to minimize temperature effects imposed on the specimen ends. Due to the extremely low force level needed to break both silk types, quasi-static tests were performed on a TA Q800 DMA machine via implementation of a displacement controlled run sequence. This device houses a vertical rod translating on air bearings via a noncontact, direct drive motor, enabling a precise force production (±0.1 mN resolution). The system is also equipped with both a force transducer capable of measuring load levels down to 10 nN and a high-resolution optical encoder allowing for accurate displacement resolution in the range of 1 nm. Additionally, this translation sensor provides for a displacement feedback signal guiding the drive motor. Fiber specimens of both silk types were sequentially loaded into the device and tested via strain-rate controlled sequence employing a rate of 10−3 s−1. System compliance was assumed 2241

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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 Currently Employed Ballistic Fibers silk type major minor KM2 dyneema

gage length (mm)

rate (s−1)

failure stress (GPa)

failure strain (%)

initial modulus (GPa)

failure energy MJ/m3

diameter (μm)

5 3 5 3 10 10

0.001 1700 0.001 1700 600 600

0.83 ± 0.08 1.43 ± 0.11 1.07 ± 0.12 1.5 ± 0.35 4.38 ± 0.68 3.81 ± 0.29

12.0 ± 2.2 19.0 ± 4.2 14.8 ± 3.2 16.2 ± 6.2 4.07 ± 0.94 2.65 ± 0.62

12.06 ± 1.61 34.39 ± 8.89 8.93 ± 1.16 35.52 ± 13.80 152.45 ± 23.62 237.94 ± 28.47

63.16 ± 16.30 193.0 ± 53.43 88.77 ± 29.18 168.45 ± 101.67 102.04 ± 35.69 67.33 ± 19.58

5.23 ± 0.16 3.17 ± 0.10 12.31 ± 0.17 16.21 ± 0.74

modulus were 0.12 ± 0.022 and 12.06 ± 1.61 GPa for the MA silk and 0.148 ± 0.032 and 8.93 ± 1.16 GPa for the MI silk, respectively. Finally, the energy density required to rupture both the MA and MI silks was determined to be 63.16 ± 16.30 MJ/m3 and 88.77 ± 29.18 MJ/m3, respectively. These results are 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 miniature tension Kolsky bar apparatus described above. At least 10 tests were performed on both silk types, and both sets of stress− strain curves are also depicted in Figure 3. Like the quasi-static results, at this greatly increased testing strain-rate, both MA and MI silks again behaved similarly, having a failure stress of 1.43 ± 0.11 GPa and 1.5 ± 0.35 GPa, respectively. Likewise, the failure 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 ± 0.062 and 35.52 ± 13.80 GPa for the MI silk, respectively. Finally, the rupture energy density exhibited by the MA and MI silks was 193.0 ± 53.4 and 168.5 ± 101.7 MJ/m3, respectively. These results 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

2B, wherein a detailed strain rate history is depicted in tandem with the engineering stress experienced in the silk sample. A region of constant strain rate of 1700 s−1 is evident 100 microseconds after the onset of bar deformation and lasts until ultimate failure of the specimen. There is no sign of slippage in the glue joints during this high 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 with AuPd using a Hummer 6.2 sputter coater. Samples were then introduced into an FEI Nova HRSEM and imaged at a 5 mm working distance using either a 5 or 6 kV accelerating voltage. Fiber diameter measurements yielded values of 5.23 ± 0.16 μm and 3.17 ± 0.10 μm for the MA and MI silks, respectively.

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RESULTS AND DISCUSSION In efforts to gather a rate sensitivity baseline, quasi-static tension tests were performed on both single fiber MA and MI silks at a rate of 10−3 s−1. At least 10 tests were repeated on each silk, and the resultant stress−strain response can be found in Figure 3. The results show both MA and MI silks behaving similarly, possessing a failure stress of 0.83 ± 0.08 GPa and 1.07 ± 0.12 GPa, respectively. The failure strain and initial elastic 2242

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

have arisen from the variability in the tested silk itself. The MI silk is a compilation of strands from several different spiders silked at differing times, while the MA silk is a single strand from one spider derived during a singular silking session. It is accepted that fibers silked from various individuals within the same species can differ drastically in mechanical properties.13 It is also possible that the periods wherein MI silk was drawn coincided with cycles of large fluctuation in applied force rendered from the spider’s braking mechanism, which is not uncommon.12 It has been shown that silk tensile properties are governed by the force experienced during the silking process,12,30 thus potentially rendering the MI silk mechanical response relatively variable. In light of this force governing parameter, it is likely the MA silk tested for this study originated during a relatively constant force region of the forcible silking procedure, resulting in the minimal amount of scatter exhibited by both the quasi-static and high-rate stress− strain response of the MA silk. It is also important to note the relative similarities seen in mechanical properties from both the MA and MI silks. As opposed to the current work wherein fiber diameter measurements are made via HRSEM, many previous studies have used optical microscopy or laser diffraction, rendering error in diameter measurement up to 50%.8 This amount of error could easily account for previous works concluding that the MA silk is typically stronger and stiffer than its MI counterpart. Upon closer inspection of the quasi-static results, a slight difference exists in the stress−strain evolution between the MA and MI fiber, with the latter portraying a definite 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 that spiders will usually provide an extremely high friction-brake drawing force in efforts to quell the loss of such precious lifeline material, 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 an increase in crystalline region alignment and thereby potentially wipe 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 be seen in Figure 4 for both the MA and MI silks. Clearly there is an increase in failure stress, initial elastic modulus, and rupture energy with an increased rate of strain. Indeed, direct comparison of resulting low and high rate mechanical properties shows a clear increase with a rise in strain rate as seen in Figure 5. Regarding failure stress, there is a 70% and 40% increase for the MA and MI silks, respectively, while the initial elastic modulus increases 3-fold and 4-fold, respectively.

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

Most impressive is the increase in rupture energy, resulting in a 3-fold and 2-fold amplification for the MA and MI silks, respectively, upon increasing strain rate. Concerning failure strain, the MA silk exhibits a 60% improvement in value, while the rate dependency of MI failure strain is unclear. Comparison to High-Performance Fibers. In light of the nature of this study, it is worthwhile to discuss the similar characteristics exhibited by both of these structural spider silks and currently employed high performance fibers. Figure 6 shows a stress−strain plot depicting a few representative MA and MI silks tested at 1700 s−1 along with several single fiber Dyneema and KM2 fibers tested at 600 s−1. Immediately, four features become apparent. First, the elastic modulus and failure strength of the high performance fibers are much greater than the two tested spider silks. The high-performance fiber-tospider silk modulus and strength ratios are almost 10-fold and 3-fold higher, respectively. The former results in a drastic decrease in deflection exhibited by the high-performance fibers as compared to both spider silks during tensile loading and the latter of course results in the high-performance fibers being much stronger than both spider silks in the axial direction. Second, the elastic-plastic nonlinearity exhibited by both spider silks renders a nonrupture deformation cycle susceptible to permanent deflection, as opposed to the linear elastic response prevalent in both Kevlar and Dyneema fibers, wherein if loaded 2243

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Origin of Viscoelastic Properties. It is likely that the presence of this rate-sensitivity in the silk fibers has arisen due to the results of 400 million years of evolution.1 In order to survive, efficient web architecture may have evolved via both web geometry constraints and innate single fiber material cost.35 While some researchers have suggested that silk is optimized due to the evolutionary time scale, thereby acutely limiting possible improvements in biomimetic applications,36 it is much more likely that silk has been optimized for a variety of conditions, rendering each silk type suboptimal in some specific applications.2 Regardless, the cost of web production does affect the size and thread density of the web architecture, rendering depletion of silk material from the gland storehouses detrimental to the spider’s foraging capabilities.37 In light of the caloric expenditure needed for each web, it is reasonable to assume that thread development and web design have coevolved over time, introducing mechanisms to prevent web destruction. First, it is impractical for smaller sized spiders to produce extremely large webs capable of halting prey much larger than the spider itself while still ensuring that the web will not be utterly destroyed by prey. Thus, it is more advantageous for smaller spiders to build webs of reduced size, which can be constructed with a reduced risk of destruction.38 Second, it would be beneficial for a silk to exhibit mechanical properties dependent on strain rate, as this would allow for a prey size/ mass sorting mechanism. Ultimately, in collecting prey with a wide size and mass range, viscoelasticity would allow varying effects 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 ultimate strength of the web structure would preferably be lower than needed to capture large prey, preventing destruction of the web. In contrast, smaller prey, which can also impact the web in a range of varying velocities, would still be effectively captured if the web rupture energy was consistently greater than that needed to halt the smaller prey. As a comparison, if the web fiber was not rate-sensitive (e.g., Kevlar fiber), the maximum amount of stopping energy of the web structure would be constant. If a web was able to catch a smaller insect moving at a fast speed, then it may too allow for slow moving large insects to 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 due to a cutoff web rupture energy. As noted recently35 even if larger prey were caught, it appears that only a local area of destruction will occur, which can be repaired by the spider. It is also important to note the elastic-plastic response of the frame silk, as this deformation mechanism allows energy to be dissipated via heat during insect impact. In contrast, if the deformation response was purely elastic, incoming prey being stopped by the web would then experience a spring-back effect possibly catapulting the prey out of the orb-web entrapment.10 Fracture Surfaces. Due to the lack of conclusive findings regarding MA spider silk failure mechanisms under tensile loading, and because, to the authors’ knowledge, no analysis of MI fracture surfaces has been published, both silk types were broken in tension at two drastically different strain rates, and the resulting surface topographies have been inspected. For both rate extremes tested, the customary fracture contours consist of a rough texture with a relatively constant peak and valley distribution with no presence of a major defect causing ultimate failure. This globule-like surface undulation behavior,

Figure 6. Stress−strain curves of representative spider silks and highperformance fibers.

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

U=

σε 2ρ

E ρ

(1)

with σ, ε, ρ, and (E/ρ) representing fiber failure stress, failure strain, density, and elastic wave speed, respectively. (U)1/3 may then be used to compare the possible velocity (V50) at which a specific projectile will penetrate different armor systems. Although the increased failure energy characteristic of both MA and MI silks is impressive, resulting in a (U)1/3 prediction for the MA and MI silks of at least 780 m/s, the lack of axial stiffness cannot be outweighed from a deflection standpoint. During armor transverse impact, it is imperative that the magnitude of fabric deflection is as minute as possible in order to ensure the wearer’s bodily deformation is minimized. The drastically reduced stiffness of the tested spider silks as compared to the synthetic fiber renders the former material much less adept at minimizing bodily harm due to fabric deflection, even if it may be able to halt an oncoming projectile. It is also important to note that the previous determination of U assumes a linear elastic stress−strain response, being common in high-performance fiber testing, thus the previous (U)1/3 value may be overvalued as the elastic moduli of the silks reduce with increasing strain. Nonetheless, the remarkable characteristics of spider silk make it a superb structure for analysis and may unveil key fundamental aspects needed to better engineer currently employed high-performance fabrics. 1/2

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mode was uncovered during the typical quasi-static testing experience, while the latter was found during efforts to generate a kink-band surface defect, which is highly uncommon in spider fiber.45 In order to promote the evolution of kinks bands, a MA silk was folded on itself, and firm pressure was applied to the corner zone with thumb and index finger application. This sample was then gently pulled in tension and imaged via HRSEM, rendering a most unusual fibrillated fracture surface as seen in Figure 8B. Clearly, there is the presence of a fibrillated failure topography. Both of these fracture mechanisms, axial splitting and fibrillation, are commonly evidenced in highperformance fiber failure and are indicative of a highly fibrillar fiber architecture.42 It can be tentatively stated that if the presence of fibrils does exist, they possess a high degree of lateral bonding, which would explain the lack of kink-bands evidenced in all samples tested.45

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

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CONCLUSIONS

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AUTHOR INFORMATION

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 a very large increase in mechanical properties such as failure stress, initial elastic modulus, and rupture energy for both silk types upon increased testing strain rate. The latter mentioned material response (rupture energy), yields both silks several times tougher than high-performance fibers such as Kevlar or Dyneema. It is this deformation characteristic that has prompted spider silk to be of such great interest and it is postulated that this rate-sensitive mechanism has evolved in order to allow the orb-web to act as a selective prey filtration device. Analysis of fiber rupture surfaces have yielded commonly described globular topographies regardless of the testing strain rate and various unusual fiber breaking morphologies have alluded to a potential fibrillar microstructure.

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.

works alluding to the former11,39,40 and latter41 mechanisms of action. It is important to note that even though MA and MI silks exhibit a high degree of extensibility, ductile fracture is not required, as is the case with Lycra, which fails in tension at strains over 500% in a brittle fashion,42,43 albeit Lycra exhibits a strain hardening response.44 More importantly, in both MA and MI silks, the deformation sequence disperses the majority of the loading cycle energy via heat.10 In light of this and due to the minimal damage seen on the typical fracture surfaces, the point of ultimate failure most likely does not drastically alter the total energy dissipated during loading regardless of whether the ultimate failure is a more instantaneous brittle rupture or a progressive ductile process. This is also corroborated by the congruency exhibited by both the low- and high-rate resulting fracture topographies even though there is a very large increase in the energy needed to rupture both fiber types. Thus, the energy dispersion mechanisms incurred during the tensile loading 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 displayed both axial splitting and fibrillation rupture morphologies, which can be seen in Figure 8A,B, respectively. The former fracture

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was supported by the US ARMY PEO Soldier program. The first author would also like to thank the NDSEG fellowship for graduate research funding.

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REFERENCES

(1) Koover, Ecophysiology of Spiders; Springer-Verlag: BerlinHeidelberg, 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 8. Atypical fracture surfaces seen during: (A) MI silk low rate testing, and (B) MA silk fold-pull test. 2245

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dx.doi.org/10.1021/bm3003732 | Biomacromolecules 2012, 13, 2240−2246