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Mechanisms and behavioural functions of structural coloration in cefalopods

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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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REVIEW
Mechanisms and behavioural functions of
structural coloration in cephalopods
Lydia M. Ma
¨thger
1,2,3,
*
,†
, Eric J. Denton
3,‡
, N. Justin Marshall
2
and Roger T. Hanlon
1
1
Marine Biological Laboratory, Woods Hole, MA 02543, USA
2
Sensory Neurobiology Group, School of Biomedical Sciences, University of Queensland,
Brisbane, Queensland 4072, Australia
3
Marine Biological Association of the UK, Citadel Hill, Plymouth PL1 2PB, UK
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 activelycontrolled 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.
Keywords: iridescence; multilayer reflector; light diffusion; leucophore
1. INTRODUCTION
Animals can be extraordinarily colourful. There are
innumerable examples in both the vertebrate and
invertebrate worlds, and, while in some animals these
colours function to camouflage their owners, in others
they have clear functions in signalling, and some may
even perform both functions simultaneously.
Colour is produced by either a structural or
pigmentary medium. Structural coloration involves
materials that are themselves colourless—the colours
are created by coherent scattering. A pigmented
material has selective absorbance properties that
determine the spectral reflectance of the incident light.
Cephalopods (squid, cuttlefish, octopus) show an
impressive repertoire of body patterns for camouflage
and signalling, despite their apparent colour blindness
(Holmes 1940;Brown & Brown 1958;Packard &
Hochberg 1977;Hanlon 1982;Moynihan 1985;Hanlon&
Messenger 1988,1996;Marshall & Messenger 1996;
Hanlon & Shashar 2003;Ma
¨thger et al. 2006; but see
examples of cephalopod with colour vision, e.g. Kito
et al. 1992;Michinomae et al. 1994). What is even more
impressive is their ability to almost instantaneously
change colour and pattern. This is mediated by the dual
action of thousands of chromatophores, which are small
pigmented organs (grouped into two or three colour
classes depending on the species: red; yellow/orange;
and brown/black), and structural reflector cells (irido-
phores and leucophores) (Williams 1909;Scha
¨fer 1937;
Cloney & Brocco 1983;Messenger 2001;figure 1). The
appearance of the animal thus depends on which skin
elements affect the light incident on the skin. Light may
be reflected by either chromatophores or structural
reflectors, or a combination of both, and it is the
physiological changeability of the chromatophores and
iridophores that enables these animals to produce such
a wide repertoire of optical effects.
J. R. Soc. Interface (2009) 6, S149–S163
doi:10.1098/rsif.2008.0366.focus
Published online 15 December 2008
One contribution of 13 to a Theme Supplement ‘Iridescence: more
than meets the eye’.
*Author and address for correspondence: Marine Biological Labora-
tory, Woods Hole, MA 02543, USA (lmathger@mbl.edu).
Some of the presented material was part of L.M.M.’s postdoctoral
research, Sensory Neurobiology Group, School of Biomedical
Sciences, University of Queensland, Brisbane, Queensland 4072,
Australia, and PhD, Marine Biological Association of the UK, Citadel
Hill, Plymouth PL1 2PB, UK.
Deceased (2 January 2007).
Received 28 August 2008
Accepted 19 November 2008 S149 This journal is q2008 The Royal Society
A chromatophore consists of a pigment-containing
sac that has dozens of radial muscles attached to its
periphery. These muscles are innervated directly
by the brain, and by contracting and relaxing the
chromatophore muscles the pigment sac increases or
decreases in area ( Florey 1969) in less than a second
(Hill & Solandt 1935). Chromatophore size varies among
cephalopods. In squid, such as Loligo plei, an expanded
chromatophore may be up to1.5 mm in diameter, while a
retracted chromatophore may be barely visible to
the naked eye, measuring as little as a tenth of a
millimetre (Hanlon 1982;Ma
¨thger & Hanlon 2007).
ch.
ir.
leuc.
ir.ir.
leuc.leuc.
(c)
(f)
(g)
(e)
(h) (i)
(d)
(a) (b)
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 mm (image courtesy of Alan Kuzirian).
S150 Review. Structural coloration in cephalopods L. M. Ma
¨thger et al.
J. R. Soc. Interface (2009)
By selectively expanding and retracting distinct
groups of chromatophores, cephalopods can produce an
array of patterns, such as bands, stripes and spots.
In this review, we deal mainly with the other optical
system that interacts with light—the different types of
structural reflectors. Various cell arrangements have
been identified and described in the cephalopod
literature: (i) those that produce iridescence, a working
definition of which would be the production of rainbow-
like colours or a metallic sheen, and (ii) those that
produce scattering broadband diffuse reflectance, the
most striking of which are the distinct white body
markings of many cephalopod species.
2. IRIDESCENCE
There has been some confusion about the various terms
that have been introduced in the literature to describe
cephalopod skin structures that produce iridescence.
For example, Cloney & Brocco (1983) used the term
‘reflector cell’ (containing plates that are arranged into
distinct groups, called reflectosomes) to describe the
cells that produce iridescence by thin-film interference,
whereas ‘iridocytes’ were described as cells that
function by diffracting light. Iridescent cells whose
optical mechanisms were unclear were termed ‘irido-
phores’ following these authors’ definition; iridophores
contain a number of iridosomal plates that are grouped
into iridosomes. These plates (along with the spaces
separating them) are ultimately responsible for the
observed iridescence. Since the 1980s, there have been
several studies looking at the ultrastructure, optical
mechanisms and composition of iridescent cells in
cephalopods, some of which have revealed inconsisten-
cies with the definitions of Cloney & Brocco (1983). For
example, in their paper, the iridescent cells of squid
were described as iridocytes, implying that they
function as diffraction gratings. This has not been
confirmed—on the contrary, all existing papers show
evidence that squid reflectors are multilayer reflectors,
i.e. they reflect light by thin-film interference, which
would warrant the term reflector cell. However, in the
more recent literature, these cells are consistently
referred to as iridophores. This review will be consistent
with these recent publications insofar as iridophores are
defined as the cells that produce iridescence.
In this paper, we deal mainly with multilayer
reflectance, rather than diffraction, because to date,
there is no convincing evidence that diffraction is
responsible for iridescence in cephalopod skin. Diffrac-
tion gratings differ from multilayer reflectors, in that
the structures producing iridescence are oriented in the
same plane as the surface. They are characterized by an
orderly array of ridges that are ‘engraved’ into the
surface. Diffraction gratings produce spectra on the left
and right sides of the zero order (the direction of the
incident light beam) and have been shown to be the
basis of iridescence in some beetles, wasps, ostracod
crustaceans and butterflies (Hinton & Gibbs 1969;
Parker 1995;Brink & Lee 1999). Certainly, considering
the large number of modern cephalopod species (over
700) (Hanlon & Messenger 1996), it may nevertheless
be possible that both diffraction gratings and
multilayer reflectors play a role in creating iridescence,
but evidence thus far suggests that only multilayer
reflectors are involved.
2.1. ‘Spectral’ iridescence
Cephalopods have iridophores in many parts of the
body and they have precise arrangements that may
signify specific functions. Squid generally have only
iridophores, i.e. they do not have the broadband
reflecting leucophores found in octopus and cuttlefish
(some species of the squid genus Sepioteuthis may be an
exception; see §3). In most parts of the body (e.g.
mantle and head), the iridophores are located in a
distinct layer beneath the pigmented chromatophores
(Williams 1909;Scha
¨fer 1937;Mirow 1972a,b;Hanlon
1982;Cloney & Brocco 1983). Iridophores are colourless
cells that vary in size but are generally smaller than
1mm(Mirow 1972b;Cooper et al. 1990). They contain
stacks of thin plates that reflect light by thin-film
interference (Denton & Land 1971;Land 1972;
Ma
¨thger & Denton 2001;Ma
¨thger et al. 2004). Light
reflected from a multilayer reflector is almost always
coloured, as long as two prerequisites are met: (i) there
is a difference in the refractive index between the plates
and the spaces separating them, and (ii) the plates and
spaces have a specific thickness for the constructive
interference of light to occur. The mechanism of
reflectance is the same as that of coloured soap bubbles.
If the soap film (or multilayer plate) is very thin,
shorter wavelengths are reflected, e.g. blue light; if it is
thicker, longer wavelengths, such as yellow and red, are
reflected (Boys 1959;Huxley 1968).
Multilayer reflectors have distinct optical features,
the most obvious of which is the effect of changing the
angle of illumination/observation on the spectrum of
the reflected light. The more oblique the angle, the
shorter the peak wavelengths of the reflected light, i.e. a
multilayer reflector that appears red at near-normal
viewing angles will appear first yellow, then green and
blue at increasingly oblique angles (figure 2a). This may
seem counterintuitive, and, for the interested reader,
we point out that the book by Boys (1959) has a
beautifully written section on this optical phenomenon.
Furthermore, at around Brewster’s angle (angle at
which maximum linear polarization occurs), the
reflected light is highly polarized (figure 2a), an
interesting property that may have some behavioural
function because cephalopods have the ability to detect
polarized light (see below).
Some species of squid (such as Loligo vulgaris,Loligo
forbesii,Loligo pealeii,Alloteuthis subulata,Sepioteuthis
australis,Loliolus noctiluca,Euprymna tasmanica,
Todaropsis eblanae and probably others) appear to
have prominent red-reflecting iridophore stripes
arranged longitudinally on each side of the mantle
(figure 2a,b). These are arranged in either distinct
stripes or ‘splotches’. Ma
¨thger & Denton (2001)
suggested that these iridophores may aid in communi-
cation between individuals of a school. Although the
availability of daylight in the red parts of the spectrum is
much reduced at the depths at which these squid live,
the majority of the reflective plates of these iridophores
Review. Structural coloration in cephalopods L. M. Ma
¨thger et al. S151
J. R. Soc. Interface (2009)
are oriented approximately parallel to the skin surface,
which means that shorter wavelengths (green and blue)
are reflected in a horizontal direction. This would make
the stripes highly visible when viewed horizontally,
because green and blue are the most prominent
wavelengths found in the light environments these
animals inhabit (such as the example given in
figure 2b, calculated for a depth of 19 m; Ma
¨thger &
Denton 2001). Furthermore, the patterns change
dramatically with direction and movement of the
squid, so that they may be used by squid to coordinate
the movements of individuals of a school.
Squid are able to change their iridescence depending
on behavioural context, showing iridescence especially
during agonistic encounters (Hanlon 1982). In vitro,
iridescence is changed by the topical application of
acetylcholine (ACh) acting on muscarinic cholinergic
receptors (Hanlon 1982;Cooper & Hanlon 1986;
Cooper et al. 1990;Hanlon et al. 1990;Ma
¨thger et al.
2004). However, in contrast to the chromatophores that
can change within a fraction of a second, iridophore
reflectance changes take longer, e.g. several seconds to
minutes. In L. pealeii, the reflected wavelengths have
been shown to shift by over 100 nm (Ma
¨thger & Hanlon
2007), from non-reflective to red and orange after the
application of ACh. The reflectance changes in vitro
typically take several seconds (up to 1–2 min). Inter-
estingly, in L. pealeii, the collar region (anterior end) of
themantlehashighlyreectiveiridophoresina
tightly packed arrangement, and this group has been
shown to reflect in the IR parts of the spectrum
(approx. 800 nm) when they appear non-reflective to
the human eye (figure 2c).
To date, it is not known exactly how this wavelength
change is achieved. Recent evidence has provided
confirmation that the plates of squid iridophores are
made up of proteins called reflectins (Crookes et al.
2004); see also Cooper et al. (1990), who pointed out
that a protein state change (affecting refractive index)
combined with a change in the thickness of plates could
explain the observed changes in reflectance.
The squid reflectin protein has received interest from
researchers in the fields of materials science and optical
nanotechnology. For example, Kramer et al. (2007)
showed that reflectin proteins have self-assembling
properties and that they can be processed into thin
films, photonic grating structures and fibres that could
find various applications in society.
Another way of changing iridescence is by selectively
expanding and retracting the overlying chromatophores.
Since chromatophores are innervated directly from the
0
20
40
60
80
100
400 500 600 700 800 900 1000
wavelen
g
th (nm)
reflectance (arb. units)
0
20
40
60
80
100
(a)
(b)
(c)
400 500 600 700 800
wavelength (nm)
reflectance (arb. units)
10°40°45°
±30°
±30°
±30°
off
on
(i)
(ii)
(iii)
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. 408and
458) 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 (408and
458), 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 458angle 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 Ma
¨thger & Denton (2001) for more details
(modified from Ma
¨thger & 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.
S152 Review. Structural coloration in cephalopods L. M. Ma
¨thger et al.
J. R. Soc. Interface (2009)
brain, this effect can be immediate. Chromatophores are
generally located in a distinct layer above the iridophores
and, by selective expansion, they can either change the
reflected spectrum of the iridescence (figure 3ae; see also
Ma
¨thger & Hanlon 2007), create contrast against which
iridescence is viewed (see, for example, the blue iridescent
rings of the blue-ringed octopus; figure 4b) or block it
altogether, such as a brown chromatophore expanding
over reflective iridophores (figure 3f).
Some of the aforementioned squid (L. vulgaris,
L. pealeii,A. subulata and L. noctiluca) also have a
blue reflective stripe along the side of the mantle (see
Ma
¨thger & Denton 2001). These iridophores are best
seen when observed and illuminated from above the
animal (rather than from a horizontal direction where
the ‘red’ stripes are visible), and we speculate that they
may function in ways similar to the red stripes
described above: since the reflectance pattern and
intensity change with the movements of the animal,
other members of a school may be able to use this
information to coordinate their movements.
In all pelagic squid studied so far (namely L. vulgaris,
L. pealeii and L. noctiluca), the ventral iridophores
reflect red light, when viewed and illuminated from the
side (see Ma
¨thger & Denton 2001). The iridophores
making up the ventral side are densely packed and their
flat surfaces make an angle of approximately 608with
the skin surface. Owing to this orientation, when the
iridophores are viewed at oblique angles of incidence
(such as from below), the light reflected from the
iridophores comes from the inside of the mantle
(see fig. 16 in Ma
¨thger & Denton 2001). This may have
0
25
50
75
100(e)(f)
(g)(h)
reflectance
(arb. units)
0
5
10
400 450 500 550 600 650 700
wavelen
g
th (nm)
400 450 500 550 600 650 700
wavelen
g
th (nm)
reflectance
(%)
green
iridescence
yellow chromatophore
over green iridescence
red
iridescence
brown chromatophore
over red iridescence
(a) (b)
(c) (d)
Figure 3. (ad) 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.
Review. Structural coloration in cephalopods L. M. Ma
¨thger et al. S153
J. R. Soc. Interface (2009)
an interesting function. Midwater animals are most
visible when seen from below against the background of
the strongest radiance in the sea. Any downwelling light
that is absorbed by the animal cannot be replaced by the
reflections of light from any other direction (biolumines-
cence is the only solution to this problem). Being
transparent makes a midwater animal less likely to be
detected by the predators lurking below, and in
comparison with other muscular animals, such as
fishes, cephalopods can be very transparent. However,
total transparency is impossible because the internal
organs (e.g. ink sac, digestive tracts) cannot be made
transparent. The dorsal mantle iridophores transmit a
great portion of the incoming light into the mantle
cavity. The light that enters the mantle cavity then falls
on the ventral iridophores obliquely and is channelled
downwards. This may help mitigate shadows cast to an
observer below the animal (Ma
¨thger & Denton 2001).
Benthic cephalopods, such as Sepia officinalis and
E. tasmanica, also have densely packed iridophores
lining their ventral mantle, but instead of reflecting red
light as the above squid species, they strongly reflect
green light when viewed and illuminated side-on. In
E. tasmanica, for example, the iridophores lie at an
angle of approximately 508with the skin surface. Sepia
and Euprymna are much more opaque than most
pelagic cephalopods, and it appears unlikely that any
considerable amount of light enters the mantle cavity to
be channelled downwards in the manner described
above, so their function is unknown.
The blue-ringed octopus is well known for its
potentially deadly bites and flashing blue rings. It was
previously suggested that this blue iridescence may be
the result of the Tyndall scattering (Herring 1994).
However, we found that ultrastructural analysis of the
rings and lines of Hapalochlaena fasciata (the blue-lined
octopus) reveals densely packed reflective plates (up to
approx. 30 in one iridophore) grouped together in a
parallel arrangement, suggesting that the blue irides-
cence is caused by multilayer constructive interference
(figure 4), which would warrant the term reflector cell
following Cloney & Brocco’s (1983) definition
(however, see above for the reasoning behind calling
iridescent cells iridophores). Spectrometer measure-
ments have confirmed this (data not shown). Each
iridophore appears to be oriented at a different angle
relative to the surface of the skin, and this correlates
well with the optical appearance of the rings: the blue
iridescence is visible from a wide range of angles. The
reflective plates have thicknesses of approximately
70 nm. This appears to be the thickness required for
this stack to act as an ideal quarter-wave reflector for
which l
max
Z4nd, where nis the refractive index and d
is the actual thickness of the plate. Assuming a
refractive index of 1.59 (Kramer et al. 2007), the
wavelength of maximum reflectance of the blue-ringed
iridophores would be at 445 nm.
Tyndall scattering may nevertheless be a method of
producing the blue iridescence in some cephalopod
species. For example, Octopus bimaculatus has two
characteristic blue rings (often referred to as ‘ocelli’) on
each side of its head, near the eyes. This has been
attributed to the Tyndall scattering from fine purine
granules (Fox & Vevers 1960;Fox 1976;Packard &
Hochberg 1977). There may also be other squid species
in which the Tyndall scattering produces the blue
iridescence. Herring (1994) suggested that the blue
flashes of the squid Onychia caribbaea are produced by
the expansion of dark chromatophores beneath a blue-
reflecting Tyndall scatterer.
2.2. Iridophore polarization and optical
enhancement of chromatophores
For human observers, creating colour is probably the
most notable aspect of cephalopod iridophores for
our eyes. However, when viewed at oblique angles,
(a)
(b)
(c)
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 mm).
S154 Review. Structural coloration in cephalopods L. M. Ma
¨thger et al.
J. R. Soc. Interface (2009)
cephalopod iridophores also polarize light (Shashar &
Hanlon 1997;Ma
¨thger 2001;Shashar et al. 2001;
Ma
¨thger & Hanlon 2006;Chiou et al. 2007). Light is
polarized most strongly at Brewster’s angle (q), which
is simply defined as follows: tan qZn
1
/n
2
, where n
1
and n
2
are the refractive indices of the two media (e.g.
going from a watery surrounding, nZ1.33, to protein,
nZ1.59, Brewster’s angle is approx. 508).
For cephalopods, this may have a useful behavioural
function. Cephalopods have a rhabdomeric visual
system that allows them to detect linearly polarized
light (Moody & Parriss 1960;Shashar & Cronin 1996;
Shashar et al. 1998,2002), and it is therefore
conceivable that the polarized aspect of iridescence
may have communication functions (Cronin et al. 2003;
Boal et al. 2004). This has also been termed a ‘hidden
communication channel’ because cephalopod preda-
tors, such as teleost fish, sharks and marine mammals,
are believed not to be polarization sensitive and would
therefore not be able to perceive this sort of visual
information (Shashar et al. 1996;Land & Nilsson 2002;
Boal et al. 2004;Ma
¨thger & Hanlon 2006).
In cephalopod skin, polarization is a ‘side product’ of
iridescence, and iridescence can be very conspicuous.
This is where having a variety of optical structures in
the skin is beneficial. In a study on L. pealeii, it was
shown that the polarized aspect of iridescence is
maintained after passing through the overlying pig-
mented chromatophores, which produce the most
visible and dynamically changeable aspect of camou-
flage patterns in cephalopods (Ma
¨thger & Hanlon 2006,
2007). Cephalopods are polarization sensitive and can
regulate polarization via skin iridescence (Shashar &
Hanlon 1997;Ma
¨thger & Denton 2001;Chiou et al.
2007). Two behavioural functions come to mind. First,
it is conceivable that they could send polarized signals
to conspecifics while using chromatophores to regulate
the potentially conspicuous iridescence and stay
camouflaged to fishes or mammalian predators, most
of which are probably not polarization sensitive
(Land & Nilsson 2002). Second, they could use
polarization signals during intense intraspecific
interactions (sexual selection); Boal et al. (2004)
found that females showed more polarization signals
than males and also changed their behaviour in
response to polarized patterns. Boal et al.’s results
suggest (but did not prove) that females may use
polarized signals as a source of information about
conspecifics (e.g. species, sex, location, size).
Iridophores are generally located just beneath the
pigmented chromatophores (there are some exceptions
to this) and the final appearance of the animal is
frequently the result of the optical interactions between
iridophores and chromatophores. Chromatophores are
very thin when expanded and can filter light reflected
from the iridophores; or, turning this idea around,
iridophores can enhance the chromatophores’ appear-
ance. Ma
¨thger & Hanlon (2007) showed evidence that
three colour classes of pigments (yellow, red and brown),
combined with a single type of reflective cell (with
dynamic iridescence), produce colours that encompass
the whole of the visible spectrum, enabling the extreme
visual diversity for dynamic camouflage and signalling.
3. BROADBAND REFLECTANCE AND
SCATTERING
3.1. Broadband ‘silvery’ reflectors
Cephalopods have very striking silvery iridescence
around their eyes (figure 5a,b). This was studied in
detail for A. subulata and L. vulgaris and it was shown
that, unlike the iridophores described above, the
reflected wavelengths do not change with angle of
incidence/view (Ma
¨thger 2001) and the reflected light
is not polarized at oblique angles (figure 5c). When
viewed closely, the skin shows some variations in colour
on a scale of a few micrometres (figure 5b). Some parts
reflect red, others green and blue and the reflective
properties of each of these microscopic parts are typical
of multilayer reflectors: with increasing angle of
incidence, the reflected wavelengths move towards the
shorter end of the spectrum and become polarized.
When viewed from a distance, however, the various
coloured parts merge together and the net effect is the
reflectance of unpolarized white light. Ultrastructu-
rally, we can see that the stacking sequence of the plates
and spaces is responsible for the silvery appearance
(figure 5d). The plates are long (more than 10 mm) and
wavy with varying thicknesses (ranging from 80 to
130 nm) and irregular spaces between them, which
facilitates this broadband reflectance. This natural
pointillistic approach to creating colour can also be seen
in Ribbonfish (Trichiurus spp.), whose silvery surface
is covered with fine streaks that show a variety of
colours when examined microscopically (Nicol &
Van Baalen 1968).
The orientation of the reflectors relative to the
surface of the skin offers a clue to the possible function
of this iridescence (figure 5e). These measurements
were obtained following the methods described
originally by Denton & Nicol (1962). A piece of silver
foil is placed adjacent to the reflective area under
investigation, and, using a goniometer, the difference
in angle between the light reflected from the foil
(which equals the skin surface) and the reflector
(which may or may not be angled with respect to the
skin surface) is measured. These measurements show
that the reflective plates are tilted towards the true
vertical. Figure 5eshows that the reflectors in the
dorsal and ventral areas are oriented at an angle with
respect to the skin surface, while those in the anterior
and posterior areas lie parallel. This arrangement
would give close to perfect camouflage, much like that
in silvery fish: the reflectors reflect light as a mirror
suspended vertically in the sea. The orientation of the
reflective plates is such that the light reflected from
almost any angle equals the intensity of the back-
ground light against which the animal is viewed
(Denton & Nicol 1962,1965,1966;Denton 1970;
Denton & Land 1971;Denton et al. 1972). The
organization of the plates furthermore minimizes
the polarization of the reflected light, which reduces
the squid’s chances of being detected by the predators
that are polarization sensitive.
Cephalopods have pupils that respond to the
changes in light levels as well as under specific
behavioural contexts. In squid (L. vulgaris,L. pealeii,
Review. Structural coloration in cephalopods L. M. Ma
¨thger et al. S155
J. R. Soc. Interface (2009)
A. subulata), these pupils are lined with silvery
iridophores that are tilted towards the horizontal.
The iridophores are weakly reflective when the pupil
covers the eye but reflect strongly when the pupil is
open, for example during low light levels or aggressive
encounters. In such situations, the iridophores may
function to prevent strong downwelling light from
entering the eye. The pupil of Octopus vulgaris is also
lined with silvery iridophores (Froesch & Messenger
1978), although the plates are much shorter (less than
3mm in length) and do not have the wavy structure as
those of squid.
Longley (1917) found that the internal organs of
some transparent fishes (e.g. Coralliozetus cardonae)
are camouflaged by the principle of countershading.
This is also true of the ink sac of cephalopods: the dorsal
area is black; the sides are silvery; and the ventral area
is white (Denton 1970;Denton & Land 1971;Ma
¨thger
2001). In A. subulata, the silvery iridophores of the ink
sac reflect light in a way similar to that of the
iridophores around the eyes and their structural
arrangement is also similar, with plates ranging in
thickness from 85 to 120 nm with irregular spaces
between the wavy plates (Ma
¨thger 2001).
At least some cephalopods from the families
Ommastrephidae, Sepiolidae and Pyroteuthidae (e.g.
T. eblanae,Sthenoteuthis pteropus,Ommastrephes
bartrami,Heteroteuthis dispar and Pterygioteuthis
microlampas) have a very striking silvery golden stripe
that runs along each side of the mantle and head. As is
common in silvery fish, the iridophores of this stripe are
tilted towards the vertical (figure 5 f), suggesting an
obvious role in camouflage. The iridophores of this
stripe are very densely packed and, unlike other
iridophores, no single iridophore cell can be distin-
guished by eye. Figure 5gshows that the plates are the
thickest (approx. 140 nm) nearer the skin surface and
become thinner farther from the skin surface (to as thin
as 70 nm) ( Ma
¨thger 2001).
3.2. Broadband reflectance from
photophore reflectors
In habitats with ample supply of daylight, such as the
coastal areas and the upper layers of the sea, camouflage
and communication signals can be created by reflecting
light. However, at night and at greater depths to which
daylight does not penetrate, this is nearly impossible,
and, instead, many animals, such as crustaceans,
cephalopods and fishes, use luminescence for camouflage
and communication, either through intracellular
mechanisms, extracellular excretions or symbiosis with
bioluminescent bacteria (e.g. Nicol 1960; Herring 1988,
2000). Bioluminescence is particularly widespread in the
m
pupil
dorsal
ventral
lens
anterior
and
posterior
parts
400 450 500 550 600 650 700 750
reflectance
1
0
1 µmm
ch.
ir.
dorsal
ventral
wavelength (nm)
(a)
(c)
(f)
(e)
(d)
(g)
(b)
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 458incidence
(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.).
S156 Review. Structural coloration in cephalopods L. M. Ma
¨thger et al.
J. R. Soc. Interface (2009)
marine environment, but it is by no means restricted to
it. Some terrestrial organisms, such as some fungi,
bacteria and insects emit light, although their lumines-
cent structures are generally quite simple, lacking the
additional optical components (such as reflectors, lenses
and filters) that control the optical characteristics of the
more complex light-emitting photophores in some
cephalopods and fishes (Harvey 1952;Lloyd1975,
1978;Lall et al. 1980; Herring 1988,2000;Wilson &
Hastings 1998). However, particularly in insects, lumi-
nescence behaviour may be very elaborate: glow-worms
and fireflies are known to point their light organs in
specific directions to attract mates or lure prey. This
makes up for the lack of directionality in their light
organs. At the same time, male/female signalling
dialogues may be extremely complex (Lloyd 1975,1978).
Cephalopods and fishes have many photophores that
can be highly directional and have very complex
structures (e.g. Chun 1910;Nicol 1960;Robison &
Young 1981, Herring 1988,2000;Young & Bennett
1988; Johnsen et al. 1999a,b). Although there is an
impressive anatomical variety in cephalopod photo-
phores, especially with respect to the occurrence and
position of lenses, filters and reflectors, the common
theme among cephalopods is a thick layer of reflective
plates at the base of the photophore. Acting together, in
ventral photophores, these optical structures help to
channel and direct light downwards for effective
countershading (e.g. when viewed from below against
the more brightly lit downwelling light; see Arnold et al.
1974;Herring et al. 1981;Herring 1985,1988,2000;
McFall-Ngai & Montgomery 1990). Cephalopod photo-
phore reflectors differ in their composition and appear-
ance from diffuse to highly specular. In the midwater
squid Abralia and Watasenia, both of which have
several different types of photophore, the simplest ones
have only a basal concave reflector, formed of a highly
organized multilayer of collagen rods that reflect
specific wavelengths (Young & Arnold 1982;Young &
Bennett 1988; see also reflectin protein in Euprymna
photophores, Crookes et al. 2004). Collagen fibres also
provide the main reflector in the photophores of
Stauroteuthis syrtensis,Vampyroteuthis infernalis and
Spirula spirula, as well as being primarily responsible
for the silvery appearance of the main body wall of the
last species (Herring et al. 1981,1994;Johnsen et al.
1999b). Some of the more complex photophores (lensed
and filtered) have additional areas with reflective
tissue, such as light guides and filters (Herring 1988;
Young & Bennett 1988). Photophores often have a
pearly iridescent appearance that can result from
irregularity in thickness and organization of reflective
plates, similar to the silvery reflectors around the eyes
of cephalopods (described above). In the shallow-water
Hawaian bobtail squid Euprymna, for example, the
reflective plates appear to be of various thicknesses
(average 100 nm) and orientations (McFall-Ngai &
Montgomery 1990). Some mesopelagic squid, such as
Liocranchia, have highly wavy reflective plates; in
Sandalops and Megalocranchia, the reflective plates are
highly organized into stacks but the overall orientation
differs between stacks (Herring et al. 2002). Both
arrangements could be the cause of the photophore’s
‘pearly’ appearance. These basal reflectors reflect light
back through the photophore for more efficient light
emission. Reflectors can also play a role in tuning the
wavelength of the emitted light. In the squid Pterygio-
teuthis, the reflective plates are spaced and oriented so
that they reflect only blue light vertically downwards
(Arnold et al. 1974). The spectral characteristics of
light production are determined by the luminescence
chemistry, but the photophore emission can be
modified by spectrally selective filters and reflectors
that alter the bandwidth. Interestingly, some squid are
able to regulate their bioluminescence emission spectra
to match the spectral composition of downwelling light.
Young & Mencher (1980) showed that, in the squid
Abraliopsis and Abralia, the changes in water tempera-
ture experienced during diel vertical migration alter the
spectral emission of light from their photophores,
resulting in a match with the downwelling light
spectrum, which is different during day and night.
This may be achieved in the following way: the
photophore iridophores are surrounded by muscle
tissue, and the tensional forces of the muscles could
affect the spacing of the plates, which in turn could
affect the spectral composition of the emitted light
(Arnold et al. 1974;Young & Arnold 1982). There
appears to be no evidence to suggest that the
photophore iridophores are physiologically active
as the iridophores in the mantle skin of many
squid (see above), but to our knowledge this has not
been tested.
3.3. Diffuse white scattering
The body patterns that cephalopods use for camouflage
and communication show a wide variety of contrast and
brightness levels. In addition to iridophores, cuttlefish
and octopus have another structural reflector type that
creates bright white patterns, shapes and spots. These
reflectors are called leucophores (‘white cells’) and they
are made up of spherical assemblages called leucosomes
(Froesch & Messenger 1978;Cloney & Brocco 1983).
Leucophores reflect the ambient wavelengths of light
(i.e. they look white in white light, red in red light, blue
in blue light, etc.) and are found in high density in
specific skin areas (zebra stripes, fin spots, fin line and
various other skin components) that can be bright
white depending on the body patterning that is shown
(figure 6a). Squid generally do not have leucophores
(Sepioteuthis lessoniana and Sepioteuthis sepioidea
may be exceptions).
Ma
¨thger et al. (submitted) show that the leuco-
phores of cuttlefish, S. officinalis, have the optical
properties of a perfect diffuser, appearing equally bright
from all angles of view and that they reflect light at
consistently high levels (up to 70% at wavelengths from
300 to 900 nm). The light-scattering elements of
leucophores are spheres (leucosomes) that range in
size from 250 to 1250 nm in diameter (figure 6b) and are
composed of mucoproteins—highly sulphated and
weakly acidic mucopolysaccharides (they stain nega-
tively with antibodies to reflectin, which is the light-
reflecting protein in squid skin).
Review. Structural coloration in cephalopods L. M. Ma
¨thger et al. S157
J. R. Soc. Interface (2009)
4. CONCLUSIONS
In cephalopods, colour change is mediated by two types of
skin components: pigmented chromatophores and struc-
turally reflecting cells (iridophores and leucophores).
Iridophores are the cells that are made up of stacks ofthin
protein plates that function as multilayer reflectors,
whereas leucophores contain spherical protein assem-
blages that scatter light equally well throughout the
visible, IR and UV parts of the spectrum.
In this paper, we have shown that iridescence in
cephalopods spans the whole of the visible spectrum,
including the near-IR. Biologically, IR reflectance most
likely plays little or no role in cephalopod behaviour
because IR is absorbed rapidly by sea water. Further-
more, most cephalopods studied thus far appear to be
colour blind, having only one visual pigment, with the
absorbance peak generally in the blue–green part of the
spectrum (Brown & Brown 1958;Bellingham et al.
1998; but see Kito et al. 1992;Michinomae et al. 1994).
Therefore, reflectance in the IR is most likely irrelevant
for vision in these animals. Interestingly, in the
cephalopod species discussed in this paper, there has
so far been no evidence for iridescence in the UV parts
of the spectrum, but considering the diversity of
cephalopod skin coloration, and the fact that some
fish predators can see UV, this possibility should not be
ruled out.
Leucophores create the white skin areas that are part
of various camouflage and signalling body patterns of
cuttlefish and octopus. They provide a backdrop against
which chromatophores (and iridophores) can create
highly contrasting patterns, such as those typical of the
light skin components of disruptive coloration in cuttle-
fish (Hanlon & Messenger 1988;Chiao & Hanlon 2001;
Barbosa et al. 2007;Kelman et al. 2007;figure 6a).
Leucophores are not physiologically active (as some
iridophores are), they do not polarize light and they look
equally bright from all angles of view. Leucophores reflect
the ambient wavelengths of light (they look red in red
light, blue in blue light, white in white, etc.), which may
aid both wavelength and intensity matching at least at a
localized level in the skin ( Froesch & Messenger 1978).
This may be particularly useful in the habitats in which
shorter (blue and green) wavelengths predominate,
primarily those of greater depths (Jerlov 1976).
Two clear functions of structural coloration in
cephalopods emerge: (i) camouflage and (ii) signalling/
communication.
0035 15 KV 10 µm WD33
(a)(b)
(c) (d)
(e) ( f)
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).
S158 Review. Structural coloration in cephalopods L. M. Ma
¨thger et al.
J. R. Soc. Interface (2009)
4.1. Camouflage
Many iridophores are oriented in precise ways to
facilitate reflectance in specific directions. Iridophores
provide a range of wavelengths that complement the
yellow, red and brown pigments in the chromatophores,
so that camouflage can encompass the entire visible
spectrum. Additionally, some squid are able to regulate
the intensity of light reflected from iridophores, and
matching the intensities of the ambient light field is a key
step towards achieving effective camouflage. Further-
more, the silvery iridescence that is found around the
eyes, the ink sac and the sides of the mantle suggests a
role in camouflage by acting as vertically oriented
mirrors. The reflective plates are tilted towards the
vertical and they maximally reflect the incident light,
much in the same way as silvery fish (e.g. Denton & Nicol
1962;Denton 1970;Denton & Land 1971).
Leucophores also play a role in camouflage: they
provide light areas that may facilitate both background
matching (by resembling specific light objects in the
background) and disruptive coloration (by visually
breaking the body into distinct objects of high-
contrasting patches) (Cott 1940;Hanlon & Messenger
1988;Hanlon et al. 2009).
4.2. Signalling/communication
The optical properties of the structural reflectors
provide cephalopods with an excellent means of
communication. Optical signals, both intra- and
interspecific, can vary dramatically from the zebra
stripes of cuttlefish (the light stripes are created by
leucophores; figure 6b) to the flashing blue iridescent
rings of the blue-ringed octopus (figure 4). Some
iridescent areas are strongly polarized at certain angles
(e.g. Shashar & Hanlon 1997;Ma
¨thger & Hanlon 2006;
Chiou et al. 2007) and, since cephalopods have the
ability to detect polarized light, this may have
behavioural functions (e.g. Cronin et al. 2003;Boal
et al. 2004). It has been shown that cuttlefish take
advantage of their polarization vision when hunting for
silvery fish whose scales polarize light (Shashar et al.
2000), so that it is conceivable that polarization may be
used in various signalling aspects of cephalopod
behaviour (Boal et al. 2004).
Squid are commonly found in large schools. The
communication of the movements of individuals in a
school is crucial for maintaining the integrity of a school
and iridescence may play such a role. The various
iridescent stripes and splotches in squid (e.g. Hanlon
1982;Hanlon et al. 1999;Ma
¨thger & Denton 2001) have
characteristic optical features that differ depending on
where the onlooker is positioned, so that it is possible
that the squid may use their iridescent markings to
communicate changes in swimming direction, etc.
(Ma
¨thger & Denton 2001).
Thus far, there is no optical evidence that cephalo-
pod iridescence may be caused by diffraction gratings.
In a short communication, Hanlon et al. (1983), showed
that the iridophore plates of some squid are oriented
‘edge on’, i.e. with their short ends facing the
skin surface, in some ways resembling the face of
a diffraction grating. By contrast, Ma
¨thger & Denton
(2001) subsequently showed that iridophores with
reflective plates of this orientation, as commonly
observed in the iridophores of the lateral and ventral
mantle skin, nevertheless act as multilayer reflectors.
However, considering how few species have been
studied in detail, compared with the diversity of the
class Cephalopoda, it should not be ruled out that
diffraction gratings may be a mechanism of iridescence
in some cephalopod species.
Iridescence is widespread in the animal kingdom and
its function is not always associated with signalling or
camouflage (e.g. mother of pearl, in which the
iridescent layer on the interior of the mollusc shell
provides structural strength; Barthelat et al. 2007) but
for many species it is. Some of the most exotic iridescent
patterns can be seen in a great number of butterfly
species (e.g. Ghiradella 1991; Vukusic et al. 1999,2000;
Sweeney et al. 2003;Vukusic & Sambles 2003;Stavenga
et al. 2004) and the plumage and skin of many birds
(Prum et al. 1998;Vorobyev et al. 1998;Cuthill et al.
1999;Osorio & Ham 2002;Prum & Torres 2003). The
feathers of the male peacocks and birds of paradise
(Frith & Beehler 1998;Zi et al. 2003) are superb
examples of how nature has built complex optical
devices for achieving special visual effects.
Many marine vertebrate and invertebrate species—
mantis shrimp and coral reef fish are particularly
remarkable—have incorporated iridescent structures
into their body markings whose function it is to attract
females, warn intruders or aid in blending into the
visual background (Kasukawa et al. 1987;Fujii et al.
1989;Lythgoe & Shand 1989a;Fujii 1993;Herring
1994;Marshall 2000;Marshall et al. 2003;Mazel et al.
2004;Siebeck 2004;Chiou et al. 2005; R. Caldwell 2008,
personal communication). Arachnids also have irides-
cent markings, some of which are most prominent in the
UV parts of the spectrum (Oxford & Gillespie 1998;
Lim & Li 2007;Taylor & McGraw 2007).
Most animals have available to them only one body
pattern that may undergo seasonal or ontogenetic
changes but more often stays the same throughout the
animal’s life (Cott 1940;Edmunds 1974;Booth 1990).
Changeable iridescence is not common in the animal
kingdom, presumably because of the physical challenge
of creating such devices. Squid are one of a few known
animals that have changeable iridescence. In
vertebrates, iridescence changes occur: most have not
been well quantified, and those that have been generally
appear to take minutes, hours or even days (e.g. fishes:
Lythgoe & Shand 1982,1989b,Kasukawa et al. 1987,
Fujii et al. 1989; lizards: Hadley & Oldman 1969,
Taylor & Hadley 1970,Morrison et al. 1996; tree frogs:
Stegen et al. 2004). One known exception may be the
paradise whiptail (Pentapodus paradiseus), a tropical
fish whose reflective changes are very fast (i.e. fraction
of a second (Ma
¨thger et al. 2003). Billfish are also
reported to have fast reflective changes, but this has not
been quantified to the best of our knowledge (e.g. Davie
1990;Fritsches et al. 2000).
By studying animal structural coloration, we gain
insight into how nature has solved the problem of
creating optical devices with specific functions in
Review. Structural coloration in cephalopods L. M. Ma
¨thger et al. S159
J. R. Soc. Interface (2009)
ecological contexts. The impressive repertoire of
cephalopod colour change reaches far beyond the field
of biology. In recent years, cephalopod iridophores and
chromatophores have received interest from materials
scientists who aim to model the optical properties of
these structures and create synthetic materials with
similar characteristics for various applications in
optical nanotechnology (e.g. Crookes et al. 2004;
Kramer et al. 2007;Sutherland et al. 2008a,b;Vaia &
Baur 2008).
In summary, studying animal structural coloration is
mesmerizing not only because of the sheer beauty that
is created by the microscopic assemblies of reflective
materials with highly precise arrangements and orien-
tations, but also because of what we can learn from
these biophotonic structures in our efforts to produce
electronic visual displays as well as various kinds of
paints and coatings (e.g. Vaia & Baur 2008). Despite
the recent attention to cephalopod structural color-
ation, many questions remain unanswered. For
example, what are the behavioural functions of
iridescent signals? What other structural light reflec-
tors are present in the diverse class Cephalopoda?
Cephalopods have made their way into all the world’s
oceans, including the tropics and polar waters, and even
to the depths exceeding 3000 m (Hanlon & Messenger
1996), so we are likely to find more fascinating
structural reflectors in the future.
We thank Malcolm Clarke for providing some of the speci-
mens that L.M.M. used during her PhD. Sir E. J. Denton was
L.M.M.’s PhD mentor and he was involved in much of the
characterization of iridescence of squid presented in this
paper. We would also like to thank Morley Stone for
continuous stimulating discussions of these topics. L.M.M.
gratefully acknowledges funding from the Gottlieb Daimler-
and Karl Benz-Foundation (PhD) and the Royal Society
(postdoctoral fellowship in Australia). We are also grateful to
Peter Herring and an anonymous reviewer for their con-
structive comments that greatly improved this manuscript.
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... As a result, in the context of this paper, we can understand them as relative synonyms. 2 See, e.g., Lishak (1984); Lugli et al. (2003); Marler and Slabbekoorn (2004); Belanger and Corkum (2009);Houck (2009) ;Mäthger et al. (2009);Bruschini et al. (2010); Costa-Leonardo and Haifig (2010); Haddock et al. (2010); Wyatt (2010); Thiel and Breithaupt (2011). 3 When Chomsky discusses 'language' (or, more typically, 'grammar'), he means 'I-language'-i.e., a bio-computational system represented in the brain, with a capacity for generating a discrete infinity of hierarchical structures. ...
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... Unlike most organisms known to date, coleoid cephalopods (i.e., squid, octopi, and cuttlefish) represent some of the very few examples of animals that are able to alter their appearances (both coloration and texture) almost instantaneously ( Figure 4A,B) [37][38][39][40]. Specifically, the animals' amazing color changing abilities are enabled by complex hierarchical skin architectures, which contain both pigment-containing organs and iridophore and leucophore cells, which act as narrowband and broadband reflectors, respectively ( Figure 4C) [10][11][12]40,41]. ...
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