biological materials science overview the cutting edge...

2008 March • JOM 21www.tms.org/jom.html

OverviewBiological Materials Science

Through hundreds of millions ofyears of evolution, organisms havedevelopedamyriadofingenioussolu-tions to ensure and optimize survivalandsuccess.Biologicalmaterials thatcompriseorganismsaresynthesizedatambienttemperatureandpressureandmostly in aqueous environments. Thisprocess, mediated by proteins, limitsthe rangeofmaterialsat thedisposalofnatureandthereforethedesignplaysapivotal role.This article focusesonsharp edges and serrations as impor-tantsurvivalandpredatingmechanismsin a number of plants, insects, fishes,andmammals.Someplants(e.g.,Pam-pas grass and Cortaderia selloana)have sharp edges covered with serra-tions.Theproboscisofmosquitoesandstingerofbeesareexamplesininsects.Serrations are a prominent featurein many fish teeth, and rodents haveteeththataresharpenedcontinuously,ensuring their sharpnessandefficacy.Somecurrentbioinspiredapplicationswillalsobereviewed.

IntroductIon

Many biological systems have me-chanicalpropertiesthatarefarbeyondthose that can be achieved using thesamesyntheticmaterials.Thisisasur-prisingfact,consideringthatthebasicpolymersandmineralsusedinnaturalsystems are quite weak. This limitedstrengthisaresultoftheambienttem-perature, aqueous environment pro-cessing,andthelimitedavailabilityofelements(primarilyC,N,Ca,H,O,Si,P).Biologicalorganismsproducecom-posites that are organized in terms ofcomposition and structure, containingbothinorganicandorganiccomponentsincomplexstructures.1–3Theyarehier-archically organized at thenano-,mi-cro-,andmeso-levels.

the cutting Edge: Sharp Biological Materials*

M.A. Meyers, A.Y.M. Lin, Y.S. Lin, E.A. Olevsky, and S. Georgalis

Thecomplexity anduniquenessofbiological materials is well illustratedin the Arzt4 pentahedron, which hasfivecomponents:ambienttemperatureand pressure processing, self assem-bly, functionality, hierarchy of struc-ture, and evolution/environmental ef-fects. The components of the E. Arztpentahedronshown inFigure1of thecommentaryonpage18areindicativeofthecomplexcontributionsandinter-actions necessary to fully understandand exploit (through biomimicking)biologicalsystems.Thesecomponentsareprominentinallbiologicalsystems,all the way from the molecular, cel-lular,organ,andorganism levels.Thelimited scarcity of materials availabletonaturebecauseoftherestrictionsinsynthesisandprocessingshiftsthefo-cusonthedesignofthesematerials.Inasense,andparaphrasingM.F.Ashby,5

materialsanddesignareinseparableinnature. This article illustrates these uniqueaspectsby focusingononecharacter-isticofbiologicalmaterials:theirabil-itytopuncture,cut,andshred.Thefactthatserrationsandneedlesarepresentin many species and in diverse con-figurationsisdirectevidencethattheydevelopedindependently,byamecha-nism that anthropology calls conver-gentevolution.

PlantS: razor graSS

Figure 1 shows a blade of pampasgrass(Cortaderiaselloana)withserra-tionsalongitsouteredge.Eachserra-tionisintheshapeofathornprotrud-ingupwardalongthesideoftheblade.Theyextendapproximately50µmfromthe body of the leaf and form sharppoints with an apex angle of roughly20˚.Thissharpcuttingedgewasevolu-tionarilydesignedasadefensemecha-nismagainstgrazinganimals.Thisfea-tureisalsoprominentinothergrasses,such as Hypolitrium Shraderenium.Other examples can be found in cac-tuses,whichhavetheirbodiescoveredinsharpneedlesforprotection.

InSEctS: MoSquIto and BEE

Figure2showstheproboscisofthemosquito (Culex pipiens). The pro-boscisiscomposedofanoutersheaththat is used to detect the surroundingenvironment such as temperature andchemical balance. Inside this sheaththere are two tubes which enter themosquito’s unsuspecting prey. One ofthesheathsisterminatedwithaninnerstyletthatisusedtopiercethroughtheskinanddrawbloodwhiletheotherin-jectsananticoagulantintotokeeptheblood flowing. Figure 2 shows three

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JOM • March 200822 www.tms.org/jom.html

Figure 1. Pampas grass (Cortaderia selloana); note serrations at edges.

Figure 2. Scanning-electron micrographs of mosquito (Culex pipiens) proboscis; top: proboscis covered with hairy sheath; middle: partially exposed stylet extremity; bottom: exposed serrated stylet designed to section tissue for dual needle penetration.


Figure 3. A bee (Apis mellifera) stinger; notice directional barbs that ensure retention of stinger in tissue of prey.

Figure 4. A dogfish (Hydrolycus scomberoides) and teeth.

Figure 5. A piranha (Serrasalmus manu-eli) teeth: (a) hierar-chical structure from jaw to single tooth to micro serrations; (b) and (c) diagrams of guillotine-like confine-ment of material dur-ing the biting action of a piranha.


syringe. The stinger of the common bee(Apismellifera),showninFigure3,isyetanotherexampleoffunctionalser-rations; in this case they are reverse-facing barbs that help to propel theneedledeepintothetissueofitsprey.Thesebarbsareonthescaleof10–20µmingaugelengthandrunalongtheshaftofthestinger.Whentheinsecthasused the stinger it stays embedded inthe skin and therefore the delivery ofpoisonisensured.

FISh

The function of the fish teeth ex-aminedhere areofparticular interest.Thereisagreatvarietyofteeththatareevolutionarily adapted to the diet andpredation habits. The long sword-liketeethoftheAmazondogfish(Hydroly-cusscomberoides)areagoodexampleof extreme piscivorous evolutionarydesign.Theyareusedtopunctureandhold prey and are thus designed in ahook-likefashionfacinginwardtowardthemouthofthefish.Theyactuallyaresolongthattheyprotrudethroughthehead once the mouth is closed. ThiscanbeseeninFigure4.Theyalsohavesharplateraledgesthatcutthroughthefleshofotherfish. The piranha (Serrasalmus manu-eli) is quite different, although livingin the sameAmazonbasin.Figure5ashows the structural hierarchy of thecutting mechanisms found in the jawofapiranha.Thejawisdesignedwithsharp triangular teeth aligned so thatasthemouthofthefishclosesthetipsof the teethofboththelowerandup-per jaw are superimposed and punc-turetheprey.Asthejawfurtherclosesany tissuecaught in the troughof thealignedteethisseveredinaguillotine-likeaction.ThisisshowninFigure5b.There are superimposed compressionandshearforceswhicheffectivelycutthrough skin and muscle. Each toothexhibitsmicro-serrationsalongitscut-tingedge,seen in thedetailofFigure5a. These serrations, approximately10–15 µm in wavelength, are used tocreate a highly efficient cutting effectwhich converts some of the draggingforce into normal force at localizedpoints. The sharks evolved teeth from thescales of their ascendants. There is

Figure 8. A rabbit tooth (incisor).

Figure 7. A Mako shark and tooth.

scanning-electron microscopy (SEM)images at increasing magnifications;the top micrograph shows the sheath,covered with hair; the middle micro-graph shows the tip of the stylet pro-truding from the sheath; and the bot-tomone,at thehighestmagnification,showstheserrationsontheedgeofthestylet.Therearetworowsofserrations,

oneoneachside.Theyaredesignedtoreducecompressionandnervestimula-tionduringabitebyincreasingtheef-ficiencyofthecuttingedge.ThisisincongruencewithK.Okaetal.6andT.Ikeshoji,7 who concluded that the ini-tial bite of a mosquito is painless be-causeofthehighlyserratedproboscis.Theyusedthisasinspirationforanovel

Figure 6. Great white shark (Car-caradon carcha-rinus) teeth.


considerable variation8–12 in the con-figuration and morphology of sharkteeth,which is illustratedhereby twoexamples:thegreatwhitesharkandtheMakoshark. The great white shark (Carcaradoncarcharinus)usessharpteethtoperformaveryspecifickillingaction.Toavoidself-injury thegreatwhiteshark takesone efficiently large bite into its preythenretreatsandwaitsforitsvictimtoundergoshockorhemorrhagingbeforefinalconsumption.Thepreyisveryof-tenamammalsuchasa sealora sealion. This bite takes only one secondtocomplete8andthusextremelysharpteetharerequired.Eachtoothisoutfit-tedwithalineoflargeserrations,withupto300µmbetweenpoints.Theser-rationsareperfectlyalignedalongthecuttingedgeofthetooth,eachcreatinga mini tooth on the side of its parenttooth.Similar to thepiranha tooth theserrations on this edge maximize theefficiencyofthedragforceandconvertitintopointsofnormalforcesummedalong the side of each serration. Thisconfiguration of serrated teeth is fa-voredwhenthedietconsistsoftougherflesh. Indeed, the Tyranosaurus13 teethhave serrations with spacing of ap-proximately200µm,veryclosetothegreat white shark. Figure 6 shows (a)anoptical imageof theoverall jawofagreatwhiteshark,withmultiplerowsofteeth,(b)ascanning-electronmicro-graphof thecuttingedgeof the toothwithlargeserrations,(c)asideviewofserrations,and(d)atop-downviewofserrations. Comparedwiththegreatwhiteshark,thereareno serrationson theedgeoftheshortfinMakoshark(Isurusoxyrin-chus) tooth.The teethareslenderandslightlycurvedinahook-likefashion.The functionof these teeth is primar-ilytopunctureandcaptureprey10whilein the great white shark the teeth areused more as cutting tools. It is clearinFigure7 that theangleof theapexofthetoothofaMakoismuchsmallerthenthatofthegreatwhite.Thissharpangle, similar to that of the dog fish,is used to puncture and swallow preyinonebite;thesidesoftheteethhavesharpedgestoslicethroughthetissuesthatwereperforated.

rodEnt IncISorS

Figure 10. Possible biomi-metic devices: (a) syringe inspired by mosquito pro-boscis; (b) scissors inspired by piranha teeth; (c) shred-der cutting blades inspired by rabbit incisors.

Figure 9. Self-sharpening rat incisors.

The incisor teeth of rodents suchastherabbitandrat(Figures8and9,respectively) have been evolutionarilydesigned to “self-sharpen” through aprocess that takes advantage of natu-ral wear and difference in wear ratesdepending on the hardness of certainmaterials.These teetharedesigned insuchawaythatasofterdentineback-ing iswornawayat a faster rate then

thehardenamelcuttingedge.Thisac-tioncontinuouslyexposesnewsectionsof the enamel material, as the rodentperiodically self-sharpens its teeth. InFigure9theenamelanddentineofratincisorsareshown.

BIoMIMEtIc dEvIcES

Figure10showsschematicrepresen-tationsofsomepossibleandsuccessful


biomimetic approaches to devices in-spiredfromthesharpobjectsdescribed.Figure 10a represents a hypodermicneedleinspiredbytheproboscisofthemosquitowhichwasfirstdevelopedbyOkaetal.6Thishypodermicneedlehasdimensionscomparablewith themos-quitoproboscisbut,moreimportantly,uses the serrated edges (one on eachside)toslicethroughthetissue.Thesy-ringemanufacturedbyOkaetal.6hasabuilt-inreservoirandisequippedwithjaggededgesthatmimicthemosquitostylet.ItismadefromSiO

2usingasili-

conmicromachiningtechnology. Figure10brepresentsapossiblede-signofscissorsinspiredbythemouthof a piranha. The angle, spacing, andconfiguration of the scissor serrationsmatch thoseof thepiranha.Thiscon-ceptual design is ideally suited to cutthroughtissuehavingtheapproximatemechanicalresistanceofflesh. Figure10cisaschematicdrawingofa cutting tool which was designed toself-sharpen using the same mecha-nismsastherodenttooth.Thisequip-ment,inspiredontheratandrabbitin-cisors,was successfullymanufacturedin Germany by Jürgen Berling andMarcus Rechberger from the Fraun-hoferInstituteUMSICHT.14Theyuseda hard titanium nitride ceramic rein-forced with nanoparticles as the hard‘enamel’ portion of the cutting blade.Thesoft‘dentine’partoftheknifewas

madebya tungstencarbide-cobalt al-loy. The titanium nitride layer wastwiceashardasthealloy.InFigure10ctheinnerregionsofthethreebladesofthe shredder rub against the materialsto be cut and wear out, keeping theouter layer, (thehard titaniumnitride)exposedandsharp.

acknowlEdgEMEntS

ThisresearchhasbeenfundedbytheNational Science Foundation GrantDMR 0510138, Biomaterials Pro-gram).TheauthorsthanktheInstitutefor Laser Science & Applications atLawrenceLivermoreNationalLabora-tory for support of Albert Lin. Scan-ning-electron microscopy by EvelynYorkandScrippsInstitutionofOcean-ography is gratefully acknowledged.Discussions with Prof. J. McKittrickare greatly acknowledged. ProfessorsH.J. Walker and P. Hastings of SIOwereinstrumental intheidentificationof various fish species. E. Kisfaludyprovided valuable specimens. A. Du-ong captured the mosquitoes. To all,ourwarmthanks.

references

1. U.G.K. Wegst and M.F. Ashby, “The Mechanical Efficiency of Natural Materials,” Phil. Mag., 84 (2004), pp. 2167–2181.2. M.A. Meyers et al., “Biological Materials: Structure and Mechanical Properties,” Progress in Materials Science, in press. [Please update if possible.]3. M.A. Meyers et al., “Structural Biological Composites:

An Overview,” JOM, 58 (7) (2006), pp. 35–41.4. E. Arzt, “Biological and Artificial Attachment Devices: Lessons for Materials Scientist from Flies and Geckos,” Materials Science and Engineering C, 26 (8) (2006), pp. 1245–1250.5. M.F. Ashby and K. Johnson, Materials and Design (Oxford, U.K.: Butterworth-Hinemann, 2003).6. K. Oka et al., “Fabrication of a Microneedle for a Trace Blood Test,” Sensors and Actuators A, 97-98 (2002), pp. 478–485.7. T. Ikeshoji, The Interface between Mosquitoes and Humans (Tokyo: University of Tokyo Press, 1993), pp. 189–214.8. J.M. Diamond, “How Great White Sharks, Saber-Toothed Cats and Soldiers Kill,” Nature (London), 322 (1986), pp. 773–774.9. R.A. Martin et al., “Predatory Behaviour of White Sharks at Seal Island, South Africa,” J. Mar. Biol. Ass. U.K., 85 (2005), pp. 1121–1135.10. T.H. Frazzetta, “The Mechanics of Cutting and the Form of Shark Teeth (Chondrichthyes, Elasmobranchii),” Zoomorphology, 108 (1988), pp. 93–107.11. L.O. Lucifora, R.C. Menni, and A.H. Escalante, “Analysis of Dental Insertion Angles in the Sand Tiger Shark, Carcharias Taurus Chondrichtheyes: Lamniformes,” Cybium, 25 (1) (2001), pp. 23–31.12. K. Shimada, “Dental Homologies in Lamniform Sharks (Chondrichthyes: Elasmobranchii),” Journal of Morphology, 251 (2992), pp. 38–72.13. W.L. Abler, “The Serrrated Teeth of Tyrannosaurid Dinosaurs, and Biting Structures of Other Animals,” Paleobiology, 18 (1992), pp. 161–183.14. Jürgen Berling and Marcus Rechberger, “Knives as Sharp as Rat’s Teeth,” Research News 1 (Oberusel, Germany: Fraunhofer Institute for Environmental, Safety and Energy Technology, October 2007), Topic 3, www.fraunhofer.de/fhg/EN/press/pi/2005/01/Mediendienst012005Thema3.jsp.

M.A. Meyers and A.Y.M. Lin are with the University of California at San Diego; E.A. Olevsky is with San Diego State University; Y.-S. Lin is with the University of California at San Diego and San Diego State University; and S. Georgalis is with Modern Marvels, History Channel, Manhattan, NY. Dr. Meyers can be reached at [email protected].

biological materials science overview the cutting edge...

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