Biomimetic isotropic nanostructures for structural coloration

Jason D. Forster1, Heeso Noh2, Seng Fatt Liew2, Vinodkumar Saranathan3

Lin Yang4, Jin-Gyu Park1, Richard O. Prum3, Corey S. O’Hern1,5,Simon G. J. Mochrie2,5, Hui Cao2,5, and Eric R. Dufresne1,5,6,7

1Mechanical Engineering, Yale University

2Applied Physics, Yale University

3Ecology and Evolutionary Biology, Peabody Museum of Natural History, Yale University

4National Synchrotron Light Source, Brookhaven National Laboratory

5Physics, Yale University

6Chemical Engineering, Yale University

7Cell Biology, Yale University

28 October 2009

Many species of birds have feathers that arebrilliantly-colored without the use of pigments. Inthese cases, light of specific wavelengths is selectivelyscattered from nanostructures with variations in in-dex of refraction on length scales of the order of vis-ible light. [1] This phenomenon is called structuralcolor. The most striking examples of structural colorin nature are iridescent colors created by scatteringfrom periodic structures. [2][3] The colors producedby these structures change dramatically dependingon the angle of observation. Nature also producesstructural colors that have very little angle depen-dence. These colors are the result of scattering fromisotropic structures. [4][5][6]

In recent years, periodic biological structures haveprovided inspiration for groups trying to make pho-tonic materials. [7][8] Much of this work has beenmotivated by producing a photonic band gap (PBG).[9][10][11][12][13][14] However, Nature’s alternative de-sign, based on isotropic structures is just startingto be explored. [15][16] Hallam et al have usedbiomimetic random structures to make ultra-thinmineral coatings that are brilliant white. Takeoka etal recently showed that a wide range of colors withvery little angle dependence can be produced by mi-

crogel dispersions. In this communication, we de-scribe the self-assembly of biomimetic isotropic filmswhich display structural color that is amenable to po-tential applications in coatings, cosmetics, and tex-tiles. We find that isotropic structures can producecolor if there is a pronounced characteristic length-scale comparable to the wavelength of visible lightand wavelength-independent scattering is suppressed.

We make two types of films that are structurally-colored by exploiting the self-assembly of colloidalpolymer nanoparticles. The first type of sample is athin film on a glass coverslip produced by spin castingan aqueous suspension of spheres (Figure 1a). Whilemonodisperse dispersions form anistropic polycrys-talline films, as shown in the lower inset of Figure 2,a mixture of two sizes of spheres ensures an isotropicstructure.[17] The blue-green film in Figure 1 is madefrom a bidisperse suspension of polystyrene sphereswith diameters of 212 nm and 254 nm in roughlyequal numbers.

We image the structures of the film using scanningelectron microscopy (SEM). An SEM image of thetop layer of a film in Figure 1b shows that there is nolong range order. The SEM of a similar film in topinset of Figure 2 reveals a representative thickness of

1

arX

iv:0

912.

4290

v1 [

cond

-mat

.sof

t] 2

1 D

ec 2

009

0.02 0.03 0.040

0.2

0.4

0.6

0.8

1

I(q

)/I(q

0)

q [nm!1]

(a) (b)

(c) (d)

Figure 1: Structure of isotropic films. a) Photographof a film spun-coat onto an 18 × 18 mm glass cov-erslip. Inset : Photograph of a dried sessile droplet.b) SEM image of the top layer of a sample compara-ble to the one in (a): the field of view is 5.2 µm. c)SAXS pattern from a sample comparable to the onein (a): the field of view is 0.15 nm−1 and the grayvalues are logarithmic in intensity. d) The red dotsare the azimuthal average of the scattering pattern in(c), the line is optical reflectivity data taken at an an-gle of 10◦ (experiment geometry shown in Figure 4)converted to q-space.

2.3±0.2 µm.

The optical properties of isotropic and crystallinefilms are quite different, even for samples preparedwith very similar particles. We compare the trans-mission spectra of isotropic and crystalline samplesin Figure 2. The isotropic film is composed of sphereswith diameters 212 nm and 268 nm, the crystallinefilm is composed solely of 212 nm spheres. Both sam-ples show a dip near 500 nm at normal incidence.However, when the angle of incidence is changed, thespectral position of the dip for the crystalline sam-ple shifts and eventually disappears. In contrast, theposition of the dip for the isotropic sample does notmove. This illustrates the trade-off in optical perfor-mance between crystalline and isotropic structures:while the crystalline film has more pronounced fea-tures at some angles, the isotropic film performs con-sistently over a wide range of angles.

To quantify the structure of the films, we performsmall-angle X-ray scattering (SAXS) measurementson samples prepared on kapton tape. A typical scat-tering pattern is shown in Figure 1c. The patternis dominated by a ring of uniform intensity, indicat-ing that there is a well-defined length scale with nopreferred direction – the structure is isotropic withshort-range order. The azimuthal average of this pat-tern is shown in Figure 1d. The position of the firstpeak q0 = 0.03 nm−1 corresponds to a length scaleof 210±4 nm, which agrees with the size range ofspheres used to make the film. The full width at halfmaximum (FWHM) of the first peak, ∆q, character-izes the range of spatial order ξ = 2π/∆q = 870 nm.In powder crystallography, ξ describes the crystal do-main size, here, ξ is only a few particles diameters insize.

We directly compare the optical reflectivity mea-surements to SAXS measurements by plotting thereflected intensity as a function of wavevector q =(4πne/λ) cos (θm/2), where ne is the effective refrac-tive index of the material; θm is the angle betweenillumination and detection, taking into account re-fraction at the film surface; and λ is the wavelengthof light in vacuum (Figure 1d). The peaks from bothmeasurements match when ne = 1.24. We apply the

2

400 450 500 550 600 650 700 750 8000

10

20

30

40

50

60

70

80

90

100

Wavelength [nm]

Per

cent

Tra

nsm

issi

on

Figure 2: Effect of disorder and order on opticalproperties. The top set of curves show the trans-mission spectra for a film composed of isotropically-arranged spheres. The bottom set of curves showthe results of the same measurement performed witha crystalline sample. The data were taken with thesample normal to the optical path (solid line), at anangle of 30◦ (dashed red line), and at an angle of 80◦

(dotted blue line), represented schematically in theupper right hand corner. Insets: side-view SEM im-ages of the isotropic (top) and crystalline (bottom)samples, showing the thickness of the films.

Maxwell-Garnett equation,

ne = nair

(2n2

air + n2s + 2φs(n2

s − n2air)

2n2air + n2

s − φs(n2s − n2

air)

)1/2

to calculate the volume fraction of spheres, φs =0.46±0.04, where ns is the index of refraction of thespheres, taken to be 1.58, and nair is taken to be 1.00.

Isotropic films can produce structural color withlittle angle dependence, but the film thickness criti-cally affects its color, as seen in the inset of Figure 1a.Here, we cast a thick film by drying a sessile droplet ofthe same suspension used to make the thin films. Inthick regions near the center, the film appears white.In thin sections near the edge, it appears blue-green.This thickness dependence can be understood in thefollowing way. The film preferentially scatters wave-lengths corresponding to the peak in I(q). In a thinfilm, only these wavelengths will be scattered to thedetector resulting in a structural color. In a thickfilm, all wavelengths are scattered multiple times andreach the detector.

The sensitivity of the color to the film thicknessrequires well-controlled casting procedures which in-crease the cost and limit the coated area. There-fore, for many potential applications it is necessary toeliminate the thickness-dependence. We address thisby introducing broadband absorption to the bulk ofthe films. The absorption length plays a similar roleas the thickness: it limits the path length of lightthrough the film by absorbing photons that do notget scattered within a small distance from the surface.Thus, only wavelengths with the strongest scatteringwill escape the film before being absorbed.

We make a series of thick films with different ab-sorption lengths by drop-casting films with varyingconcentrations of carbon black. The photo in Fig-ure 3a illustrates the effect of adding carbon black onthe color of the material. From left to right, the con-centration of carbon black, [CB], is increased. Intu-itively, one might expect a mixture of black and whiteto make gray, but here they make blue-green over arange of [CB]. The plot in Figure 3b shows the nor-malized optical scattering spectra for these five sam-ples. As [CB] is increased from 0.02 wt% to 1.80 wt%,the contrast between scattered intensity at the peak

3

and at shorter wavelengths is increased, improvingthe color of the sample. When [CB] = 11.2 wt%, thescattered intensity is reduced by a factor of ten com-pared to the brightest sample (inset in Figure 3b),and the film appears dark gray. The reflectance peakis narrowest for [CB] = 1.80 wt% (Figure 3c), andindeed this sample has a distinct blue-green color.Table 1 lists the [CB] for each sample and the cor-responding extinction length: the extinction lengthis extrapolated from measurements of aqueous sus-pensions of CB. Interestingly, the extinction lengthfor sample 3 is 1.3 µm, which is comparable to thethickness of the thin film pictured in Figure 1a.

Table 1: Carbon Black Extinction Length

Sample [CB] [wt%] Extinction Length [m]1 0.02 1.3×10−4

2 0.18 1.3×10−5

3 1.80 1.3×10−6

4 3.60 6.5×10−7

5 11.2 2.1×10−7

The thick films with CB are not iridescent un-der omnidirectional illumination, but, under direc-tional illumination, the peak wavelength scattereddoes change slightly when the angle between illumi-nation and detection is varied. [18] Since the colorsare the result of single scattering, the position of thescattering intensity maximum does not vary with re-spect to q, as demonstrated by the spectra in Fig-ure 4. The red dots connected by a red line in Fig-ure 4 represent the azimuthal average of the SAXSpattern for a sample with the same [CB] prepared onkapton tape. The peaks from the optical and SAXSmeasurements match when ne = 1.29, implying thatφs = 0.54±0.05. The higher value of φs for the thickfilms relative to the thin films is most likely the re-sult of the different quench-rates used to make thesamples. In the spin coating of thin films, the wa-ter evaporates within seconds, while water evaporatesfrom the thick films over a few hours, allowing par-ticle rearrangement which leads to a higher φs. Inthe thick film, we find that ξ = 940 nm, only a fewparticle diameters.

These isotropic films mimic the essential optical

400 500 600 700 8000

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

! [nm]

I(!

)/I(!

0)

400 600 800

10 4

10 3

5

43

21

I (!)

10 2 10 1 100 101 10260

80

100

120

140

5

43

2

1

CB Concentration [wt%]

Spec

trum

Wid

th[n

m]

(a)1

0.02

2

0.18

3

1.80

4

3.60

5

11.2

(b)

decreasing[CB]

(c)

(d)

Figure 3: Optimizing color by adding absorption. a)Photograph of five samples containing carbon black.Sample numbers and [CB] in wt% appear above andbelow the samples, respectively. b) Normalized op-tical scattering spectra recorded at an angle of 20◦

(experiment geometry shown in Figure 4) for the fivesamples in (a). Inset : Non-normalized scatteringspectra for the same samples. c) SEM image of in-terior region of a sample with [CB] = 0.8 wt%: thefield of view is 7.8 µm wide, a piece of CB is indicatedwith an arrow. d) The width of the spectra for eachsample in (a) at I(λ)/I(λ0) = 0.90

4

0.02 0.025 0.03 0.035 0.04 0.0450

0.5

1

1.5

2

2.5

10°

20°

30°

40°

50°

60°

q [nm!1]

I(q

)/I(q

0)

10 20 30 40 50 600.02

0.025

0.03

0.035

0.04

! [degrees]

q0

[nm!

1]

Figure 4: Color is the result of single scattering.Black lines are normalized reflectance spectra takenover a range of angles and converted to q-space forsample 2 in Figure 3, and the azimuthal average ofthe SAXS pattern for a similar sample (red dots).The spectra have been vertically offset for clarity.Inset : Position of the peak as a function of angle.Schematic: the source and sample are fixed and thedetector is rotated.

properties of bird feathers that have structural colorfrom isotropic nanostructures. A photograph of anexample of these feathers from the crown of Lepi-dothrix coronata is shown in Figure 5a, and a trans-mission electron micrograph (TEM) of the color-producing structure is shown in Figure 5b. Normal-ized I(q) from both L coronata and sample 2 fromFigure 3 are plotted as a function of q/q0 in Fig-ure 5c. The SAXS patterns reveal similar structuresout to the third peak in I(q). Beyond that, the thickfilm has additional peaks that arise from the unifor-mity of the spheres used in the sample. We com-pare the performance of the feathers and films byplotting optical scattering spectra for both at 20◦ inFigure 5d. The scattered optical intensity peak forL coronata is narrower than the film: the full-widthat I(λ)/I(λ0) = 0.90 is 49 nm for the feather and82 nm for the film. Similarly, L coronata has a nar-rower first peak in I(q). L coronata also displays lessscattering at shorter wavelengths. This may be dueto a significant difference in the two structures: thefeathers have spheres of air in a high-index of refrac-tion background whereas the films have spheres of ahigh-index in a background of air.

Non-iridescent structural color is realized when anisotropic structure has a peak in I(q) and wavelength-independent scattering is suppressed. Using a bidis-perse mixture of spheres produces isotropic struc-tures. Controlling film thickness or absorption lengthare effective at enhancing contrast in reflectance spec-tra. These films may have applications in coatings,cosmetics and textiles. The basic optical properties ofstructurally-colored feathers have been reproduced,but more work must be done before the biomimeticsamples perform as well as their biological counter-parts.

The authors would like to acknowledge seed fund-ing from the Yale NSF MRSEC (DMR-0520495), aNSF CAREER grant to ERD (CBET-0547294), anda NSF grant to HC (DMR-0808937). Research car-ried out in part at the National Synchrotron LightSource (NSLS), Brookhaven National Laboratory,which is supported by the U.S. Department of En-ergy. Research carried out in part at the AdvancedPhoton Source (APS) at Argonne National Labs withthe help of Drs. Alec Sandy and Suresh Narayanan,

5

Figure 5: Comparison with feathers. a) Photographof crown feathers from L coronata: the field of viewis 1 cm. b) TEM image of air spheres in beta-keratinfrom L coronata: the field of view is 5.5 µm. c)Azimuthal averages from SAXS measurements of Lcoronata (dashed line) and a thick film with the same[CB] as sample 2 in Figure 3 (solid line). Inset: SAXSpattern from L coronata: the field of view is 0.14nm−1 and the gray values are logarithmic in intensity.d) Comparison of optical scattering data taken at anangle of 20◦ (experiment geometry shown in Figure 4)from L coronata and sample 2 from Figure 3. Theline color corresponds to the apparent color of thefeathers and the thick film.

and supported by the U.S. Department of Energy, Of-fice of Science, Office of Basic Energy Sciences, underContract No. DE-AC02-06CH11357.

1 Experimental

Monodisperse polystyrene spheres were synthesizedusing a surfactant-free polymerization technique.[19] Particles were electrostatically stabilized by co-polymerization with sodium 4-vinylbenzenesulfonate.After synthesis, particle suspensions were washed bycentrifugation and resuspension at least three timeswith DI water. After washing, all particle suspen-sions were adjusted to φs = 0.3. Particle sizes weredetermined using a Beckman Coulter LS 13 320 par-ticle size analyzer and confirmed with SEM imageanalysis using a Philips XL-30 ESEM with an accel-erating voltage of 10 kV, after being coated with athin layer of gold.

To prepare bidisperse suspensions, equal volumesof two monodisperse suspensions were mixed bypipetting approximately 20 times and vortexing forat least 30 seconds. Prior to spin coating for thinfilms or water evaporation for thick films, the sus-pensions were sonicated for at least 20 minutes. Thinfilms were spin cast onto glass coverslips cleaned withethanol using a Headway Research, Inc. PWM32-PS-R790 spin coater. Typical spin speeds were between500 and 5000 RPM, the spin speed determined thefinal thickness of the film. [20]

Cabot Vulcan XC72R GP-3919 carbon black wassuspended in DI water at [CB] = 4.2 wt% with 1 wt%Pluronic F108 to stabilize the CB. Different volumesof the CB suspension were added to bidisperse sus-pensions of spheres to produce samples with differentfinal [CB].

To estimate the extinction lengths quoted in Ta-ble 1, the transmission spectra of aqueous suspen-sions of CB were measured using an Ocean Op-tics USB 650 Red Tide spectrometer. Suspensionsranging from 8×10−5 to 2×10−2 wt% were used.Measurements were made with three different pathlengths: 1 cm, 0.04 cm, and 0.03 cm. The ex-tinction length for all path lengths was proportionalto [CB]−1, allowing us to extrapolate the extinction

6

length to the [CB] range used in our thick film sam-ples. We use extinction instead of absorption becausewe did not discriminate between absorbed and scat-tered light.

SAXS measurements of biomimetic samples werecarried out at beamline X9 at the NSLS, BrookhavenNaitonal Laboratory, using a Rayonix Mar 165 CCDdetector. The X-ray energy was 7 keV (a wavelengthof 1.771 A) and the sample-to-detector distance was5 m. The conversion from the detector image to recip-rocal space was calibrated using the diffraction pat-tern from a standard silver behenate sample (q0 =0.1076 A−1). The first ring from silver behenate isout of the angular range covered by the detector at7 keV, therefore the standard pattern was collectedwith the same scattering geometry but at an X-rayenergy of 15.65 keV (0.792 A). The finite beam sizeat the detector corresponds to FWHM q resolutionof 0.00045 A−1, which is ∼17% of the width of thefringe produced by the spheres (π/120 nm ≈ 0.0026A−1). Biomimetic samples for SAXS measurementswere prepared on 0.0025”-thick Kapton Tape, pur-chased from McMaster-Carr (catalog no. 7648A33).

SAXS measurements of the feathers were carriedout at beamline 8-ID-I at the APS, Argonne NationalLabs.

Optical transmission spectra were performed usinga Hitachi U-2001 spectrophotometer. Optical reflec-tion and scattering spectra were performed with acustom-built setup in Hui Cao’s laboratory describedin detail in this journal [18].

References

[1] M. Srinivasarao, “Nano-optics in the biologicalworld: beetles, butterflies, birds, and moths,”Chemical reviews, vol. 99, no. 7, pp. 1935–1961,1999.

[2] P. Vukusic and J. R. Sambles, “Photonic struc-tures in biology,” Nature, vol. 424, 2003.

[3] V. L. Welch and J. P. Vigneron, “Beyondbutterflies—the diversity of biological photoniccrystals,” Optical and Quantum Electronics,vol. 39, pp. 295–303, 2007.

[4] E. R. Dufresne, H. Noh, V. Saranathan, S. G. J.Mochrie, H. Cao, and R. O. Prum, “Self-assembly of amorphous biophotonic nanostruc-tures by phase separation,” Soft Matter, vol. 5,no. 9, pp. 1792–1795, 2009.

[5] R. O. Prum, E. R. Dufresne, T. Quinn, andK. Waters, “Development of colour-producingbeta-keratin nanostructures in avian featherbarbs,” Journal of The Royal Society Interface,vol. 6, pp. S253–S265, 2009.

[6] R. O. Prum, R. H. Torres, S. Williamson, andJ. Dyck, “Coherent light scattering by bluefeather barbs,” Nature, vol. 396, pp. 28–29, 1998.

[7] A. R. Parker, “A vision for natural photonics,”Philosophical Transactions of the Royal SocietyA: Mathematical, Physical and Engineering Sci-ences, vol. 362, no. 1825, pp. 2709–2720, 2004.

[8] A. R. Parker and H. E. Townley, “Biomimeticsof photonic nanostructures,” Nature Nanotech-nology, vol. 2, pp. 347–353, 2007.

[9] E. Yablonovitch, “Inhibited spontaneous emis-sion in solid-state physics and electronics,” Phys.Rev. Lett., vol. 58, no. 20, pp. 2059–2062, 1987.

[10] J. D. Joannopoulos, R. D. Meade, and J. N.Winn, Photonic Crystals: Molding the Flow ofLight. Princeton University Press, 1995.

[11] S. Noda and T. Baba, Roadmap on PhotonicCrystals. Kluwer Academic Publishers, 2003.

[12] C. M. Soukoulis, Photonic Crystals and LightLocalization in the 21st Century. Springer, 2001.

[13] S. Kinoshita, S. Yoshioka, and J. Miyazaki,“Physics of structural colors,” Reports onProgress in Physics, vol. 71, no. 7, p. 076401(30pp), 2008.

[14] M. Muller, R. Zentel, T. Maka, S. G. Romanov,and C. M. S. Torres, “Photonic crystal films withhigh refractive index contrast,” Advanced Mate-rials, vol. 12, no. 20, 2000.

7

[15] B. T. Hallam, A. G. Hiorns, and P. Vukusic,“Developing optical efficiency through optimizedcoating structure: biomimetic inspiration fromwhite beetles,” Applied Optics, vol. 48, no. 17,pp. 3243–3249, 2009.

[16] Y. Takeoka, M. Honda, T. Seki, M. Ishii, andH. Nakamura, “Structural colored liquid mem-brane without angle dependence,” ACS Appl.Mater. Interfaces, vol. 1, no. 5, pp. 982–986,2009.

[17] R. P. Sear, “Phase separation and crystallisa-tion of polydisperse hard spheres,” EurophysicsLetters, vol. 44, no. 4, pp. 531–535, 1998.

[18] H. Noh, S. F. Liew, V. Saranathan, R. O.Prum, S. G. J. Mochrie, E. R. Dufresne, andH. Cao, “How non-iridescent colors are gener-ated by quasi-ordered structures of bird feath-ers,” Advanced Materials, preprint.

[19] Y. Chonde and I. M. Krieger, “Emulsion poly-merization of styrene with ionic comonomer inthe presence of methanol,” Journal of AppliedPolymer Science, vol. 26, no. 6, pp. 1819–1827,1981.

[20] P. Jiang and M. J. McFarland, “Large-scale fab-rication of wafer-size colloidal crystals, macro-porous polymers and nanocomposites by spin-coating,” J. Am. Chem. Soc, vol. 126, pp. 13778–13786, 2004.

8