Avian Materials and Structures:Cornified and Calcified

Sara G. Bodde21 June 2006

Literature Review

How birds see . . . materials scientists

How materials scientists see birds

• Keratinous Material– Feather

• Structure • Color• Mechanical Properties

– Rhamphotheca (beak) & Podotheca– Claw

• Calcified Material– Bone– Eggshell

• Conclusion

Outline

Structure of Feather

R.D.B. Fraser and T.P. MacRae, Symp. Soc. Exp. Biol. ;34:211-46 (1980)

Pigment and Structural Elements

©J.

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Chloebia gouldiae

A. Brush and H. Seifried, The Auk, 85: 416- 430 (1968)

-Short rachis, long barbs-Thick barbules, heavily deposited with melanin

-Short rachis, flat barbs-Lacking barbules where canthaxanthin is present

Short rachis, long barbs -Proximal: numerous barbules, heavily deposited with melanin-Middle: lacking barbules, containing carotenoids-Distal: lacking pigment

Lutein (xanthophyll)

Colors: Pigmentary• Melanin

– Eumelanin– Phaeomelanin

• Carotenoids– Xanthophylls (oxidized

carotenoids)• Astaxanthin: pheasant wattles• Lutein, zeaxanthin: egg yolk

– Carotenes: • β-carotene• Rhodopsin

• Fluorescent• UV

• Others– Turacoverdin unique to

Touracos (Musophagidae)– Turacin– Psittacofulvins

©D

. Jan

son

Tauraco persa

H.M Fox and G. Vevers, The Nature of Animal Colours (1960)

?

Analysis of sub-Species Dimorphism in Fairy Wren

S.M. Doucet et al., Proc. R. Soc. Lond. B (2004)

Malurus leucopterus leuconotus Malurus leucopterus leucopterus

Feather Color: A closer look at Fairy Wrens

S.M. Doucet et al., Proc. R. Soc. Lond. B (2004)

Feather Barb (TEM)

0.5 µm0.5 µm

5 µm5 µm

C – Cortex (keratinous) M – MelanosomesS – Spongy layer (medullary) V – Vacuoles

Structural Colors: Schemochromes• Iridescence by Interference

– Barbules rotated and flattened– Transparent keratin at the surface– Examples:

• melanin granule impinge on keratin layer (Pigeon)

• Melanosome platelets → mosaic structure → stacks of 8–10 mosaics → boat shaped scales (Hummingbird)

• Elongated melanin rods: Starling

• Scattering: Tyndall/Rayleigh Scattering?

Refractive index of melanin: 2.2Refractive index of keratin: 1.5 Refractive index of air: 1.0

Lamprotornis superbus

Pavo muticus

Calypte anna

H.M Fox and G. Vevers, The Nature of Animal Colours (1960)

Structural Colors: Coherent Scattering

R.O. Prum and R.H. Torres, Integrative and Comparative Biology, 43:591–602 (2003)

200 nm

Nectarinia coccinigastra

Melanosomesin barbules

Cross-section of Collagen Fibers

Quasi-ordered

β-keratin and air vacuoles in medulla of feather barb

Philepitta castanea Agapornis roseicollis

Crystal-likeLaminar

200 nm 200 nm

Scattering: Blue Plumage

R.O. Prum et al., Nature, 396: 28-29 (1998)

Cotinga maynana.

Medullary keratin matrix of a blue feather barb ■ - observed spectrum

2D Fourier Power Spectrum

Iridescence: Peacock (Pavo muticus)

Zi et al., Proc. Natl. Acad. Sci., 100 (22) 2003

Transverse cross-section of cortex consisting of keratin with embedded 2D photonic-crystal like structure

Melanin Rods Air spaces

Melanin Rods: 0.7 µm

Longitudinal cross section of barbule(keratin cuticle removed)

Keratin connectors

Medullar region

Lattice constants Blue: 140 nm Green: 150 nm Yellow: 165 nm

Transverse cross-section of barbule (SEM)

Iridescence: Hadeda Ibis (Bostrychia hagedash)

• Keratin layer sufficiently thick to contribute solely interference

• Melanosomesserve only to define keratin layer

D.J. Brink and N.G. van der Berg, J. Phys. D: Appl. Phys. 37 (2004) 813–818

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Iridescence: Hadeda Ibis (Bostrychia hagedash)

SEMicrograph of flattened, twisted feather barbules

EMicrographs of Barbules

Melanosome

D.J. Brink and N.G. van der Berg, J. Phys. D: Appl. Phys. 37 (2004) 813–818

Barbule cross-section (TEM)Keratin thickness: 0.8 µm

Feather: Mechanical Properties

2.50Mean2.67Common Starling1.78Grey heron2.76Tawny owl2.04Black-headed gull

2.41Eurasian sparrowhawk

2.39Mute swan2.71Willow ptarmigan2.42Rock pigeonE [GPa]Species

R.H.C. Bonser and P.P. Purslow, The Journal of Experimental Biology 198: 1029–1033 (1995)

Stiffness of Feather Keratin Stiffness of Rachis: Longitudinal Variation

Cygnus Olor

Mechanical Behavior of Rachis

A.M. Taylor et al., Journal of Materials Science, 39 (2004) 939– 942

Tensile Stress-Strain Responseafter moisture humidity conditioning

100%50%0%Mechanical Property

16.310.49.2Strain [%]

106.27129.99221.03Tension [MPa]

1.472.583.66ETension [GPa]

Relative Humidity

©M

.G. M

artin

Struthio camelus

Feather: Strain during Flight in Columba livia

W.R. Corning and A.A. Biewener, The Journal of Experimental Biology, 201:3057–3065 (1998)

In-Flight Feather Strain • Flight speed: 5-6 m/s

• Mean Compressive Strain: -0.0033 (late in downstroke) corresponding to -8.3 MPa(Maximum: 15.7 MPa)

• Maximum Tensile Strain: 0.0017 (upstroke) corresponding to 4.3 MPa

• Mean stress at failure: 137 MPa(compressive)

• Flexural stiffness of rachis is more critical than tensile strength

W.R. Corning and A.A. Biewener, The Journal of Experimental Biology, 201:3057–3065 (1998)

Failure: Feather Rachis

Buckling of Rachis (SEM)

Micro-fractures transverse to rachis axis (dorsal view)Buckling at 166 MPa

- Rachis keratin more susceptible to buckling than to tensile rupture- Fracture follows interstitials between keratin bundles

Tensile Failure of Rachis (SEM)

W.R. Corning and A.A. Biewener, The Journal of Experimental Biology, 201:3057–3065 (1998)

Feather Flexure

IMr

flex

M

• Stress dependent upon cross-sectional area of rachis

• Neglected torsion would decrease critical bending moment

- Bending MomentI - Moment of InertiaF - Applied Load

l - Length of Shaft

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Adapted from Seki et al.

4FLM

○- unmelanized● - melanized

M. Butler and A. S. Johnson, The Journal of Experimental Biology, 207: 285-293 (2004)

Effect of Melanin on Feather Breaking Strength

Feather Barb

Other Keratinous Structures(a) the central framework of the filament.

(b) Model for the arrangement of the β-sheet portions of the protein molecules in the filaments of avian keratin.

R.D.B. Fraser and T.P. MacRae, Symp. Soc. Exp. Biol. ;34:211-46 (1980)

Rhamphotheca: Micro-Hardness of Bill Keratin

• Seasonal: Increased wear endured during Winter

• Increased melanin production less costly than increased growth rate

• Color compromise is not crucial during Winter

R.H.C. Bonser and M.S. Witter, The Condor, 95:136-138 (1993)

Effect of Melanin on HardnessSturnus vulgaris

Rhamphotheca

Y. Seki et al., Acta Materialia, 53: 5281–5296 (2005)

©J.

&C

. Cur

d

Ramphastos toco

Micro-hardness: 22.43 kg/mm2

SEMicrograph of keratin tiles

Beak = Rhamphotheca + Closed-Cell Foam

Y. Seki et al., Acta Materialia, 53: 5281–5296 (2005)

Trabeculae and Membranes

Foam filled shell

Shell+foam

Strain

0

5

10

15

20

25

30

35

0 0.2 0.4 0.6 0.8 1

Stre

ss (M

Pa)

Interaction effect

+

Stress-Strain Curve for Toucan Bill(Compression)

Keratinous Podotheca

G.A. Clark, Jr., A Journal of Ornithological Investigation, 84 (4):301-402 (1977)

P.R

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an Z

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1–47

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000)

• Scales– Scutellate: -keratin– Reticulate: -keratin

• Cornified in terrestrial birds• Softer/more flexible in

marine birds

Pipilo erythrophthalmus

Humidity Response of Ostrich Claw

A.M. Taylor et al., Journal of Materials Science, 39: 939– 942, (2004)

Tensile Stress-Strain for Conditioned Keratinous Claw Section

0.231.832.98ECompression [GPa]

Strain [%]

Tension [MPa]

ETension [GPa]

Mechanical Property

5.71

90.28

2.70

0%

6.66

68.68

2.07

50%

20.51

14.03

0.14

100%Relative Humidity

Hydration Sensitivity of Ostrich Claw

R.H.C. Bonser, Journal of Materials Science Letters, 21:1563 – 1564 (2002)

Avian Bone• Pneumatic bone (large

gliding birds)

• Lightweight for flight

• Durable for stress of taking off and alighting

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IMr

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Phalacrocorax carbo©

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ite.c

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Avian Bone: Mineral/Protein ContentTibiotarsus

L. Knott and A.J. Bailey, British Poultry Science 40: 371–379 (1999)

Avian Bone: Hardness

■ - cortical bone□ - trabecular bone

R.H.C. Bonser, The Journal of Experimental Biology 198: 209–212 (1995)

- Middle of bone is harder than at epiphyses- Middle bone is more “mature”

Distance from Proximal Epiphysis [mm]

Vick

er’s

Har

dnes

s [k

g/m

m2 ]

Micro-Hardness along Humerus

Laminarity of Avian Bone

Wing Bone Vasculature

E. de Margerie, Journal of Anatomy, 201, 521–526 (2002)

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AAAAA

Laminarity

Anas platyrhynchos

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oblique

circularradial

longitudinal

© Kardong

© Weaver & Ashby

Laminarity

• Shear stress varies linearly with distance from axis of bone

• Thin-walled, round

IT

shear

- Distance from the axis

© Weaver & Ashby

E. de Margerie, Journal of Anatomy, 201, 521–526 (2002)

T - Torsion

Laminarity• Laminar bone (wing)

adaptation to torsional loads caused by flapping flight

• Laminar structures in all wing bones except radius + femur

• Orientation of osteonsindependent of growth rate

E. de Margerie, Journal of Anatomy, 201:521–526 (2002)

Mechanical Properties of Long Bone

• No correlation between [Ca] and mechanical properties in long bone

• Rather correlated to [Mg] and [P]

11.96181.85Tarsometatarsus

16.63227.08Tibiotarsus

9.69145.65Femur

20.98242.00Radius

12.06191.05Ulna

10.49167.35Humerus

Eflex [GPa]flex [MPa]Bone

J. Cubo and A. Casinos, European Journal of Morphology, 38 (2):112–121 (2002)

IMr

flex

Woodpecker Skull

• Acorn Woodpeckers: 600 – 1200 Gs!

• Compressive stress travels along maxilla and then along a bony structure below the brain

• Broad surface of brain dissipates shock

©J.

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gMelanerpes formicivorus

Melanerpes carolinus

©C

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P.R.A. May et al. Lancet, 1:454-455 (1976) / W.J. Bock, Ostrich 70 (1): 23-31 (1999)

Woodpecker Skull

• Shock absorption: frontal overhang (linearity of pecking), hyoidalapparatus

• Little cerebral-spinal fluid: comparatively close brain-cranium contact

• Ethmoid cushion: numerous thin-walled air cells©

A. B

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Melanerpes aurifrons

©J.

P. P

aris

P.R.A. May et al. Lancet, 1:454-455 (1976) / P.R.A. May et al. Arch. Neurol., 36:370-373 (1979) /

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Eggshell

Eggshell

Palisade Vesicles

Crown Vesicles

Vertical Matrix

Calcite Grain Boundaries

Cuticle Vesicles

Fiber

Mantle

Crown

Outer Membrane

Inner Membrane

Cuticle

Calcium Reserve Assembly

Calcium Reserve Body-sac

Baseplate

PalisadeColumns

J.E

. Den

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l., J

ourn

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f Mor

phol

ogy

228:

287-

306

(199

6)Hydroxyapatite• Composition:

– Calcitic CaCO3

– 5% organic• Shell Proper: 250 µm

(chicken)• Cuticle: hardens after

ovoposition– Water retention– Protection against

bacteria• Membranes: collagen

(non-mineralized)• Porous: 0.02 – 0.03 mm,

100/cm2 (ostrich)• Calcium Reserve

Assemblied: Ca for embryo skeleton (mineralized matrix)

Eggshell as a model for Biomineralization

J. Ruiz and C.A. Lunam, British Poultry Science 41: 584–592 (2000)

- Palisade layer contains dermatansulfate

- Vaterite observed in some cases (meta-stable)

- Collagen found in membranes is associated with mineralization

J.E

. Den

nis

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l., J

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228:

287-

306

(199

6)

Allometrics of Avian Egg

trP

t - Thickness [µm]

2tF

448.006.54 wt

3,434 Species (all literature)

915.086.50 wF F - Yield force [g]

w - Mass of egg [g]

47 Species, 26 Families, 11 Orders

Nectarinia osea Struthio camelus

w = 0.86 gF = 37 gt = 52 µm

w = 1.46 kgF = 75.75 kgt = 2.2 mm

~ 1500 – 1700 kg/cm2

A. Ar et al., Condor, 81:331-337 (1979)

Eggs withstand 150 – 170 MPa!

Summary • Feather colors accomplished by pigment and by

structural features of feather (iridescence and scattering)

• Mechanical properties of feather dependent upon keratin strength as well as feather structure/geometry

• Bill properties are dependent upon both keratinous shell and foam center

• Bending strength of avian bone is highest in principal wing bone and the principle leg bone

• Laminar bones suited for high torsion forces• Eggshell is a model for biomineralization consisting

of an organic matrix which guides deposition of inorganic mineral

Acknowledgements• Advisor: Professor M.A. Meyers

• Committee Members: Professor V. Nesterenkoand Professor G. Thomas

• Group-mates: Buyang Cao, Po-Yu Cheng, Hussam Jarmakani, Albert Lin, Anuj Mishra, Yasuaki Seki, GlaucioSerra*, Liliane Serra de Morais*

* Photo credit

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