biological materials science overview structural...

2008 June • JOM 23www.tms.org/jom.html

OverviewBiological Materials Science

How would you…

…describe the overall significance of this paper?

This paper presents a description of the authors’ latest studies of unusual structure/property relationships of various biological taxa.

…describe this work to a materials science and engineering professional with no experience in your technical specialty?

This paper is an overview of some of the structures and mechanical properties of natural biological materials.

…describe this work to a layperson?

This paper is an overview of the structure and strength of various biological materials such as seashells, crab exoskeletons, bird beaks, and deer antlers.

Through specific biological exam-ples this article illustrates the complex designs that have evolved in nature to address strength, toughness, and weight optimization. Current research is re-viewed, and the structure of some shells, bones, antlers, crab exoskeletons, and avian feathers and beaks is described using the principles of materials sci-ence and engineering by correlating the structure with mechanical proper-ties. In addition, the mechanisms of de-formation and failure are discussed.

IntroductIon

Thecompositionandstructureofin-organicandorganiccomponentswithinnature’sbiologicalcompositesisoftenintimately connected to the differentstructuralscalelevels,creatingahierar-chythatoptimizesstrengthandtough-nesswhileminimizingweightforspe-cificapplications.Thedamagemecha-nisms in biological materials are farmoresophisticatedthancurrenttechno-logical designs. One of the importantdifferencesisthatnaturedoesnothaveatitsdisposalthecornucopiaofstrongsynthetic materials developed in thepastcenturythatrely,forthemostpart,onhigh-temperatureprocessing.Thus,ingeniousdesignhastobecoupledwiththeabilitytochangeshapeandconfigu-rationduring the lifeof theorganism.Multifunctionality and self-healingability are inherent characteristics ofmanyof thesecomponents,whichen-suresurvivalinanenvironmentwherenatural selection constantly ‘tunes’them. TheArztpentahedron1showssche-maticallyhowthevariouselementsthatareuniquetobiologicalmaterialscon-tributetothestructures.Whilethestudyofthesebiologicalmaterialsperseisafascinating field with plenty of chal-

Structural Biological Materials: overview of current research

P.-Y. Chen, A.Y.-M. Lin, A.G. Stokes, Y. Seki, S.G. Bodde, J. McKittrick, and M.A. Meyers

lenges formaterialsscientists,materi-alsengineerslookatthemwithakeeneyeforthemultifunctionalityandhier-archical structure of these materialsthat is a matter of life or death.Thus,evolutionhasplayedandcontinues toplayapivotalroleinselectingthestruc-turesthatofferoptimumperformance.Indeed,naturalselectionandevolution-ary constraints constitute one of theverticesof theArztpentahedron.Thisarticlefocusesonafewstructuralbio-logical materials that are under studyby the authors. The materials scienceapproach that is illustrated here hasproventobeveryusefulandisreveal-ing features and properties heretoforenot studied by other fields. This briefarticlerepresentsthecontinuationofanearlier article published in JOM.2 M.Meyers et al. provided greater detailandanin-depthoverview.3

ShellS

While there are a great variety ofshells in the oceans and rivers, thisstudyhas focusedon theconch,4aba-lone,5–8theAmazonRiverclam,andgi-antclam.9Notablestudiesonshellsarethe early works by J.F.W. Vincent,10V.J.Laraiaetal.,11andM.Sarikayaetal.,12,13tonamejustafew.Therearesig-nificantcurrenteffortsfocusedonelu-cidating the fundamental mechanismsof deformation and failure from thenanometertothestructurallevel. Oftheshellsstudied,abalonewillbethe focus here. The abalone shell hastwo layers: an outer prismatic layer(rhombohedralcalcite)andaninnerna-creouslayer(orthorhombicaragonite).This inner layer has been intenselystudied because of its excellent me-chanical strength. Aragonitic CaCO

3

constitutestheinorganiccomponentofthenacreousceramic/organiccompos-ite (95wt.%ceramic,5wt.%organicmaterial).Thiscompositeiscomprisedofstackedplatelets(~0.5µmthick)ar-ranged in a brick-and-mortar micro-structurewithanorganicmatrix(20–50nmthick)interlayerthatistraditionallyconsideredasservingasgluebetweenthesingleplatelets.Thereisahighde-greeofcrystallographictexturecharac-terized by a nearly perfect “c-axis”alignment normal to the plane of thetiles. Figure1shows(a)anabaloneshell,(b)itsmesostructure,and(c)itsmicro-structure. The mesostructure (Figure2a)ischaracterizedbythepresenceoforganic mesolayers which are due togrowth cycle interruptions. These or-ganiclayersarethemselvespermeatedwith mineral, as shown in Figure 2b.Theprincipalfeatureofthemicrostruc-tureisthestackingoftileswithdimen-

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JOM • June 200824 www.tms.org/jom.html

sions of 0.5 µm thickness and~10µmdiameter.Itwillbeseenbelowthat they are connected by mineralbridgesthatplayapivotalroleinme-chanicalstrengthandensuregrowthinaquasi-monocrystalmode;subsequentlayers have the same crystallographicorientation,asseeninFigure3.Figure3 illustrates that the crystallographicorientationofadjacenttilelayersisthesame. Similar transmission-electronmicroscopy (TEM) results had beenobtainedearlierbySarikaya.13

The determination of the shellstrength when the loading is appliedperpendiculartoitssurfacecandirectlyaddresstheroleplayedbytheorganiclayer.Adramaticdifferenceinstrengthisfoundbetweenthetensileandcom-pressivestrengths,muchgreaterthaninconventionalbrittlematerials.Theratiobetween compressive and tensilestrengthisontheorderof50,whereasinbrittlematerialsitvariesbetween8and12.Thisdifferenceisindeedstrik-ing,especiallyifoneconsiderstheten-silestrengthparalleltothelayerplane;itisontheorderof150–200MPa,onethirdofthecompressivestrength.Itcanbe concluded that the shell sacrificestensilestrengthintheperpendiculardi-rectiontothetilestouseitintheparal-leldirection.Interestingly,theaverageof the tensile strength (in the perpen-dicular and parallel directions) is ap-proximately75–100MPa,whereasthecompressivestrengthisapproximately500 MPa. This is much closer to the‘normal’ value for the ratio betweencompressiveandtensilestrengthofce-ramics.Figure4showsinaschematicfashion the compressive and tensilestrengths collected from a variety of

past studies,5,12–16 both perpendicularandparalleltotheshellsurface.Thera-tiobetweenthecompressiveandtensilestrengthsparalleltothesurface,3:5,ismuchsmallerthanthatcharacteristicofceramics. Figure 5 shows, in schematic fash-ion,thefailuremechanismsofabalone

shells in different loading conditions:(a)tensionparalleltoshellsurface,(b)shearparalleltoshellsurface,(c)com-pression parallel to shell surface, and(d) tensionperpendicular to shell sur-face.When tension is appliedparalleltothesurface,thetilesslidepasteachotherratherthanfracturing.Themech-

Figure 1. The hierarchical structure of abalone nacre. (a) An abalone shell, (b) its mesostructure, and (c) the aragonite tiles of its microstructure.

a b c

Figure 3. A TEM of aba-lone nacre tiles show-ing that crystallographic orientations of adjacent tiles in the same growth stack are identical.

Mesolayers

AragoniteTile Region

250 µm20 µm

A

A

BC

D

E

a b

Figure 2. (a) A macrostructural view of a cross section of the Haliotis rufescens shell. Growth bands are observed separating larger regions of nacre. (b) An SEM micrograph of polished surface of mesolayers. Tiles (A): block-like calcite (B): organic/inorganic mix (C): organic (D): and spherulites (E) are observed.


6

5

4

3

2

10 100 200

Diameter of Mineral Bridge (nm)

Max

imum

Stre

ss σ

max

(GPa

)

300 400 500 0 20

250

200

150

100

50

040

Diameter of Mineral Bridge (nm)

Num

ber o

f Min

eral

Brid

ges

Per T

ile (n

)

60 80 100

anismoffailureinvolvesfractureofthemineral bridges and stretching of theorganic. Upon compression parallel to theplane of the tiles, an interesting phe-nomenon observed previously in syn-thetic composites was seen along themesolayers:plasticmicrobuckling.Thismodeofdamageinvolvestheformationofaregionofslidingandofaknee.Fig-ure 6a shows a plastic microbucklingeventinanAmazonRiverclam.Plasticmicrobuckling,which isamechanismto decrease the overall strain energy,wasobservedinasignificantfractionofthespecimens.Plasticmicrobucklingisacommonoccurrenceinthecompres-sive failure of fiber-reinforced com-positeswhenloadingisparalleltothereinforcement.Thecoordinatedslidingoflayersegmentsofthesameapproxi-matelengthbyashearstrainγproducesanoverall rotationof the specimen inthe region with a decrease in length.Figure6b showsacharacteristicmicro-bucklingregionfoundinabalonenacre.Theangleαwasmeasuredandfoundtobeapproximately35°.Theidealangle,which facilitates microbuckling ac-cordingtoArgon,is45°.17

Thelowtensilestrengthisthedirectresult of the growth process, whichinvolvestheperiodicdepositionofor-ganiclayersthatreducethevelocityofgrowthinthecdirectionoftheortho-rhombicaragonitestructureandcreatethetilestructure.Itispossibletoesti-matethetensilestrengthofeachindi-vidualmineralbridgeandtocalculatethe overall tensile strength, from thedensity of these bridges. The mineralbridgeshavediametersinthenanome-

Figure 4. The compressive strength and ultimate tensile strength of nacre with respect to loading direction.

Equations

(1)

(2)

(3)

(4)

(5)Figure 7. (a) The tensile strength of mineral as a function of size; (b) the calculated number of mineral bridges per tile as a function of bridge diameter.

a b

a b

Figure 6. (a) A plastic microbuckling event in an Amazon River clam; (b) a characteristic microbuckling region found in abalone nacre.

Figure 5. Failure mecha-nisms of abalone shells in different loading con-ditions: (a) tension par-allel to shell surface, (b) shear parallel to shell surface, (c) compres-sion parallel to shell surface, and (d) tension perpendicular to shell surface.

nA

At T

th B

=σσ

fnA

AB

T

=

f t

th

=σσ

σ th

E=30

σπfr

IcK

a=

terrange(~50nm).Usedhereisanex-tensionof theapproachintroducedbytheMaxPlanck Institute (H.J.Gaoetal.,18B.H.JiandGao,19andJietal.20)for biological materials. The classicalfracturemechanicsequationisapplied

toaragonite.Themaximumstress,σfr,

as a function of flaw size, 2a, can beestimated, to a first approximation,as shown in Equation 1, where K

Ic is

the fracture toughness. (All equationsare given in the table.) However, the

a b

c d

20 µm

Microbuckling

α

q

s


strength is also limited by the theo-retical tensile strength, which can beapproximated as Equation 2 (Gao etal.18). WeassumethatK

Ic=1MPa▪m1/2,E=

100GPa,andthat2a=D,whereDisthespecimendiameter.Figure7ashowsthe two curves given by Equations 1and 2. They intersect for a = 28 nm(D=56nm).Thisisindeedsurprising,and shows that specimens of this andlowerdiametercanreachthetheoreti-calstrength.Thisisinagreementwiththe experimental results: the holes intheorganiclayerandasperities/bridgediametersarearound50nm.Itispos-sibletocalculatethefractionofthetilesurfaceconsistingofmineralbridges,f.Knowingthatthetensilestrengthisσ

t

andassumingthatthebridgesfailatσth,

wehaveEquation3. The number of bridges per tile, n,can be calculated from Equation 4,whereA

Bisthecross-sectionalareaof

eachbridgeandA

Tistheareaofatile,

resultinginEquation5. Assumingthatthetileshaveadiam-eterof10μmandthatthebridgeshaveadiameterof50nm(theapproximateobservedvalue),oneobtains,forσ

t=3

MPaandσth=3.3GPa,n=36asrepre-

sentedinFigure7b.Thisresultstronglysuggests that mineral bridges can, bythemselves, provide the bonding be-tweenadjacenttiles.

Thenumberofasperitiesseeninsur-facesoftilesgreatlyexceedsthevaluesforbridgescalculatedherein.Theesti-mateddensity is60/µm2.Oneconclu-sion that can be drawn is that a largenumberofasperitiesareindeedincom-pletebridgesandthatthesebridgesarea small but important fraction of theprotuberances.

craB exoSkeletonS

Arthropods are unique in that theyhaveanexoskeleton,andnotanendo-skeletonlikefishes,reptiles,andmam-mals.Thisexoskeletonisamultifunc-tionalbiologicalcomposite:itservesasattachment to the muscles, exchangesfluidswiththeenvironment,andoffersprotectionagainstpredators.Incrusta-ceans (e.g., sheep crab studiedby theauthors21andtheMainelobsterstudiedby the Max Planck Düsseldorfgroup22–26)theprimaryconstituentsarechitin,proteins,andminerals. In the horseshoe crab from whichcrustaceans evolved (this species hasexisted for200millionyears) there isanabsenceofmineralizationandthere-forethestrengthoftheshellisconsid-erablylower.Figure8showsthehierar-chical structure of horseshoe crab(Limulus polyphemus) exoskeleton.Theexoskeletonofhorseshoecrabsisasandwichcompositeconsistingofthreelayers:anexteriorshell,anintermedi-

Figure 8. The hierarchical structure of the horseshoe crab exoskeleton.

80

70

60

50

40

30

20

10

00.00 0.02 0.04 0.06 0.08 0.10 0.12

Strain

Stre

ss (M

Pa)

0.14

Figure 9. A typical stress-strain curve for American kestrel primary feather rachis is depicted. The data that appear in black are those used in determining Young’s modulus.

atelayer,andaninteriorcore.Theex-teriorshellofahorseshoecrabissimi-lar to crab exoskeletonswithnomin-eralpresence.Beneaththeexteriorshellis an intermediate layer consisting ofvertical laminate about 2−3 μm widethat connects the exterior shell to theinterior core.The interior corehasanopen-cellfoamstructureandishollowin themiddle.Thecellularnetwork isakintotheinteriorstructureoftoucanandhornbillbeaks,asdescribedinthefollowingsection.Oneofthefascinat-ing aspects of horseshoe crabs is thatthebloodcellsdonotcontainironbutcopper;thus,theyaretruebluebloods.Their blood is harvested and used to


a b

Figure 10. Scanning-electron micrographs showing (a) the fracture surface of the American kestral primary feather rachis. Cleavage of the cellular solid is observed on ventral side of the rachis. (b) The mean diameter of honeycomb cells is approximately 20 µm.

Figure 11. The structure of exterior beaks with scanning-electron micrographs of (a) toucan beak keratin and (b) hornbill beak keratin.

a

a

testbacterialendotoxinsinpharmaceu-ticalandbiomedicalindustries.

avIan FeatherS and BeakS

Intherecenttrendtowardbiomimet-ics,engineershaveturnedtowhathasattracted experimental biologists fordecadesalready:avianappendages.Y.Sekietal.27describedthebillofaTocoToucan (Ramphastos toco) as a sand-wich-structured composite, consistingof a closed-cell foam encased by thiskeratinous shell (ramphotheca). Thismodelwithinputsfromdatacollectedby tension and compression tests aswellashardnessdatawasusedtosimu-latethestructureinflexure,forwhichfoam-filledstructuresareoptimized. Previousandongoingstudiesrevealanalogousstructureinthefeathershaft(rachis). P. Purslow and J. Vincent28havequantifiedthemorphologyofpri-maryfeatherrachisofpigeon(Colum-balivia)andinthecontextofmechani-calproperties.Consistentwiththemo-tifofcellularsolidencasedbycornifiedexterior,thefeatherrachisconsistsofamedulla foamenclosed in a relativelythin keratinous cortex. The medulla(Figure10)canbedescribedasahon-eycomb structure. Based on prelimi-nary analysis of micrographs, cell di-ameter is estimated to range from 10µmto30µm. Sections ranging in length from1–2cmhavebeenexcisedfromprima-ryremigesofasinglespecimenoftheAmerican Kestrel (Falco sparevirus).Tensile testing isconductedatafixedstrainrateof0.11/min.(1.83×10–3/s,corresponding to A. Taylor et al.29Basedonpreliminaryresults,therachisof American Kestrel has a Young’smodulusofapproximately1GPawithultimate tensile strength ranging from40MPato90MPa.Figure9isrepre-sentative of the mechanical response.Figure10aandbdepictscanning-elec-tronmicrographs(SEM)ofthefracturesurface corresponding to the data ofFigure9. Beaksarecomposedofaningenioussandwich structure and achieve ultra-lightweightconstruction.Thefaceskin,ramphotheca, is made fromβ-keratin,which maintains a certain stiffnessmainly for food gathering and func-tionsasaprotectivebarrierfromnatu-

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ral environments. The internal foamcoremadefromboneisanextensionofabirdskullandisusuallyhollowatthecenter.The twoentitiesareconnectedbythedermis.Mostbeaksareshortandthickorlongandthin.Thetoucanandhornbillbeaksareunique;theyarebothlongandthick.Thetoucanbeakis1/3of the total lengthof thebird and thehornbillbeakis1/4ofthetotallength.Theuniquepropertiesofthetoucanandhornbill beaks motivated a recentstudy27,30andwereinvestigatedinrela-tiontostructureandmechanicalprop-erties.Inpreviousstudies,themechan-icalpropertiesoftheTocotoucanbeakhavebeen investigatedwithanalyticalmodelsinambientcondition.Thefiniteelement method is used to model themechanical responses of the beak in-cluding the synergistic effect betweenthe external shell and foam core. Theauthorshavefurtherevaluatedthestruc-tureofbeakswithcomputedtomogra-phy and the mechanical properties oftoucan beak keratin at high humiditycondition. Figure 11 shows photographs andscanning-electronmicrographsofTocotoucanandwreathedhornbillbeakex-teriors. Both beak keratins consist ofmultiple layers of keratin tiles. Thetoucan ramphotheca surface is con-structed from a homogenous distribu-tionofkeratintiles.Thediameterofthetileis~45µmandthethicknessofthetileis~1µm.Thegeometryoftilesispolygon and symmetric. Three typesof ramphotheca surface are observedin the hornbill exterior keratin. Thesmoothsurfaceisdetectedonhornbillramphothecaandissimilartothetou-canramphothecasurface.Thetilehasa

somewhat elongated shape and alignsinacertaindirection. Thekeratintilestructureoncasque,aprojectiononmaxillary,isnotdistin-guishableand individual tile is tightlyconnectedormergedwithneighboringtiles.Ontheridgesurface,theconnect-ingglueisobservedinthekeratintileboundary region. The protruded gluedifferentiatessurfacemorphologyfromtheothertwosurfaces. Themechanicalpropertiesofmam-malian keratins are highly influencedby their moisture content.31–33 In thecaseofaviankeratins, thestiffnessoffeathers and claws at high humidityconditions significantly decreases.34Thetypicaltensilestress-straincurvesoftoucanbeakkeratinundertwocondi-tions(23ºCand45%relativehumidity(RH),38ºCand95%RH)areshowninFigure12.Underthelowhumiditycon-dition,theYoung’smodulusoftoucan

keratin is isotropic in both directions,rangingfrom1.04±0.06GPa(longitu-dinal)to1.12±0.13GPa(transverse).Thetensilestrengthoftoucanbeakker-atininthetransversedirectionwasap-proximately32%higherthaninlongi-tudinaldirectionshowninFigure12a.The strength of toucan beak keratinsignificantly decreases under the highhumidity condition shown in Figure12b.Theelongationat95%RHexhib-its approximately twofold higher thanat45%RH.Thevariationinstrengthinlongitudinal and transverse directionsismoredistinctiveunder thehighhu-midity.Theaveragestrengthis16.7±2.2MPa in longitudinal direction and31.0±4.4MPaintransversedirection.TheYoung’smodulus is0.093±0.02GPa (longitudinal) and 0.17 ± 0.003GPa (transverse). The stiffness in thehigh humidity condition drops by ap-proximately an order of magnitude.Themassofhydratedkeratin increas-es~10%for5hoursofexposureunder95%RHcondition,whichsignificantlydecreasesthemechanicalpropertiesoftoucanbeakkeratin. Thetoucanandhornbillfoamcoresconsist of a closed-cell foam. Thethinmembranescover individualcellscomposed of bony rods (trabeculae).Thetypicalcellsizeoftoucanfoamis~1 mm and that of hornbill foam is~3 mm. The foam core increases themechanical stability especially in thebendingandenergyabsorptioncapac-ityofthebeak,includingthesynergismbetweentwocomponents.Thetrabecu-

a bFigure 13. Three-dimensional models of beak foams; (a) toucan foam, (b) hornbill foam with keratin exterior.

Figure 12. The stress-strain curves of toucan beak keratin; (a) 45% RH and 23ºC condition, (b) 95% RH and 38ºC condition.

a b

140

120

100

80

60

40

20

00.350.30.250.20.150.10.050

Strain

Stre

ss (M

Pa)

0.70.60.50.40.30.20.10Strain

4035302520151050

Stre

ss (M

Pa)


lae of the toucan and hornbill are ar-rangedinacomplexmannerandhavehighhardnessincomparisonwithbeakkeratin.ThemicrohardnessorVickershardness of toucan and hornbill kera-tinsis0.22±0.02GPaand0.21±0.07GPa (smooth surface), respectively, atatmosphericcondition.Themicrohard-nessof toucanandhornbill foamma-terials is 0.28±0.04GPaand0.39±0.01GPa.Themicrohardnessofhorn-bill trabecula is comparable to avianbone.35 The beak foams collapse in abrittlemannerandfailbythebucklingofrodsincompression. Thecomplexfoaminteriorstructureis reconstructed by the three-dimen-sional (3-D) visualization techniques.Theauthorshaveused200imageslicesfrom micro-computed tomography at93 µm resolution. Digital Data View-erandVisualizationToolkitwereusedto generate isosurface mesh by usingamarchingcubealgorithm.36TheDI-COMformatofimagesisconvertedto.tiffformatbyImageJ.Inthisstudy,theauthorstookhalfthesizeoftheorigi-nalimagedataset(hornbill,505×555,andtoucan,450×505)anddoubleditssize in the visualization process. Fig-ure13showsthe3-Dstructureoftou-canandhornbillfoams.Forthetoucan,1,372,890 mesh elements and for the

hornbill, 1,799,760 were used to cre-ate the contour surface. The exteriorof the toucan is eliminated and onlybonyfoamisreconstructed.Thehorn-billfoamincludesexteriorkeratinandasecondaryhollowisobservedbetweenbonyfoamandcasque,showninFigure13b.Themodelsclearlyshowthehol-lowstructureoffoamcores.Thebeakfoams consist of a thin-walled struc-

turewithaninterconnectednetworkofthe rods.Themembranesdisappearedfromthemodelsduetothelowinten-sityofthemembranesincomputedto-mography(CT)images.

antlerS and BoneS

Antlersareoneofthemostimpact-resistant and energy-absorbent of allbiomineralizedmaterials.Theyareoneof the fastest-growing tissues in theanimal kingdom,growing asmuch as14kgin6months,withapeakgrowthrateofup to2–4cm/day.36Theantleristheonlymammalianbonethatisca-pable of regeneration, and thus offersunique insights into bone mineraliza-tionandgrowth.Antlershavetwopri-mary functions: they serve as visualsigns of social rank within bachelorgroups37–40 and are used in combat,bothasashieldandasaweapon.37Theantlershavebeendesignedtoundergohigh-impactloadingandlargebendingmomentswithoutfracture.Theunusu-alstrengthofantlersisattestedbytheveryfewobservationsofantlerbreak-ageduringfighting in largegroupsofcaribouandmoose.38Figure14showsthe aftermath of one battle, in whichonebulldiedfromexhaustion/dehydra-tion(notwounds).Theantlersbetweentheliveanddeadbullsweretightlyin-terlockedsothattheliveanimalcouldnotfree itself,evenbyrepeatedpush-ingandtuggingwith~400kgofbody

a

b

Figure 14. Two elk bulls in Utah with antler locked after a fight. The downed animal died from exhaustion/dehydration. The photographer had to saw off the dead elk’s antlers to free the live one. It is estimat-ed that 10% of the bulls die during a battle. Photos cour-tesy of Prof. John Skedros, University of Utah.

Figure 15. The hierarchical structure of antlers.


growingfawnskeletonsthattake~34g/day.41Thisquantityofmineralscannotbeobtained through food sourcesandhasbeenshowntocomefromtheskel-etonoftheanimal.36,41,42Thelongbonesofthelegsandtheribsaretherichestsource, and are found to decrease indensityastheantlersincreaseinsize.42Thus,structuralboneresorptionoccursalongsideantlerboneremodelingdur-ingantlerogenesis.Anotherdifferenceisthatantlersarelessmineralizedthanbone,andareoneoftheleastmineral-izedofallbiomineralizedtissue.43

Figure 15 shows the hierarchicalstructure of antlers. Antlers contain acore of trabecular (cancellous) bonesurroundedbycompactbonethatrunslongitudinally through themainbeamof the antler and the prongs. The tra-becularboneissomewhatanisotropic,with aligned channels directed paral-leltothelongaxisoftheantlerbeam.Compactbonesurroundsthiscore,con-sistingofosteonsthathavealaminatedstructure of concentric rings extend-ing from the main vascular channel.The concentric rings contain alignedcollagen fibrils that have the mineral,hydroxyapatite (or more specificallydahllite), dispersedonorbetween thefibrils. The alignment of the collagenfibrils changes direction between theindividuallamellae. Acrosssection,perpendiculartothegrowthofanantlerfromanAmericanelk,isshowninFigure16,identifyingthefourmainregionsradiatingoutwardfromthecenter:cancellous,atransitionzonebetweencancellousandcompactbone, compact bone, and the subvel-vet.44 Optical micrographs show thesubvelvettobe100–150µmthickwiththe transition region to compact bonenotableforthelowdensityofosteons.

Table I. Summary of Mechanical Properties of North American Elk Antler Compared to Bovine Femur

Property Elk Antler Ref. Bovine Femur Ref.

Density (g/cm3) 1.72 55 2.06 47

Mineral Content (% ash) 54.8 55 67 47

Porosity (%) 9.1 55 5.8 48,49

Elastic Modulus (GPa) 7.6 56 13.5 47

Bending Strength (MPa) 197 56 247 47

Compressive Strength (MPa) 126 56 254 57

Fracture Toughness (MPa.m1/2) 11.0 56 2.1–5.2 58–60

Figure 16. An antler cross section showing optical micrographs of the (a) subvelvet/compact interface, (b) compact, (c) transition (compact to cancellous) zone, and (d) a SEM micrograph of the cancellous bone.

mass.Theantlersfromthedeadanimalhadtobesawedofftofreethelivebull.Antlersaredeciduousandarecastoff(dropped)attheendoftherut,thustheageofthecastantleris~7–9months. Antlershaveacompositionandmi-crostructureverysimilartoothermam-malianbonesbuttherearedistinctvari-ationsduetothefunctionaldifferencesbetween the tissues. Bones providestructuralsupportandprotectionofor-gans whereas antlers provide neither.Given the long,slenderappearanceofmostantlers,thenaturalcomparisonistomammalianlongbones.Longbonesare hollow and contain interior fluids(blood, marrow, etc.). Bones producevital cells and minerals necessary forthebodywhereasantlersremovefluidsandmineralsfromthebodyinordertogrow. Antlerogenesis (antler growth)

requiresalargeamountofcalciumandphosphorus in a short period of time.Red deer (Cervus elaphus, a Europe-an deer almost identical to the NorthAmericanelk,Cervuscanadensis)ant-lersrequire~100g/dayofbonemate-rial inordertogrowincomparisonto

1 cm

500 µm

a

b

c

500 µm

d

Cancellous

Transition Zone

Subvelvet/Compact

Compact


Movingfromthecompactbonetothecancellous bone shows an increase inthe sizeof theporosity,with theporesizerangingfrom300µmatthecom-pact/cancellous interface to severalmillimetersattheinteriorofthecancel-lousregion.Thevolumefractionofthecancellousboneis~0.4ofthetotalvol-ume. Figure17showsopticalmicrographsofcrosssections takenfromthecom-pact bone of the antler and a bovinefemur.Theantlershowsosteons(100–225 µm diameter), Volkmann canals,vascular channels (15–25 µm diame-ter),andlacunaespaces(~10µmdiam-eter), as indicated on the micrograph.Themajorityof theosteonsappear tobealignedalongthegrowthdirection.Dependingontheageofthebone,hu-manosteonsrangefrom200–300µm,substantiallylargerthanwhatisfoundin the antler.This is likelydue to theage difference between the reportedvaluesforhumanbone,typicallytakenonadults,asopposedtowhatisfoundintherelativelyyoungantler. Twotypesofosteonscanbepresentin bone: primary and secondary. Pri-

maryosteonscontainvascularchannelssurroundedbyconcentricbone lamel-lae. Primary osteons are generallysmaller,donothaveacementlinesur-rounding them and are embedded inlayersof interstitialorcircumferentialbone.Thecementlinehasbeenshownrecentlytobemineralrich,incontrastto earlier conclusions that the region

wasmineralpoor.45Secondaryosteonsresultfromboneremodelingandoftenintersect each other and have a morerounded, uniform shape than primaryosteons. J.D. Currey and others havepointed out that primary osteons arestronger than secondary osteons.46,47We could not completely distinguishbetween the two types in the micro-graph,howeverthemajorityappeartobeprimaryosteons,sincetheyshowasomewhatdistortedcrosssection.Sec-ondaryosteonsoftenariseinresponsetomechanicalstress.Becauseanantlerdoes not undergo mechanical forcesduring the growth process and onlyspends 1–2 months in sporadic (if atall)combat,itseemsunlikelythatsec-ondary osteons would be present in alargeamountinantlers.Theantlerpo-rosityisestimatedtobe~9.1%byvol-ume, counting the vascular channelsandlacunaevoidspaces. Theosteonsinthebovinefemuraremoresparselydistributedcomparedtothoseintheantlers.Theseappeartobesecondaryosteons,given theuniform,circular shape of the majority. Theseosteonsareembeddedinparallelfiber(interstitial)bone,whichiscontinuallyremodeledtoformsecondaryosteons.Several elongated pores are observed,whichactuallyaresectionsoftheVolk-manncanals,alsoappearingintheant-lermicrograph,alongwiththelacunae.Thevoidspaceisestimatedtobe5.1%,in agreementwith a porosityof 5.8%measured in other bovine femora.48,49The interstitial bone has a higher

Figure 18. A scanning-electron micrograph of the fracture surface of a longitudinal speci-men broken in bending, showing the fibrous nature of the fracture.

Figure 17. Optical micro-graphs of cross sections taken from the compact bone of (a) an antler and (b) a bovine femur. The antler shows osteons (Os), Volkmann canals (Vo), vas-cular channels (Va), and lacunae spaces (L).

b

a

OsL

Va

Os

L

Vo

Va

Vo


strengthandelasticmodulusthansec-ondary osteonal bone,50 with an aver-age modulus of ~27 GPa for mixedbone,similar towhatwasreportedbyothers.51,52Inthefemur,~41%byareaarethesecondaryosteons. While the mechanical propertiesofhumanandbovinebonehavebeenhighly documented, little data existson the mechanical properties of ant-lers. North American elk antler wasput through a variety of tests (bend-ing, compression, and fracture tough-ness)todeterminevariousmechanicalproperties.Theresultsofthesetestsarecomparedtoknowndataofbovinefe-mur, summarized inTable I.The ant-ler showed smaller values of density,amountofmineralization,elasticmod-ulus, and strength; however, the ant-ler had a higher fracture toughness.The elastic modulus and strength ofbonescaleswiththemineralcontent,53which is consistent with the resultspresented here. The interstitial bonehas a higher elastic modulus than thesecondary osteons.52,54 Thus, althoughprimary osteons have a higher modu-lus thansecondaryones, theyarestillnot as stiff as interstitial bone, whichiswhytheantlerhasalowermodulus.The higher fracture toughness of ant-lerscorrelatestotheirmainfunctionofhavinghighimpactresistance.Thede-creaseinstrength,however,isrelativelysmallwhenconsideringthemuchfastergrowthrateofantlers.Thefracturesur-faceofanantlerspecimenfracturedinthree-pointbendingisshowninFigure18. The fibrous nature of the fracturesurface is observed, showing pulloutof the osteons. The bending samplesdidnotfracturecompletely;theyfailedgracefullywithalargestraintofailure,similartoafiber-reinforcedcomposite.

acknowledgeMentS

We gratefully acknowledge support from Professor Falko Kuester, Jackie Corbeil for CT scan, and Evelyn York for scanning electron microscopy. The curator of birds at the San Diego Zoo’s

Wild Animal Park kindly provided us with hornbill beaks. Mr. Jerry Jennings, owner of Emerald Forest Bird Gardens, has helped us immensely with the tou-can beaks. We thank Project Wildlife for cooperation in providing specimens of American Kestrel for this study. We also thank Prof. Paul Price (UCSD) and Prof. John Skedros (University of Utah) for helpful discussions on bone. This research was funded by the Na-tional Science Foundation, Division of Materials Research, Biomaterials Pro-gram (Grant DMR 0510138).

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P.-Y. Chen , A.Y.-M. Lin, A.G. Stokes, Y. Seki, S.G. Bodde, J. McKittrick, and M. A. Meyers, are with the University of California, San Diego. P.-Y. Chen can be reached at [email protected].

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