Eurasian Jay Garrulus glandarius feathers display periodic variations in the reflected colour from white through light blue, dark blue and black. We find the structures responsible for the colour are continuous in their size and spatially controlled by the degree of spinodal phase separation in the corresponding region of the feather barb.
Our analysis shows that nanostructure in single bird feather barbs can be varied continuously by controlling the time the keratin network is allowed to phase separate before mobility in the system is arrested. Dynamic scaling analysis of the single barb scattering data implies that the phase separation arrest mechanism is rapid and also distinct from the spinodal phase separation mechanism i. Any growing lengthscale using this spinodal phase separation approach must first traverse the UV and blue wavelength regions, growing the structure by coarsening, resulting in a broad distribution of domain sizes.
The vibrancy and variety of structural colours found in nature has long been well-known; what has only recently been discovered is the sophistication of the physics that underlies these effects 1 , 2 , 3 , 4 , 5. Bird feathers have proved particularly important in our understanding of structural colour.
Iridescent feathers such as the tail feather of the male Peacock are a vibrant example of the wealth of possible colours. Robert Hooke, a founding father of optical microscopy was one of the first to examine the Peacock 6 , 7 and Duck 8 feathers in his revolutionary text Micrographia. He saw that by exposing them to water he could alter the intensity of the colour 9. Clyde Mason performed a comprehensive study of this effect for the case of the Blue Jay Cyanocitta Cristata.
He was able to optically contrast match the permeating solvent to that of the blue feather barbs using Canada balsam n 1. The conclusion of this repeated solvent exposure is that the blue colour is not due to a pigment, as this would not explain this switching off and on of the colour. In this paper we primarily focus on a comprehensive study of the Eurasian Jay and the origins of its structural colour. We also detail spatially modulated structures in a number of geographically diverse birds spanning the globe, from the two dominant types of isotropic structural colours found in nature.
These structure formation routes are categorized as sphere forming nucleation and growth and channel type spinodal decomposition. Initially we examine the Eurasian Jay, shown in Fig. This pattern is the same for both male and female. It is periodic on the macroscopic scale Fig. The purpose of these markings is still unclear but possible explanations include species recognition at a distance or as a sexual selection signal 12 where the ultra violet component of the signal could also play a role When the feather is seen in cross section Fig.
The microstructure of individual barbs shows a network of polygonal cells Fig. In e using a polarizer and an analyser in the optical path, it is possible to distinguish the polygonal cells boundaries, which look distinctly like Voronoi tessellation structures.
The blue colour in the barbs is located in the polygonal cells 22 due to a porous network with dimensions smaller than the wavelength of light When the grid pattern used for the SAXS scan is imposed on the optical image, the same effect is observed, see Fig. In b we can see how these two parameters are reflected in the real space correlation function. Two-dimensional Fourier analysis of electron microscopy images 17 showed that blue structural coloration in feathers is due to constructive interference between light waves, coherently scattered by a nanostructured keratin—air matrix.
Blue structurally coloured feathers are in effect Bragg reflectors 5 , Looking back in the scientific literature the proliferation of structural blues in nature had always been explained as a direct consequence of its origin as Tyndall scattering, and this was a widely held tenet in understanding this effect. The earliest observations of non-iridescent green feathers nearly always except for the pigment Turacoverdin found in Turacos consist of a pigment in combination with a structural blue 10 , 16 , 22 , 23 , Over years has passed since this comment and we have found very few examples of non-iridescent structural green, one comes very close 25 , however it still requires dispersion and absorption at short wavelengths.
The field at large did not take up this search, as the prevailing view was that the origin of the structural colour was due to Tyndall scattering. The question now finally arises after the discovery by Prum 17 of its true origin, if Tyndall scattering is not the cause of this optical effect then why do we not see a multitude of structural colours without the need for added pigment layers?
The isotropic photonic structures found in bird feather barbs come in two distinct morphologies, these are spherical nucleation and growth and channel spinodal 5. Recent measurements on the feather barbs of Cotinga maynana bird, a sphere type structure, demonstrated that these are limited to wide reflection spectra due to double scattering of light in these structures Even though these are able to produce very narrow primary reflection peaks, the secondary reflection peak will always be at a lower wavelength and so broadens the total effective reflectance.
The case for spongy spinodal structures will be highlighted later. Figure 2a is a scanning probe image of a dark blue region of the Jay feather, clearly showing the sponge morphology responsible for the colour. The long-range ordering of the cylinders is not critical to the creation of the overall structural colour, as light scattered by separate regions of the barb will not efficiently interfere. This lack of long-range periodicity in the spatial correlations explains why very little iridescence is observed in these bird species.
As such they have similar colour spectral appearance when viewed from various angles. The reflectance spectra Fig. Birds possess tetrachromic vision and have been shown to communicate using these wavelengths 12 , The peak in the reflectance spectra broadens in the transition from light blue to dark blue and eventually the reflection becomes white in colour. The Raman spectra Fig.
To probe the lengthscales present in the Jay feather we have used small angle X-ray scattering SAXS , which is a proven technique used to characterize the lengthscalesles present in a number of structurally coloured bird feathers Importantly no sample preparation is required, unlike a typical electron microscopy specimen, and the structure is therefore unperturbed. The colour map for the Jay feather in Fig. This data shows a periodic modulation of the domain size and consequently the structural colour as a function of position, which to date has not been seen in these quasi-ordered nanostructures.
Spatially modulated structural colour in bird feathers
The colour in Fig. Given the q-range available to us in our SAXS setup we were able to follow the large dynamic range in structure that the feather barbs span.
To date a handful of studies have examined structural whites 3 , In order to fully interpret the SAXS data and extract the real space morphology and transitions in size we have used one dimensional correlation analysis. An inversion of this type has been performed previously on a scattering dataset for the plum throated Cotinga Cotinga Maynana , a sphere forming structure This approach has also been used extensively in the field of semi-crystalline polymers, using the software known as CORFUNC to look at amorphous crystalline lamellae Using only the assumption that the sample is a two-phase system with differences in electron density, the auto-correlation function allows for the extraction of several properties of the underlying structure, such as the long period or the domain width of the phases.
Figure 4 shows the model and the relevant parameters, long period and domain width. The process involves fitting the low-q scattering data to a Guinier curve and the high-q data to a Porod curve, and then it is possible to create an extrapolation of the small angle x-ray signal that extends over all q. This extended function can then be Fourier transformed to return the auto-correlation of the electron density within the sample.
We have also found similar structural colour transitions like those found in the Jay for a number of geographically diverse avian feathers, including the Plum-throated Cotinga Cotinga maynana , British Kingfisher Alcedo atthis and the Indian Roller Coracias benghalensis. The transitions for these three bird species are displayed in Fig. The Cotinga shown in Fig. As such it has much higher local order when compared to the spinodal structures of the British Kingfisher and the Indian Roller.
We can see this clearly in the difference between the correlation function in Fig. The transition for the Cotinga from purple to blue is highlighted by the white dotted line in Fig. The British Kingfisher in Fig. The fact that we find similar colour transitions in a diverse array of birds from different regions of the globe shows that control over barb photonic structure is a general phenomenon. To further understand the structural colour and phase separation mechanism in the Jay we have performed a SAXS scan of a single feather barb Fig.
The same periodic pattern in oscillatory nanostructure is seen in the feather barb, using one dimensional correlation analysis we extract the peak length present at each point along the feather, clearly showing an oscillating pattern Fig. This validates our assessment that the oscillation in nanostructure is real and not due to the sampling of a number of barbs, as we have unambiguously mapped the structure for a single barb.
This points to a greater complexity in the mechanisms and nanoscale ordering present in the developing Jay feather 10 , allowing the optically active nanostructure to be controlled according to the position along the barb during growth. To reiterate, the lengthscale of the optically active nanostructure is not discrete and quantized; it has strong variation and tunability, based on the position along the feather barb.
The real space images for white, blue and black Fig. Previous work has postulated that the spongy keratin structures responsible for structural colour in feathers arise via the physical process of spinodal decomposition 32 , In order to prove this conclusively an analysis of the developing system is needed as a function of time. In our study of the Jay we examine single barb and so are able to compare a series of different effective phase separation timescales, albeit not from the same position.
Spinodal decomposition 32 , 34 is a process by which random fluctuations in composition of a liquid mixture are selectively amplified, resulting in a pattern which is spatially random but characterized by an inherent lengthscalele, giving a scattering pattern with a characteristic peak, as seen in figure Fig. At a later stage, the phase separation pattern coarsens, creating larger domains to minimize total interfacial energy 34 , The increase in lengthscale can be seen in reciprocal space by the shift in the peak position q m to smaller wave vectors Figure SI 5 , in real space this is an increase in the long period lengthscale shown clearly in Fig.
Otherwise the structure would simply phase separate and it would not be possible to have the spatially modulated photonic structures that we have directly measured using SAXS in this work. The entire barb would have to reach some end point and be all one colour. Our work suggests that in the Jay feather, it is by controlling the duration of the phase separation process before this arrest takes place, which provides modulation and fidelity over the feather colour.
The ability to arrest the phase separation at any point in the coarsening process is what leads to the continuous tuning of colour.
Potential mechanisms for arresting phase separation can be physical, for example, crystallization or other physical association mechanisms in the macromolecule-rich phase, or chemical, through the formation of a cross-linked network Currently we are unable to identify the biological mechanism at work here, but further analysis does give a clue as to its character. In late stage spinodal decomposition, theory shows simple systems are characterized by the remarkable property of self-similarity. As coarsening proceeds, the evolving structures are self-similar — that is, a pattern at later time is, on a statistical basis, simply a magnification of the pattern at an earlier time.
This self-similarity is manifested most clearly as a simple scaling property of the scattering curves. Figure 6f shows the results of this dynamic scaling analysis applied to the single barb SAXS scattering data 37 , 38 , The failure of the curves to totally superpose indicates that strict self-similarity does not apply.
But a comparison of this case with another study of phase separation in a biopolymer system 40 suggests that the departure from self-similarity is much weaker than in situations when the arrest of phase separation is effected by the simultaneous and slow process of intermolecular association. This suggests that the phase separation arrest mechanism occurs over a time-scale that is widely separated from the time-scale characterizing the phase separation and coarsening, implying a two-stage process.
Spatially modulated structural colour in bird feathers | Scientific Reports
Spongy-type structural colour reflectors are versatile in their range and flexibility, from the UV through the visible, with tremendous variation in the possible colours when combined with pigments The explanation for why blue producing spinodal structures are able to make a blue structural colour using a broad size distribution is that humans do not see wavelengths in the UV. As spinodal structures may exhibit a spread in lengthscales, and therefore significant short wavelength reflectance in the UV spectrum, without affecting the reflected blue colour.
As opposed to previous works, the data we present comprise the full range of spinodal lengthscales without gap, proving conclusively that we have shown that the structural colour from this spinodal structure is constrained to UV, blue and white, and so requires the use of pigments for the full colour range.
This use of pigments to augment the spinodal and sphere type structural colours is common in the Natural world. In particular yellow carotenoid pigments are common in bird feathers, however green pigments are particularly rare in animals; as such other architectures for producing structural greens may be too complex to evolve in feathers particularly if iridescence is not selected for. An example of one of the very few known non-angular dependent structural greens is made using a true photonic structure that is found in the elytra of the African Longhorn Beetle Prosopocera lactator see Fig.
To circumvent the iridescence that this photonic structure would normally produce, the elytra is made up of small locally ordered domains that are arranged in different orientations to disrupt iridescence In Fucales, structural color only occurs in Cystoseira spp. For example, in C. In brown algae, structural color is confined to two orders, Dictyotales and Fucales. Ancestors of Dictyotales Sphacelariales and Syringodermatales diverged from the rest of the brown algae in the Jurassic followed by the divergence of the Dictyotales about Mya.
Fucales, the only other group to retain or independently evolve structural color, diverged more recently at the end of the Cretaceous, at ca. The distribution of structurally colored brown algae was determined through an extensive literature search. Structural color in the different species was recorded throughout 10 geographical distributions adapted from ref. The presence or absence of structural color represents cases only where a species was recorded as structurally colored or nonstructurally colored in situ. For example, Dictyota dichotoma is often described as exhibiting such color and is widely distributed geographically, but only four cases were found where it had been recorded as structurally colored in situ Table 2.