2343The Journal of Experimental Biology 201, 2343–2347 (1998)Printed in Great Britain © The Company of Biologists Limited 1998JEB1393

PERSPECTIVE

THE DIVERSITY AND IMPLICATIONS OF ANIMAL STRUCTURAL COLOURS

ANDREW R. PARKER*Division of Invertebrate Zoology, Australian Museum, 6 College Street, Sydney, NSW 2000, Australia

*e-mail: arparker@laurel.ocs.mq.edu.au

Accepted 27 May; published on WWW 27 July 1996

,

Diffraction gratings were believed to be a rarecause of colour in nature. However, surface gratings,which include diffraction gratings and Bragggratings, appear to occur in many forms within a diversityof animals. Structural colours in general have

implications in the study of animal behaviour andevolution.

Key words: colour, structural coloration, light scattering, reflectiondiffraction grating, Bragg grating, iridescence.

Summary

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‘The finely colour’d feathers of some birds, and particularlythose of the peacocks’ tail, do in the very same part of the

feather appear of several colours in several positions of theye, after the very same manner that thin plates were found

do.’ (Isaac Newton, 1704,Optiks)

There is a vast body of literature documenting functioncolour in animals as the result of chemical pigmentation abioluminescence. There is, however, a third extensive categof animal light display: structural coloration. Structural colouresult from the selective reflectance of incident light due to physical nature of a structure. Employment of structucolours involves relatively little energetic expenditurcompared with bioluminescence and possibly the synthesispigment.

Newton (1704) was the first to identify an animal structurcolour, and Goureau (1843) and Rayleigh (1919) masubsequent fundamental discoveries. Süffert (1924) and Ma(1926, 1927a,b) later described the general differentiationstructural colours and pigment colours in animals, providingclassification of the former. The detailed study of thanatomical basis of structural colours accelerated following introduction by Anderson and Richards (1942) of the electrmicroscope to the subject.

In animals, structural colours are commonly known to resfrom (i) structures causing random scattering of light wav(e.g. Fig. 1A) or (ii) single or multiple thin-layer reflectors (e.gFig. 1B). Notable review papers are those by Denton (197Land (1972) and Herring (1994). However, the field may expanded with the inclusion of a third type of mechanisresponsible for structural colour: surface gratings, whiinclude diffraction gratings and Bragg gratings.

Surface gratings, like thin-layer reflectors, produc‘iridescent’ effects (some changing colour with orientatioothers appearing only as one colour). The shared spec

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(‘directional’)-type reflectance of multilayer reflectors anddiffraction gratings is indicative of the similarity of thephysical nature of the two reflector types. However, there atwo significant features that set these two systems apart. Fis the issue of the direction of the modified wavefront. Amultilayer reflector separates the incident wave into twcomponent waves: one that is transmitted and one thatreflected (Fig. 1B). These waves propagate according to tmirror-reflection laws. A diffraction grating, in contrast,separates the incident wave into many waves that propagatvarious directions set by the grating laws (Fig. 1C). The secofeature involves the orientation of the plane containing thperiodicity relative to the surface plane of the completstructure. In a diffraction grating, the plane with the periodicitis parallel to the surface plane (Fig. 1C); in a multilayereflector, it is perpendicular to the surface plane (Fig. 1BThese features give rise to a general classification that bredown a large complex subject into convenient categorieHowever, the physical processes cannot be ordered into ocategory or another and, indeed, a structure with a reflectimechanism which lies between that of a diffraction grating ana multilayer reflector is known in animals, the Bragg gratin(a term recently created to describe an analogous structdesigned for optical fibres). Bragg gratings will be considerein the category ‘surface gratings’, along with diffractiongratings, because they are surface structures, i.e. the plcontaining the periodicity is parallel to the surface plan(Fig. 1D). However, the mechanism of reflection is mossimilar to that of a multilayer reflector. A Bragg gratingconsists of a series of ridges where the ridge width, or periois λ/2n (where λ is wavelength and nis refractive index) andis almost like the edge of a multilayer reflector. One period cabe subdivided into two regions; one with a mean refractivindex that is close to that of the surrounding medium (air

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Fig. 1. Diagrammatic examples of the major categories of animal structural colours. (A) Scattering of white light by small particles(represented by black circles). If the particles are smaller than approximately 575 nm in diameter, more blue light will be reflected (‘scattered’)and more red light transmitted. If the particles are larger, all wavelengths will, on average, be reflected equally, and the resultant reflection willappear white. (B) Multilayer reflector. In this case, in a gold beetle, the reflector is ‘chirped’, but other forms of multilayer reflectors also existin animals (see Parker et al.1998c). (C) Diffraction grating, where the periodicity (w) is greater than or equal to the wavelength of violet light.(D) Bragg grating on the surface of a flattened seta.

water), and one with a mean refractive index that is closethat of the material of the animal structure (e.g. chitin). Colois observed in retroreflection when the illumination anobservation directions form a grazing geometry with respecthe surface plane (Fig. 1D).

Under the same incident white light, iridescent colours cappear much brighter than colour pigments when viewed frthe appropriate direction. This difference appears even mpronounced against a natural background where colpigments are present. Here, the chromatic effect of animpigmentation is modified by background radiation to a greaextent than the effect of iridescence. However, structu

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causing scattering produce effects rather comparable withose of pigments because the reflections are diffuse. comparison between diffuse and specular reflections can made when viewing a credit card; the coloured print (pigmenproduces a diffuse reflection while the reflection from thehologram (diffraction grating) is specular.

‘True diffraction by natural gratings occupies a place ofrelatively minor importance in the production of iridescence

in animals.’ (D. L. Fox, 1976, Animal Biochromes andStructural Colors)

Over the last 30 years or so, many cases of multilaye

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Animal structural colours 2345

reflectors have been discovered in nature, but until recediscoveries of natural diffraction gratings were rare. Feexamples had ever been suggested (Fox and Vevers, 1Fox, 1976; Nassau, 1983), and all the gratings hypothesisepre-electron microscope analyses have since been disprovsuch, with the iridescence observed resulting from multilareflectors. In fact, gratings have been established in only thgroups of animals: (i) in the beetle Serica sericea(Andersonand Richards, 1942) and other scarabaeids (Hinton and Gi1969; Hinton, 1973), although the periodicities involved heare sometimes questionably large (up to 5µm) and/or irregular;(ii) in wasps in the family Mutillidae (Hinton and Gibbs, 1969and (iii) in cypridinid ostracod crustaceans (Parker, 1995)has recently been found that natural surface gratings (includdiffraction gratings) are represented in animals in a varietyforms. These occur in a diversity of animals living on land aat the shallowest and deepest parts of the aquatic photic zfrom surface water in bright sunlight to 1000 m oceanic dep(the effective limit of sunlight penetration in the sea; Dento1990).

Surface gratings may be suitably accommodated on setae/setules, from which an extremely small and precreflection can result. Some surface gratings can reducereflection of white light more efficiently than a smooth surfacSuch an antireflection grating occurs on the corneas of cerflies and serves to increase photon capture by the eyes (Pet al.1998a). This diffraction grating is known as a zero-ordgrating because the optical behaviour is seen primarily in zero diffraction order. Zero-order gratings typically havperiodicities smaller than the wavelength of violet lighHowever, gratings that reflect first and higher diffraction ordeunder illumination normal to the surface plane may abecome antireflection structures when the angle of illuminatchanges.

‘Whenever colour has been modified for some specialpurpose, this has been, as far as we can judge, either fodirect or indirect protection, or as an attraction between

sexes.’ (Charles Darwin, 1859,On the Origin of Species byMeans of Natural Selection)

Colour is displayed in nature when the advantages of colour-producing structure outweigh its disadvantagAdvantages, however, may be associated with properties ocolour-producing structure other than the colour itself, whethe display of colour is a by-product (such as the red coloublood). Because needlessly attracting attention to onecarries obvious disadvantages, a structure that produiridescence from the external surface of an animal as a product may become modified, through selection, to prevsuch a high external reflection. The effect of a diffractigrating fades significantly when the grating period exceetwice the wavelength of light or becomes irregular. Therefoan almost colourless grating may be selected for whereflection has no behavioural advantage for the host. Selecof a colourless multilayer reflector occurs in Ovalipescrabs(Parker et al.1998b). In all species of Ovalipes, iridescence as

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a result of multilayer reflectors is a potentially useful means intraspecific communication. However, only those species Ovalipes that live at depths where only the blue portion osunlight remains can display iridescence in a plane parallel the sea floor and thus appear relatively inconspicuous to thpredators in the water column. These deep-water specpossess efficient multilayer reflectors in their cuticles. Inshallow waters, other colours exist, and these would breflected up into the water column where predators liveConsequently, the shallow-water species possess exoskeletwhere the component layers are too thick to form a multilayreflector in the visible region throughout most of their body.

In many invertebrates, the shells or exoskeletons displiridescence internally (e.g. Fig. 2C), but possess an opaqexternal surface which prevents light reaching the reflector (eFig. 2B). The internal layers of these structures contribustructural strength and comprise an ‘incidental’ multilayereflector (see Land, 1972). A similar case occurs icylindroleberidid ostracods (Crustacea), where the fine setaea comb (‘food filter’) form the ridges of a diffraction grating, butits iridescence (Fig. 2E) cannot be displayed external to thbivalved carapace that encloses the body of the ostracoAdditionally, iridescence which has a biological function can bhidden from external view when not required by the host. Foexample, some ostracods possess iridescent structures wherelight display has a function, and these can be withdrawn intheir carapace (Parker, 1995). Also, the iridescence of tanaid acallianassid crustaceans (Fig. 2A,D) is only visible when theare out of their tubes and burrows respectively.

Animal structures producing iridescence externally are ofteso efficient optically that colour display appears highlyselected for (e.g. Parker et al.1998c). Certain ostracods whichpossess surface gratings show an increase in the spectral puand reflectivity characteristics of their gratings throughevolution; the development of these gratings parallephylogeny (correlating positively with a conventionallyconstructed phylogeny) (Parker, 1995). In this caseiridescence was originally incidental to the primary mechanicfunction (Parker, 1998) in low-light regimes, becomingfunctional in high-light regimes. Additionally, there appears tobe a relationship between structural colour and thmorphology/evolution of compound eyes in ostracodcrustaceans (Parker, 1995). Another interesting point is thsome animals and plants have independently evolved the saintricate structural designs to produce the same iridesceeffect. For example, scarab beetles (Neville and Cavene1969) and the fern Danaea nodosa(Neville and Levy, 1986)possess microfibrils, which appear helicoidal on an obliquface, in their cuticles and fronds respectively. This forms reflector that is analogous to a ‘liquid crystal’ structure, whereach 180 ° rotation of the microfibrils forms a row of arcs or ‘layer’, and the whole structure effectively comprises a‘multilayer reflector’ (Land, 1972) or ‘three-dimensionaldiffraction grating’ (Nassau, 1983). Considering theparallelism, this design may be highly selected for as reflector.

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A. R. PARKER2346

The functions of structural reflectors include conspecirecognition, such as during courtship and aggregation (eParker, 1995), predator evasion (Denton, 1970; Hinto1973), colour filtering in eyes (Bernard, 1971), mirror-likoptical reflection (e.g. in eyes, photophores and iridophorHerring, 1994) and even reduction of reflection, such asthe moth eye (Miller et al. 1966) or in the eyes of certain

Fig. 2. Previously unreported examples ofiridescence from marine crustaceans(Arthropoda) photographed in water underwhite light. A and C result from multilayerreflectors, D from a Bragg grating and Efrom a diffraction grating. (A) Anteriorregion of the tanaid Tanais tennicornis,lateral view. (B) View of the externalsurface of the cheliped of a xanthid crab.(C) View of the internal surface of thesame section of a xanthid cheliped asshown in B. (D) Ventrolateral view of theterminal setae of pereiopod 3 from thecallianasid Callianassa arenosa. (E) Comb(‘feeding filter’) of a fourth limb from thecylindroleberidid ostracod Tetraleberisbrevis in motion (concealed by thecarapace in the living animal). Scale bars,0.5 mm.

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flies (Parker et al. 1998a). Determination that an animalreflector is highly efficient, physically, provides evidencetowards it having a function. However, this information ismore useful as an indicator of the potential for behaviourstudy than for speculation on function, considering tharduous task of deducing a function from experimentatiowith living hosts.

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Animal structural colours 2347

This work was funded by an Australian Research Coungrant.

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