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Review
. 2009 Apr 6;6 Suppl 2(Suppl 2):S149-63.
doi: 10.1098/rsif.2008.0366.focus. Epub 2008 Dec 15.

Mechanisms and behavioural functions of structural coloration in cephalopods

Lydia M Mäthger  1 , Eric J Denton, N Justin Marshall, Roger T Hanlon
Affiliations
Review

Mechanisms and behavioural functions of structural coloration in cephalopods

Lydia M Mäthger et al. J R Soc Interface. .

Abstract

Octopus, squid and cuttlefish are renowned for rapid adaptive coloration that is used for a wide range of communication and camouflage. Structural coloration plays a key role in augmenting the skin patterning that is produced largely by neurally controlled pigmented chromatophore organs. While most iridescence and white scattering is produced by passive reflectance or diffusion, some iridophores in squid are actively controlled via a unique cholinergic, non-synaptic neural system. We review the recent anatomical and experimental evidence regarding the mechanisms of reflection and diffusion of light by the different cell types (iridophores and leucophores) of various cephalopod species. The structures that are responsible for the optical effects of some iridophores and leucophores have recently been shown to be proteins. Optical interactions with the overlying pigmented chromatophores are complex, and the recent measurements are presented and synthesized. Polarized light reflected from iridophores can be passed through the chromatophores, thus enabling the use of a discrete communication channel, because cephalopods are especially sensitive to polarized light. We illustrate how structural coloration contributes to the overall appearance of the cephalopods during intra- and interspecific behavioural interactions including camouflage.

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Figures

Figure 1
Figure 1
(a) Iridescent spots in the squid Loligo pealeii. (b) Blue–green iridescence and white scattering leucophore stripes in cuttlefish (Sepia apama). (c) Camouflaged S. apama with pink iridescent arms and white markings caused by leucophores. (d) White leucophores in S. apama. (e) Skin in cross section showing the location of chromatophores (ch.) and structural reflectors (ir., iridophores; leuc., leucophores) in cephalopods. (f) Close-up of cuttlefish skin (Sepia officinalis) showing chromatophores (yellow, expanded; dark brown, partially retracted; orange, retracted) and white leucophores. Scale bar, 1 mm. (g) Brown, red and yellow chromatophores of squid (L. pealeii). Scale bar, 1 mm. (h) Combination of chromatophores and iridophores to illustrate the range of colours. Scale bar, 1 mm. (i) Electron micrograph showing iridophore plates (ir.) and spherical leucophores (leuc.) of cuttlefish (S. officinalis) skin. Scale bar, 1 μm (image courtesy of Alan Kuzirian).
Figure 2
Figure 2
(a) Spectral reflectance of iridophores (L. pealeii) at different angles of incidence and planes of polarization, showing that with increasing angle of incidence (i.e. 40° and 45°) the reflected light shifts towards the shorter end of the spectrum and becomes polarized. Two reflectance spectra are shown for each angle of incidence: the spectrum reflected in the plane parallel to the plane of incidence and the perpendicular plane of incidence. At oblique angles (40° and 45°), the spectral reflectance in the perpendicular plane is much reduced in comparison with the parallel plane, indicating that the reflected light is linearly polarized. (b) The visibility of the ‘red’ stripe of squid from different orientations taking into account the light distribution in the sea. (i) An observer looking down on a squid will not see any iridescence. (ii) An observer looking down at a squid from a 45° angle will see iridescence from the most anterior and posterior ends of the stripe. (iii) An observer looking directly from the side will see strong iridescence from the entire stripe. See Mäthger & Denton (2001) for more details (modified from Mäthger & Denton 2001). (c) Acetylcholine (1 mM) changes iridescence from non-reflective (black lines, reflectance in IR) through various IR steps (black and grey lines) to red reflective in the squid L. pealeii. Measurements taken at 15 s intervals.
Figure 3
Figure 3
(a–d) Close-up images of L. pealeii skin showing chromatophores and iridophores. Chromatophores can be used to modulate iridescence. Light reflected from iridophores filtered through (e) a yellow and (f) a brown chromatophore. Reflectance spectra of (g) yellow and (h) brown chromatophore.
Figure 4
Figure 4
(a) Blue-ringed octopus, Hapalochlaena lunulata, well camouflaged in a laboratory tank. Note the muted iridescent blue rings. (b) Bright blue iridescence is typically seen when a blue-ringed octopus flashes its rings. (c) Electron micrograph of the blue rings, showing closely packed iridophore plates (scale bar, 1 μm).
Figure 5
Figure 5
(a) Silvery iridescence around the eyes of squid (L. pealeii). (b) Close-up of the section highlighted in (a) showing variations in spectral reflectance. (c) Spectral reflectance on both planes of polarization at 45° incidence (black and grey lines), showing that the light reflected from silvery reflectors is not polarized. (d) Electron micrograph of silvery reflectors in cross section, showing wavy arrangement of reflective plates. (e) Orientation of the reflective plates of silvery eyes obtained using the techniques described in the text. The reflective plates (short, thick black lines) are tilted towards the vertical, much like the reflectors on the scales of the silvery fish. (f) Orientation of the reflective plates of golden silvery stripe along the lateral side of the oceanic squid Todaropsis. Reflective plates are also oriented towards the vertical. (g) Electron micrograph of Todaropsis golden silvery stripe, showing a chromatophore (chr.) and iridophore plates (ir.).
Figure 6
Figure 6
Whiteness in cuttlefish is created by scattering of light from leucophores. (a) Disruptive pattern, (b) zebra pattern, (c) close-up of white square, (d) close-up of zebra pattern, (e) close-up of white finspot, created by leucophores. Note the chromatophores in the superficial layer; chromatophores can modulate whiteness. (f) Scanning electron micrograph of leucophores showing spherical arrangement of leucosomes (courtesy of Alan Kuzirian).
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