Materials Science and Engineering C 31 (2011) 730–739

Contents lists available at ScienceDirect

Materials Science and Engineering C

j ourna l homepage: www.e lsev ie r.com/ locate /msec

Impact testing of structural biological materials

Steve Lee a, Ekaterina E. Novitskaya b,⁎, Brandon Reynante a, Joshua Vasquez a, Robert Urbaniak a,Tsukasa Takahashi a, Evan Woolley a, Luca Tombolato b, Po-Yu Chen b, Joanna McKittrick a,b

a Department of Mechanical and Aerospace Engineering, University of California, San Diego, La Jolla, CA 92093-0411, USAb Materials Science and Engineering Program, University of California, San Diego, La Jolla, CA 92093-0418, USA

⁎ Corresponding author. Tel.: +1 858 534 5513; fax:E-mail address: eevdokim@ucsd.edu (E.E. Novitskay

0928-4931/$ – see front matter © 2010 Elsevier B.V. Adoi:10.1016/j.msec.2010.10.017

a b s t r a c t

a r t i c l e i n f o

Article history:Received 19 March 2010Received in revised form 29 September 2010Accepted 24 October 2010Available online 30 October 2010

Keywords:Structural biological materialsDrop weight testCompositesImpact damageDelamination

Structural biological materials must be highly impact resistant, as appendages such as antlers and horns mustsustain repeated, seasonal impact loads. Determining the impact damage progression along with the impactstrength is very important for understanding hownature has optimized the structure and properties of biologicalmaterials in order to guide the designof superior bio-inspired syntheticmaterials. A dropweight test towerbasedon standards for testing fiber-reinforced polymer matrix composites was designed and fabricated toaccommodate the small size of biological materials. The materials tested were divided into two groups: non-mineralized and mineralized. The former demonstrated the highest impact strength and showed strongdependence onwater content, while the latterwere relatively brittle and demonstrated no dependence onwatercontent. Delamination was the most common damage mode observed for all biological materials tested.

+1 858 534 5698.a).

ll rights reserved.

© 2010 Elsevier B.V. All rights reserved.

Introduction

Many structural biological materials are considered to be compo-sites, typically consisting of crystalline nanofibers of structuralproteins or polysaccharides and a nanocrystalline mineral phase. Inbone, teeth and antler, the nanofibers are collagen, which arereinforced with hydroxyapatite, a calcium phosphate mineral. Innacre, the nanofibers are a polysaccharide, chitin, which (along withother organic materials) glue the calcium carbonate (aragonite) tilestogether. In horn, filaments of keratin in a three-dimensionalarrangement reinforce an amorphous keratin matrix [1,2].

These composites also possess a laminar structure at some level,making them akin to reinforced synthetic composite laminates. Fornacre in the abalone shell, the aragonite tiles are arranged in a brick-and-mortar structure, with layers 0.5 μm thick. In order for a crack topropagate, the tiles must pull-out from the abutting tiles. Thus, theinterfacial properties between the aragonite tiles and the organiclayer define the fracture resistance of nacre [3].

In the compact region of long skeletal bones and antler, circularlamellar structures are present. The lamella consist of orientedcollagen fibrils, ~300 nm long and 1.5 nm in diameter with~4 nm×100 nm hydroxyapatite dispersed between and aroundthem. The lamellae form concentric rings, called osteons, whichenclose the blood vessels that run longitudinally through the compactbone. In order for cracks to propagate in compact bone, they must

either travel through or around the osteons, and in tensile tests,osteon pull-out and delamination has been observed [4,5]. Theprimary difference between skeletal bone and antler is the mineralfraction: 30 vol.% for antler and 40–45 vol.% for skeletal bone.

In horns of the Bovidae family, laminates of ~4–8 μmin thickness arelayered parallel to the growth direction [1], as shown in Fig. 1. In theselaminates, crystalline keratin filaments ~7 nm in diameter (~60 vol.%[2]) reinforce theamorphousmatrix,with orientationsparallel andnon-parallel to the growth direction. Between the lamellae are tubules(~7 vol.%) that extend the entire length of the horn. These tubules areinteresting in that they form regions of natural delamination, a featurethat is avoided in synthetic laminated composites. Another unusualfeature is that the keratin filaments span the laminates [6], which isanalogous to synthetic fiber composites where cross-stitching of fibersbetween the lamina result in improved mechanical properties [7,8].

In the armadillo carapace, hexagonal bony tiles (osteoderms),covered by keratin, are held together by non-mineralized collagenfibers called Sharpey's fibers, as shown in Fig. 2(a). The bone plates havea circulatory blood system that attaches to the animal through veins.This unusual structure is similar to LAST® tiles used on tactical vehicles(Fig. 2(b)), which are hard ceramic hexagonal blocks covered by apolymer. This indicates that the armadillo shell should have excellentimpact resistant properties.

Besides having exceptional strength and stiffness, given their lowdensity, these biological composites must be highly impact resistant.The abalone shell defends the animal against predators, who attemptto break their shell, or from wave action that causes them to beheaved onto rocks. Antlers and horns undergo repeated seasonalimpact loads, with very few breakages observed in the wild. In the

Fig. 1. Hierarchical structure of the sheep horn. The horn is composed of keratin filament reinforced lamellae that have tubules between them. Modified from [1].

731S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

case of bone, impact resistance is important for activities such asrunning or jumping, but also for protection of internal organs, such asthe function of the ribs and the skull. Therefore, understanding howimpact resistance is achieved in these composites can lead to futuredesigns of bio-inspired materials.

Fig. 2. (a) hierarchical structure of the armadillo carapace. The carapace is composed of hexagheld together by Sharpey's fibers (non-mineralized collagen), and (b) LAST® tiles on an Ar

Impact testing of materials is performed to determine the amountof energy that can be absorbed during a suddenly applied force. Quasi-static fracture tests do not yield information about how a materialdeforms and fails during high strain rate loading. Impact propertiesare extremely important in designing new materials that are robust

onal bony tiles in the pelvic and pectoral shield that are covered by keratin. The tiles aremy tactical vehicle [24].

732 S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

and energy absorbent, but these properties are difficult to quantify.Impact testing is usually performed by Charpy or Izod test machines,originally designed to determine ductile–brittle transitions in metals.The Izod tests are comprised of a swinging pendulumwhich impacts anotched sample fixed in a cantilevered beam position with the notchfacing the hammer. The pendulum is rotated to a fixed height andreleased. From this, impact strength is determined as the absorbedimpact energy divided by the cross sectional area of the test sample.The Charpy test is similar in that it also utilizes a swinging pendulum.However, the notched test sample is placed in a three-point bendingconfiguration with the notch facing away from the pendulum. Impactstrength is determined the same as for the Izod test. Charpy and Izodtests most often assume a preexisting notch, which is not suitable fortesting composite materials [10].

An alternative method is the drop-weight test, in which a knownmass is dropped from a given height onto a flat, un-notched sample. Thedrop weight test is a more realistic test of what a structural biologicalmaterial would experience in the wild. One should keep in mind thatlocalized low-velocity dropweight impact testing should be consideredonly as a part of the larger impact event that occurs in nature.

The impactor is a short rod with a hemispherical cap, which isattached to the mass. Damage from a dropped impactor can manifestitself in delamination, matrix cracks and/or fiber fracture. Of these,delamination causes substantial decrease in strength and stiffness[11]. The energy of the impactor is expressed by:

E = mgh ð1Þ

Where E is the impact energy imparted to the sample, m is themass of the impactor, g is the gravitational constant and h is the heightfrom which the impactor is dropped.

Background

Most of the research done on impact strength of biologicalmaterials has been limited to bone. Kovan subjected a sheepmandibleto the Izod test and found the impact strength to vary between 4 and22 kJ/m2 along different sections of the mandible [12]. In a separatestudy, bovine tibia and humerus bones were found to have impactstrengths in the range of approximately 10–24 kJ/m2 [13]. They foundthat strength depended significantly on the formationmechanism andlocation of microcracks. The microcracks were found to cause a loss ofstrength up to 39% [13]. Several groups have investigated the highstrain rate impact behavior of elk antler [14], equine bone [15], andram horn [6]. It was found that cracks tended to propagate along thematerials' growth direction for elk antler and equine bone.

Unlike homogenous materials, a great deal of damage can occurwithin composites before it is even visible. This happens in the form ofmatrix cracking, fiber failure, and delamination within the composite,which can reduce the load carrying capacity of the compositesignificantly [16,17]. The effect on strength due to water content inthe matrix has also been studied by Takahashi [18]. Glass fiberreinforced composites were immersed in water for periods of 7, 60and 180 days and subsequently impact tested in order to comparestrength with ambient samples. They found that water had nosignificant effect on the impact strength of the composites [18,19].

Composite laminates subjected to impact testing can be charac-terized by a cone of damage with the tip at the point of impact and thebroader base projecting away from it [20]. It has been found thatmatrix cracking is the first damage mode, which can initiatedelamination due to propagating cracks along the interface [20].Carbon-fiber composites have been found to have brittle failuremodes [21,22]. This behavior can be modified by reducing porosity sothat failure instead occurs due to interlaminar shear, similar tocomposites based on glass or Kevlar fibers [21,22].

This paper reports on the deformation mechanisms and impactstrength of biological composites tested with a laboratory designeddrop weight tower built to accommodate small samples as dictated bythe geometrical restrictions of the bulk material specimens. This is thefirst report on the drop weight impact behavior of these materials.

Materials and methods

Drop weight testing of the biological specimens was carried outfollowingamodifiedASTMstandardD7136/D7136M-07 [9]. Normally,this standard is used for dropweight testing ofmultidirectional polymermatrix composite laminated plates with a rectangular free-standing(unclamped) area with dimension of 125 mm×75mm. Due to thedifficulty in preparing biological test samples of that size, amachinewasbuilt at a 1:5 scale as shown in Fig. 3(a). This reduced the crosshead'shemispherical impactor tip from 16 mm to 3.2 mm and the specimenfree-standing area to a circle of diameter 12.69 mm. The crossheadwithimpactor weighs 1.2 kg, which can be dropped from amaximum heightof 0.74 m formaximum impact energy of 8.7 J andmaximumvelocity of3.8 m/sec, making this a low velocity impact test.

The test specimens were prepared as 2 cm squares. They were cutwith a band saw or hacksaw and polished down with sandpaper to anappropriate thickness with the exception of the armadillo, which wasleft at its natural thickness due to difficulties in polishing it down. G10fiberglass [0/90] and oak plywood were tested for comparison. Thethicknesses of the different types of materials were chosen in order tobest simulate their respective natural dimensions while still allowingthe ability to extract a usable number of samples. Table I shows thethicknesses used for each type of material. 42 samples of armadillo, 15samples of abalone shell, 24 samples of ambient (air dry) bovinefemur bone, 24 samples of hydrated bovine femur bone, 23 samples ofelk antler, 45 samples of hydrated steer horn, 55 samples of ambientsteer horn, 25 samples of hydrated ram horn, 25 samples of ambientram horn, 40 samples of oak plywood, and 30 samples of G10fiberglass [0/90] were tested.

Bovine bone, ram horn and steer horn were tested in a hydratedcondition in order to mimic their natural conditions. The moisturecontent of horns on living animals is not clear, but itwas found that freshoryx horn has a moisture content of about 20 wt.% water [23]. Thehydrated bovine bone, steer and ram horns were prepared byimmersing the specimens already cut to size in deionized water for aperiod of 3 days and subsequentlyweighed. Thesewere then ovendriedat 105 °C for a period of 2 days and then weighed. The amount of waterretained in the hydrated samples is listed in Table I. For themineralizedmaterials, Table I also lists the volume fraction of the mineral.

The samples were oriented and impacted in such a way as tosimulate collisions in the natural world. The armadillo shell wasimpacted on the black keratin scales (top surface), perpendicular to theshell. The abalone was impacted onto the mother-of-pearl (nacre)surface, perpendicular to the shell. The steer and ramhorn sampleswerecut so that the lamellaewere oriented normal to the impactor, similar tocarbon fiber epoxy or fiberglass composites. The bovine femur and elkantler bonewere oriented so that the osteons in the compact bonewereperpendicular with the impactor. Table I summarizes the impactorientations for the all materials tested. Energy levels for all materialstestedwere chosen starting from the failure point, followedbygraduallyreducing impact energy at equally spaced intervals.

The impact strength was calculated according to:

En =E

ds·tð2Þ

Where En is the normalized impact energy, E is the impact energyas derived in Eq. (1), ds is the cover plate aperture diameter (Fig. 3(a)),and t is the thickness of the specimen.

Fig. 3. (a) schematic drawing of modified drop weight test tower and (b) major damage modes as illustrated in ASTM D 7136/D 7136 M [9].

Table IImpact orientation, specimen thickness, amount of water in the hydrated materials andmineral fraction for the mineralized samples. For the impact orientation A correspondsto the impact that was perpendicular to the shell, B corresponds to the impact that wasperpendicular to the materials' growth direction, and C corresponds to the impact thatwas perpendicular to the fiber direction.

Sample Impactorientation

Thickness,t (mm)

Water content(wt.%)

Mineralfraction(vol.%)

Normalizedfailure impactenergy (kJ/m2)

Armadillo A 3.5±0.6 9 43 18Abalonenacre

A 2.9±0.2 90 12

Bovinefemur

B 2.1±0.2 9 40–45 10

Elk antler B 2.9±0.1 15 30 58Ram horn B 2.1±0.2 10 71Ram horn(hydrated)

B 2.4±0.2 35 32

Steer horn B 5.1±0.4 9 99Steer horn(hydrated)

B 5.4±0.3 31 92

Fiberglass(G10)

C 3.1 182

Oak plywood(4-ply)

C 5.44 30

733S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

The failure impact strength was determined to be the point atwhich at least 50% of test samples began to fail. Failure here is definedas the puncture or complete fracture of the test sample. However, forthe armadillo, failure occurs when the impactor punctured throughthe joints, when one of the hexagonal tiles was punched out, or whenthere was fracture of one of the tiles.

Qualitative analysis is also important for impact strength testing,and different damage modes were identified by visual inspection ofthe impacted specimens. The damage modes defined for this studywere drawn from ASTM Standard D 7136/D 7136 M [9], as illustratedin Fig. 3(b).

Results

The results were analyzed using two categories: qualitative andquantitative. Qualitative results were obtained through visualinspection of damage surfaces by eye and optical microscopy.Quantitative results were obtained through the analysis of damagesurfaces and their relation to the impact energy.

Qualitative results

Figures of the major modes and progression of damage displayedby each group of samples are shown in Fig. 4–8. The abalone shell

Fig. 4. Abalone damage progression.

Fig. 5. Damage progression of (a–c) elk antler, and (d–f) bovine femur bone.

734 S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

Fig. 6. Damage progression (a–c) hydrated ram horn, (d–f) ambient ram horn, (g–h) hydrated steer horn, and (i–m) ambient steer horn.

735S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

behaved as a brittle material. The dimples in Fig. 4(a) and (b) were ofcomparable size. However, in Fig. 4(b) a very fine hairline crack isvisible opposite of the impact surface. This progressed immediately tocomplete fracture where the specimen shattered almost like glass intomany pieces with increased impact energy as seen in Fig. 4(c).

For the elk antler the impactor left a dimple on the impact surfacethat increased in diameter and depth with increasing impact energyseen in Fig. 5(a–c). The cracks that appeared at higher energiesformed along parallel with the osteons. At failure, the largest fracturedpieces of antler were also oriented parallel with the osteons as shownin Fig. 5(c). The impactor punctured the samplewith the only crackingand fractures occurring on the opposite surface while the specimenremained intact.

The impact properties of the hydrated and ambient bovine femurare nearly identical. The bone exhibited just a fewmodes of damage asshown in Fig. 5(d–f). Therewas dimpling, cracks and failurewhere thebone sample fractured into pieces. The cracks occurred parallel withthe orientation of the osteons. Bone developed delamination wherechips of bone separated from the surface opposite of impact.

Ram horn in its hydrated state is shown in Fig. 6(a–c). Dimplingwas the dominant damage mode until failure due to puncture. Inbetween, there was some minor cracking of the surface opposite theimpact surface. The development of damage in the ambient ram hornsamples is shown in Fig. 6(d–f). The major damage mode here wasshallow dimpling. Cracks and delaminations developed with increas-ing impact energy. At failure, the impactor punctured through the

Fig. 7. Armadillo damage progression. External (top) view showing (a) separation of the tile; (b) cracks between the tiles; (c) complete punch-out of a tile, and (d) fracture of a tile.

Fig. 8. Damage progression of oak plywood (a–c) and G10 fiberglass (d–g).

736 S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

Fig. 9. Impact damage histograms for: (a) armadillo (n=42), (b) abalone (n=15), (c) elk antler (n=23), (d) bovine femur (n=48), (e) ambient ram horn (n=25), (f) hydratedram horn (n=25), (g) hydrated steer horn (n=45), (h) ambient steer horn (n=55), (i) oak plywood (n=40), (j) G10 fiberglass (n=30). X-axis: normalized impact energy [kJ/m2]; y-axis:% specimens affected. The numbers above each bar denote the number of samples tested at that energy level.

737S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

10

12

18

28

30

58

71

92

99

182

0 50 100 150 200

Bovine femur

Abalone

Armadillo

Ram horn (hydrated)

Oak plywood

Elk antler

Ram horn (ambient)

Steer horn (hydrated)

Steer horn (ambient)

Fiberglass (G10) [0/90]

Normalized failure impact strength [kJ/m2]

Fig. 10. Bar graph comparing failure impact strength among the materials tested.

738 S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

sample, causing chips of the horn to fracture away from the surfaceopposite of impact (Fig. 6(f)). The chips produced in this mannerwerecircular and much thinner than the thickness of the test sample.

The hydrated steer horn exhibited the lowest number of differentdamage modes (Fig. 6(g–h)). The impactor tip only left a shallowdimple until a high enough energy was reached, at which point thespecimens were punctured through. Interestingly, the punctures didnot leave a through-hole. Instead, after dislodging the impactor fromwithin the specimen, the hole closed up and there was little evidenceof the damage as seen in Fig. 6(h).

The steer horn in the ambient condition showed all the damagemodes described in the ASTM standard [8]. For all impact energies, theimpactor left a dimple on the impact surface that increased in diameterand depth with increasing impact energy. Cracks and internal delami-nation began to occur around the same point, as seen in Fig. 6(i–j). Thesteer hornwas the onlymaterial inwhich internal delamination could beeasily identified by visual inspection due to its translucent nature. Thiswas followed by a combination of larger cracks and internal delamina-tion, as seen in Fig. 6(k). At the point of failure, the impactor puncturedpartway through the specimen and fragments of horn cracked away onthe opposite side.

The armadillo carapace exhibited the most unique modes ofdamage, as seen in Fig. 7. At lower energies, the keratinous scalescovering the osteoderm tiles chipped away leaving the osteodermexposed (Fig. 7(a)). The osteoderm tiles failed most often along theSharpey's fiber joints between tiles as shown in Fig. 7(b) and (c). Forthese cases, the osteoderm tiles broke away from their neighbors in aclean break along the perimeter. In the specimens where the tilesactually fractured, as in 7(d), the cracks propagated as far as the jointperimeter where they then stopped.

The oak plywood exhibited dimpling beginning at low impactenergies. Higher energy impacts produced partial delamination of thebottom surface with deeper dimpling visible on top. At the failurepoint, the impactor punctured through the top three layers and causesthe bottom to delaminate and crack away (Fig. 8(a–c)).

Of all the materials tested, the fiberglass exhibited damage in themost consistent manner. Up until the failure point, all samplesshowed dimpling with depths increasing with impact energy, asshown in Fig. 8(d–g). The impact damage propagated through thematerial and showed up on the underside as an opaque white circlecontrasting with the normally semi-translucent material. As theimpact energies grew higher, a slight bulge could be observed on thesamples on the bottom surface. Prior to failure, small cracks developedon the bottom surface before giving way to puncture and delamina-tion at the failure point (Fig. 8(f)).

Quantitative results

As stated previously, the impact strength is measured to be thepoint at which 50% of samples were deemed to fail, with failure beingdefined as puncture or fracture of the sample. Fig. 9 shows surfacedamage histograms for the materials tested describing the correla-tions between the impact energy (listed on the horizontal axis) andcorresponding failuremodes. Different damagemodes (dimple, splits/cracks, internal delamination, externally visible delamination, andfinal failure) are clearly shown for the all materials tested. The numberof samples tested for each energy level is superimposed on each barfor better understanding of the statistical reliability of the data. Thefailure impact strengths of the materials tested are compared inFig. 10.

Discussion

Biological materials that were used for this study could be dividedinto two categories: mineralized (hydroxyapatite or calcium carbon-

ate: armadillo carapace, abalone nacre, elk antler and bovine femurbones) and non-mineralized (keratin based: ram and steer horns).

Mineralized materials

It is difficult to determine the exact impact strength for thearmadillo carapace due to the unique manner of its failure. In mostcases, the hexagonal osteoderm tiles failed along the Sharpey's fibersthat join the tiles together. In the cases where the bony osteodermfractured, the cracks propagated only to the perimeter of thehexagonal tile on which they were started. This localization ofdamage is seen in both types of failure and is clearly seen in varioussamples shown in Fig. 7. The low strength and higher elasticity of theSharpey's fibers allow it to act as a damage buffer by stretching,bending, and absorbing impact induced cracks. Although thearmadillo carapace is much weaker than some of the other materialstested, it can maintain better structural integrity as a whole due to itsability to localize and arrest damage propagation.

The abalone shell did not exhibit significantly progressive stages ofdamage. Before complete failure, the shell developed hairline cracksthat were difficult to see with the unaided eye. This can be attributedto the microstructure, which consists of layers of carefully arrangedbrickwork of calcium carbonate [3]. The abalone shell showed brittlefracture and had the second lowest impact strength of 12 kJ/m2,showing that abalone shell is not naturally optimized for impact.

The elk antler exhibited the highest impact strength (58 kJ/m2)among the mineralized materials. Dimpling, internal cracks, delam-ination and failure were the main damage modes for elk antlersamples. The impactor tip penetrated through the entire thickness atfinal failure.

The bovine femur bone had a high mineral content (40–45 vol.%).The femur bone is much less elastic and progresses immediately fromcracking to brittle failure. Delamination was observed in both ambientand hydrated conditions. There was not a significant differenceobserved between the failure impact energy of ambient and hydratedconditions due to very low water content in the hydrated condition.

Keratin based materials

The hydrated ram horn has twice the impact resistance of the hornin the ambient condition. While tensile strength is higher in theambient state [1], once the horn has been hydrated the strain to

739S. Lee et al. / Materials Science and Engineering C 31 (2011) 730–739

failure increases greatly due to the plasticizing effect of water on theamorphous keratin matrix [2]. The increased toughness helps thehydrated material absorb more energy before failing.

The steer horn behaved like a composite laminate where a cone ofdamage caused by the impacts was visible. The translucency of thehorn samples made it possible to see the internal delaminationdamage through visual inspection. The shape of these delaminationswas always circular and increased in diameter with increasing impactforce and depth, finally reaching a maximum diameter which wasequal to the cover plate aperture. This characteristic canmost likely beattributed to the shape of the hemispherical impactor tip. Thehydrated samples exhibited fewer damage modes in comparisonwith the ambient samples, which are expected since ductile materialstypically display fewer, more predictable damage modes. Thehydrated samples also have a lower impact strength at 92 kJ/m2

compared to 99 kJ/m2 in the ambient state. Unlike the ambientsamples, the failure point for these specimens was deemed to bepuncture because the hydrated samples did not fracture. Cracks anddelaminations did not propagate to the full extent of the cover plateaperture (Fig. 6(g–h)). The hydrated steer horn showed a similarpattern of damage compared to the ambient steer horn (Fig. 6(j–m)).However, these damage modes manifested in fewer samples withdimpling being the most dominant.

Synthetic materials

The 4-ply plywood had impact strength comparable to that of ramhorn. The wood dimpled easily and only started to crack anddelaminate at impact energies higher than the brittle biologicalmaterials (bovine femur, abalone shell and armadillo carapace). Theimpactor penetrated through the first two and sometimes third layerbefore any damage, such as cracks or delamination, manifested in thebottom layer.

The fiberglass proved to be one of the strongest andmost consistentcomposite tested, as can be seen in Fig. 9(j). Each group of samplestested at the various energy levels exhibited nearly identical damagecharacteristics, which can likely be attributed to its synthetic nature.Cracks at the higher energies formed in linewith the fiberglass fibers. Atthe failure point where the impactor punctured through, the fiberglassseparated into a cross shape as seen in Fig. 8(g). This occurred in eachsample that experienced failure and is due to the [0/90] layup, sincefibersplitting occurred along the fiber direction for each ply and the plies areoriented perpendicular to one another. Unlike the biological materials,penetration through thematerial by the impactorwas a predictable andgradual process.

Conclusions

The impact properties of different biological materials were tested.The impact strengths were calculated and damage mode progressionswere discussed. For comparison, properties of several syntheticcomposites were also investigated. This is the first study to reporton impact properties of biological materials. The main findings are:

• A drop weight impact tester was designed and built based on amodified ASTM 7136/D 7136M-07 standard that was employedsuccessfully to test small biological material specimens.

• Biological materials have unique hierarchical microstructures anddid not show uniform impact behavior, indicative of multipledifferent energy mitigation mechanisms.

• Keratin basedmaterials (ram and steer horns) demonstrated a strongdependence on water content and had higher impact strengths than

mineralized materials, which is partially attributable to the fact thatthe presence of water led to increased ductility and strain-to-failure,thus delaying the occurrence of final failure.

• The mineralized materials (bovine femur bone, abalone shell, andarmadillo carapace) were the most brittle among the materialstested. No significant dependence onwater content was determinedfor these samples.

• The abalone failed as a brittle ceramic, and had one of the lowestimpact strength due to the high volume fraction of the mineralphase.

• Bone (bovine femur and antler) showed cracks that developedparallel to the osteons direction.

• Delamination was the main damage mode that occurred in all ofthese biological materials, due to large increase in surface areawhich represents an effective energy dissipation mechanism thataccomplished delamination.

Materials sources

The antler (elk, Cervus canadensis) and horns (desert big hornsheep, Ovis canadensis and bovine horn (Bos taurus) were purchasedfrom Into the Wilderness Trading Company, Pinedale, WY. The antler,from a large, mature bull, was shed approximately 1 year beforeobtaining the antler for testing. The horn is approximately 7 years old(determined by counting the annular rings). The abalone nacre wasfrom a fully grown (~15 cm in diameter) animal from the ScrippsInstitute of Oceanography. The armadillo osteoderm from a fullygrown armadillo was purchased from Jernigans Taxidermy, Waco, TX.

Acknowledgements

This work was supported by a UC-MEXUS Collaborative grant(2009–2010) and by a National Science Foundation grant (DMR0510138).

References

[1] L. Tombolato, E.E. Novitskaya, P.-Y. Chen, F.A. Sheppard, J. McKittrick, ActaBiomater. 6 (2010) 319.

[2] J.F.V. Vincent, Structural Biomaterials, 2nd edition, Princeton University Press,Princeton, New York, 19908 pp. 139–140.

[3] A. Lin, M.A. Meyers, Mat. Sci. Eng. A 390 (2005) 27.[4] P.-Y. Chen, A.G. Stokes, J. McKittrick, Acta Biomater. 5 (2009) 693.[5] M.E. Launey, P.-Y. Chen, J. McKittrick, R.O. Ritchie, Acta Biomater. 6 (2010) 1505.[6] J. McKittrick, P.-Y. Chen, L. Tombolato, E.E. Novitskaya, M.W. Trim, E.A. Olevsky, M.A.

Meyers, M.F. Horstemeyer, Mater. Sci. Eng. C 30 (2010) 331.[7] K. Dransfield, C. Baille, Y.-W. Mai, Comp. Sci. Technol. 50 (1994) 305.[8] A. Morales, Proc. 22nd Int. SAMPE Tech. Conf. 6-8 (1990) 1217.[9] ASTM Drop weight impact standard 7136/D 7136 M, Standard test method for

measuring the damage resistance of a fiber-reinforced polymermatrix composite toa drop weight impact event, ASTM, West Conshohocken, PA, 2005, pp. 434–449.

[10] H. Ku, Y.M. Cheng, C. Snook, D. Baddeley, J. Compos. Mater. 39 (2005) 1607.[11] S.W. Tsai, E.M. Wu, J. Compos. Mater. 5 (1971) 58.[12] V. Kovan, J. Biomech. 41 (2008) 3488.[13] G.C. Reilly, J.D. Currey, J. Biomech. 33 (2000) 337.[14] R.M. Kulin, P.-Y. Chen, F. Jiang, J. McKittrick, K.S. Vecchio, JOM 62 (2010) 41.[15] R.M. Kulin, F. Jiang, K.S. Vecchio, JOM 60 (2008) 39.[16] J. Morton, E.W. Godwin, Compos. Struct. 13 (1989) 1.[17] M. Freitas, L. Reis, Compos. Struct. 42 (1998) 365.[18] Y. Takahashi, J. Chai, S.W. Tan, Dent. Mater. 22 (2006) 291.[19] H. Morita, T. Adachi, Y. Tateishi, H. Matsumot, J. Reinf. Plast. Compos. 16 (1997)

131.[20] H.Y. Choi, R.J. Downs, F.K. Chang, J. Compos. Mater. 25 (1991) 992.[21] W.J. Cantwell, J. Morton, Compos. 22 (1991) 347.[22] A.V. Antonov, E.S. Zelenskii, A.M. Kuperman, J. Reinf. Plast. Compos. 22 (2003)

361.[23] A. Kitchener, J.F.V. Vincent, J. Mater. Sci. 22 (1987) 1385.[24] http://www.foster-miller.com/literature/documents/LASTGround.pdf#LASTGround.