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First published online October 5, 2007
Journal of Experimental Biology 210, 3624-3635 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.006932
Spectral and spatial properties of polarized light reflections from the arms of squid (Loligo pealeii) and cuttlefish (Sepia officinalis L.)
1 Department of Biological Sciences, University of Maryland, Baltimore
County, 1000 Hilltop Circle, Baltimore, MD 21250, USA
2 Marine Resources Center, Marine Biological Laboratory, Woods Hole, MA
02543, USA
* Author for correspondence (e-mail: chiou1{at}umbc.edu)
Accepted 16 July 2007
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Key words: cephalopod, polarized light, squid, cuttlefish, signal, iridophore, structural color
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). The
surfaces of many cephalopod species are unusual in that they reflect changing
patterns of polarization (Shashar and
Hanlon, 1997; Hanlon et al.,
1999; Mäthger and Denton,
2001; Shashar et al.,
2001). In both squid (Loligo pealeii) and cuttlefish
(Sepia officinalis L.), iridophores are responsible for the
reflection of this polarized light
(Shashar et al., 1996;
Hanlon et al., 1999;
Mäthger and Denton, 2001;
Shashar et al., 2001;
Mäthger et al., 2004).
Such iridophore cells are distributed all over the bodies of these coleoid
cephalopods (Hanlon, 1982;
Hanlon and Messenger, 1996),
although there are different types and arrangements of iridophores that have
not yet been inventoried with precision. In general, iridophore cells are
passive reflectors that are quite angle-dependent for viewing. Curiously,
reflections from some of the arm iridophores on squid and cuttlefish are less
dependent on the angles of illumination and viewing, and this provides one of
the rationales for the present study.
The multilayer platelet structures within iridophores, thought to be
responsible for the reflection of iridescent structural colors as well as the
polarized light, have been described by several investigators
(Land, 1972;
Cloney and Brocco, 1983;
Hanlon and Messenger, 1988;
Cooper et al., 1990;
Hanlon et al., 1990;
Shashar et al., 1996;
Shashar et al., 2001). Light
reflected from a multilayer reflector of this kind is almost always colored,
and it is polarized as well when the illumination is at oblique angles of
incidence. Two prerequisites for spectrally favored reflection are that (1)
there is a difference in refractive index between the platelets and the spaces
separating them, and (2) the platelets and spaces have thicknesses on the
order of wavelengths of light (Land,
1972). Moreover, since it is well known that when a light beam is
reflected from a stack of plates, the spectrum of the reflected light is a
function of their spacing, orienting the iridophore plates to a different
angle is expected to result in a change of reflectance. Changes in the
relative angle between a light source and the surface normal of a multilayer
reflector produce a sequence of color changes known as Newton's series. For
color-blind animals like cuttlefish and squids (Marshell and Messenger, 1996;
Gleadall and Shashar, 2004;
Mäthger et al., 2006),
the changes in wavelength would be perceived as different brightnesses.
Because brightness information can be easily affected by the lighting
environment, this type of reflectance change is unlikely to be a good visual
signal for communication.
In most animals, body coloration and achromatic patterns function in heat
exchange, radiation protection, communication or camouflage (e.g.
Cott, 1940). In contrast,
polarization body patterns apparently function primarily for intraspecific
communication (Cronin et al.,
2003). The `iridescent arm stripe' described in squid (Loligo
pealeii) (Hanlon et al.,
1999) and the `pink iridophore arm stripes' described in
cuttlefish (Sepia officinalis L.)
(Hanlon and Messenger, 1988)
reflect highly polarized light (Shashar et
al., 1996; Shashar and Hanlon,
1997; Hanlon et al.,
1999). It has been hypothesized that the main function of these
arm stripes is to act as visual signals for intraspecific communication
(Shashar et al., 1996;
Mäthger and Hanlon,
2006). Since light underwater generally arrives from nearly
overhead, the polarized light reflected from the arm stripes has a somewhat
horizontally oriented electric vector (e-vector) that is observable from
before sexual maturation through adulthood
(Shashar et al., 1996;
Shashar and Hanlon, 1997;
Gleadall and Shashar, 2004).
Cuttlefish and squid are capable of turning the polarization on or off
voluntarily (Hanlon and Messenger,
1988; Shashar and Hanlon,
1997), and there is recent behavioral evidence that polarization
signals are used among cuttlefish (Boal et
al., 2004). Changes of the e-vector orientation of the reflected
polarized light have also been reported to occur instantaneously in both
animal species (Shashar et al.,
1996; Shashar and Hanlon,
1997; Hanlon et al.,
1999; Shashar et al.,
2001).
Iridophores that exhibit physiological alteration of the reflection
properties (also known as active or motile iridophores) have only been found
in a few types of animals. In several species of squid (including L.
pealeii, L. vulgaris, Lolliguncula brevis, and Alloteuthis
subulata), the common neurotransmitter acetylcholine (ACh) induces an
ultrastructural change in the protein of iridophore platelets, changing their
ability to reflect light; increased quantities of ACh (in physiologically
normal quantities) change the thickness of the iridophore platelets as well as
the space between them, producing a color shift
(Cooper et al., 1990;
Hanlon et al., 1990;
Mäthger et al., 2004;
Mäthger and Hanlon,
2007). Active iridophores in fishes and lizards are also capable
of changing the spacing between reflecting platelets. The physical mechanisms
that activate the iridophores include mechanical force, osmotic pressure and
temperature (Lythgoe and Shand,
1982; Oshima et al.,
1985; Clothier and Lythgoe,
1987; Lythgoe and Shand,
1989; Nagaishi et al.,
1990; Morrison et al.,
1996).
There are two questions that this paper addresses concerning the polarized-light signaling system in cuttlefish and squid. First, we would like to know how the surface orientation of these flexible animals affects the polarization signals they reflect. In other words, since the multilayer reflectors are located in unusually flexible appendages, it would be of interest to know whether arm orientation affects the reflected signal. By manipulating the relative angles of skin samples and the direction of illumination, we measured changes of the polarization signal generated by the pink iridophore arm stripes of cuttlefish and the iridescent arm stripes of squid. Second, we examined how the above-mentioned signals are optically produced. To determine the physical basis of the optical properties of the arm stripes, the fine structures of the iridophores were studied using electron microscopy.
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). Due
to the tendency of the dermal tissue to lose its transparency over time, the
collection of spectra and images occurred within 5 h following the sacrifice
of the animal. Throughout the experiment, the tissues were submersed in
freshly collected seawater.
Sample setup and spectral measurements
All measurements were made under a Zeiss dissecting microscope with a
polarization filter attached (Quantaray; Ritz Camera Centers Inc., Irvine, CA,
USA). After marking the polarization axis of the filter, it was mounted under
the objective lens of the microscope with a custom-built adaptor
(Fig. 1A). Rotating this
polarization filter permitted the analysis of the polarized light reflected
from the preparation. Using the tilting table, we could freely change the
angle of the preparation while the positions of light source and detector or
camera remained stationary. We used a right-handed three-dimensional Cartesian
coordinate system to describe the relative position and angles of the sample,
the light source, the observer and the e-vector. We assigned the origin to the
point of measurement, with the positive z-axis pointing up,
x-axis pointing right, and the y-axis pointing away from the
observer (Fig. 1B). The angle
of the sample is defined as the angle in the xz-plane between the
surface normal of the arm stripe and the (vertical) z-axis. Starting
from 0°, at which angle the surface normal was parallel to the
z-axis, the angle was increased by bringing the surface normal toward
the positive arm of the x-axis (i.e. rotation occurred only on the
y-axis). We used the relation between the longitudinal axis of the
arms and the y-axis to denote the orientation of the arms, measuring
two sets of data by setting the longitudinal axis of the arm either parallel
or perpendicular to the y-axis. If the arm was perpendicular to the
y-axis, we changed the angle of the sample by tilting it in the
xz-plane; if the arm was parallel to the y-axis, the angle
was changed by rotating it (around the arm's axis).
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45° above the signaler.
Spectral and imaging polarimetry
The spectral properties of the light reflected from samples were measured
using a spectrometer (USB 2000, Ocean Optics Inc., Dunedin, FL, USA) attached
to an optic fiber (P1000-2-UV/VIS, Ocean Optics Inc.) that was connected to a
camera mounted on the microscope. The tip of the optic fiber was adjusted to
the image plane of the camera to permit precise positioning and focus of the
object being measured. Because the e-vector of light is always perpendicular
to the direction of propagation, in our setup it was always parallel to the
xy-plane. We define the angle of the e-vector to equal 0° when it
is parallel to the x-axis, and it increases counter-clockwise from
the observer's point of view (Fig.
1B). Therefore, at a 90° angle, it is parallel to the
y-axis.
Sets of four spectra, including a dark reference measurement and with the
polarization filter positioned at 0°, 45° and 90°, were collected
from each particular mounting position of a sample. We took another four sets
of spectra recorded in the same conditions from a strip of Teflon tape used as
a diffuse white standard having a reflection value of 100% at all wavelengths.
From these we calculated, at 1-nm intervals from 400 nm to 800 nm, the
e-vector angle and the partial polarization of the light reflected from sample
as well as the spectral reflectance of the sample. The calculation was
performed by a custom-written program that is based on the equations derived
by Wolff and Andreou (Wolff and Andreou,
1995).
In addition to the spectral measurements, images of each preparation were
taken with a digital camera (C5050 Zoom, Olympus America Inc., Center Valley,
PA, USA) that was attached to the microscope with a universal digital camera
microscope coupler (Edmund Optics, Barrington, NJ, USA). The camera was set to
the manual exposure mode to maintain a constant shutter speed and aperture
size for successive images. We also set the camera to the manual focus mode to
prevent any change of sample position or magnification within sets of images
caused by lens movements due to auto-focusing. The camera was calibrated for
its response-intensity functions as described by Cronin et al.
(Cronin et al., 2006). Sets of
three images were taken for each sample, with the polarization filter
positioned at 0°, 45° or 90°. After transferring the images to a
computer, we averaged the values of the three color channels (red, green and
blue; 8 bits per channel), weighted for linearity, and calculated the e-vector
angle, partial polarization and the relative reflectance for each pixel with a
custom-written program based on the same equations as for the spectral
measurements. The e-vector angle and partial polarization value of each pixel
were then coded with color and weighted by the relative intensity value of the
corresponding pixel to display the signal clearly. For example, if part of the
sample was highly polarized but had a very low reflectance value, the area
would be shown with a darker color of the same hue in comparison with another
part that was equally polarized and having higher reflectance.
Transmission electron microscopy (TEM)
To ensure that the orientation of iridophores did not change during
fixation, the arms were pre-fixed with 2.5% glutaraldehyde in artificial
seawater (ASW, in mmol l–1: NaCl 425, KCl 10,
CaCl2 10, MgCl2 25, MgSO4 25, Hepes 40, pH
8.0) for at least 30 min while they were still pinned to the disc on the
tilting table. No color changes were observed in the iridophore cells after
transferring the samples from seawater to the prefix solution. The arms were
subsequently transferred to individual tubes containing the same fixative and
placed at 4°C overnight. Cross sections less than 2 mm thick were taken
from pre-fixed arms near the location where polarization measurements had been
taken. Although glutaraldehyde renders the dermal tissue somewhat opaque, at
this stage the iridescent color was still visible through the incision
surface. The sample slices were post-fixed with 2% osmium tetroxide in ASW for
2 h at 4°C followed by dehydration, infiltration and embedding in Epon-812
epoxy resin. Thin sections (60 nm) were cut from the blocks with a
diamond knife on a Reichert-Jung Ultracut E microtome. Sections were examined
under an electron microscope (EM 10CA, Zeiss, Gottingen, Germany) without
further staining.
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In Figs 8 and 9, we show the arms of squid and cuttlefish as true-color images together with false-color images of the partial polarization values. In these images, regions that reflected highly polarized light (orange to red in Fig. 8B and green to yellow in Fig. 9B) coincide with the areas where the iridophore arm stripes reside (Fig. 8A, Fig. 9A). The distribution of highly polarized reflections remained unchanged throughout most tilt or rotation angles (Fig. 8B, Fig. 9B). Exceptions were found in squid arm stripes when the sample was oriented parallel to the y-axis and rotated at 0° to 10°. In these cases, only a few of the iridophores were directly illuminated by the light, and these images illustrated lower brightness and partial polarization values in the regions of the arm stripes.
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;
Hanlon, 1982;
Shashar et al., 1996). In
their overall architecture and shapes, the iridophores in the arm stripe
regions of cuttlefish and squids closely resemble one another. Each stack of
platelets forms a reflecting unit known as an iridosome
(Mirow, 1972;
Cloney and Brocco, 1983). In a
given section, different iridosomes may show different thicknesses and spaces
between plates (Fig. 10).
These apparently variable thicknesses of iridosomal plates among iridosomes
appear because the section plane was rarely perpendicular to the plates. As a
result, neither the thicknesses of the plates nor the spaces between them can
be determined accurately. For similar reasons, the number of platelets within
each iridosome was also undetermined. Nevertheless, differences found between
the species could affect the optics of the reflector. First, the number of
reflecting units in the light path (a consequence of the thickness of the
iridophore layer) appears to be different. In cuttlefish, we estimate that a
light beam perpendicular to the skin surface may pass through up to eight
iridosomes (Fig. 10B), while
in squid more than twice as many reflecting units may be encountered
(Fig. 10A). Including the
spaces between iridosomes, the total thickness of the reflecting layer
observed is between 41 µm and 60 µm in squids and 22 µm to 41 µm
in cuttlefish. The two species also differ in the orientations of the
reflecting units. While the iridophore plates in cuttlefish are generally more
or less perpendicular to the skin surface, the ones in squid appeared to be
oriented more irregularly (Fig.
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;
Shashar and Hanlon, 1997;
Shashar et al., 2001;
Gleadall and Shashar, 2004;
Mäthger and Hanlon,
2006). Nevertheless, similar results were found in pink or red
iridophores found in the mantle of squids
(Mäthger and Denton,
2001), where the reflected light was polarized only when the
iridophores appeared bluish green in color.
Theory predicts that varying the angle of incidence of light falling on a
multilayer reflector should result in a gradual shift of the dominant
reflected wavelengths (Huxley,
1968; Land, 1972;
Deparis et al., 2006). It has
been shown in several squid species that, at least for the mantle area,
altering the illumination angle does shift the reflectance and polarization
spectra in a predictable way (Mäthger
and Denton, 2001; Mäthger
and Hanlon, 2006). When the illumination angles were changed (i.e.
between Positions 1 and 2) we also observed changes in reflectance and
polarization spectra similar to those of the mantle iridophores as described
previously (Mäthger and Denton,
2001).
Both imaging polarimetry and spectral measurements showed that at any given
orientation, the light reflected from the arms of cuttlefish always had a
lower partial polarization than that from squid. Our data are consistent with
previously reported values of the partial polarization found in squid
(Shashar and Hanlon, 1997;
Shashar et al., 2001). No
quantitative data of the partial polarization from the arms of cuttlefish have
been published previously. Based on the ultrastructure of the iridophores, it
is most likely that the relatively lower reflectance and polarization values
found in cuttlefish compared to squids were caused by a thinner iridophore
layer and comparatively fewer iridosomal plates in the light path.
e-vector angle
The e-vector angles of the polarization reflections of the iridophore arm
stripes have variously been reported to be either parallel to the longitudinal
axis of the squid arm (e.g. Shashar et
al., 2001) or perpendicular to it (e.g.
Hanlon et al., 1999;
Shashar and Hanlon, 1997). As
mentioned earlier, both squids and cuttlefishes can reportedly control their
polarization reflections (Shashar and
Hanlon, 1997; Shashar et al.,
1996), so the differences between previous reports could result
from experiments on animals of different physiological states. Since we did
not measure polarizations from living animals, we cannot rule out the
possibility that the e-vector angle can be actively changed by the animals.
However, because the e-vector of the polarized light reflections is highly
dependent on the illumination angle (Figs
4,
5), it is most likely that
differences in illumination orientation alone are responsible for these
conflicting reports.
The dependency of e-vector orientation on illumination angle implies that
under illumination from two perpendicular light sources of similar brightness,
reflected light should be weakly polarized, at best. Similarly, polarization
reflections from arm stripes may be weak under diffuse illumination such as in
a turbid environment. The cuttlefish and squid species that we studied inhabit
from the surface of the sea to around 150 m and 400 m in depth, respectively,
but in most cases, they spend their time at relatively shallow depths of the
sea (<50 m), especially when they are active
(Cargnelli et al., 1999;
Sherrard, 2000). In this kind
of shallow-water environment, when looking at the arm stripes of nearby
fellows, no matter how their arms are oriented, the cuttlefish or squid should
be able to discern clear and nearly constant patterns of polarization.
Physical basis of the polarization reflections
Multilayer reflectors occur in a number of animal species. Such devices
produce bright, colorful reflectance with a `metallic' appearance. This
metallic impression is caused by constructive interference of light reflected
from different layers (Land,
1972). When a beam of light reaches a dielectric surface, at an
interface between two media of different refractive indices, the proportion of
light reflected depends on the refractive indices of the media as well as the
wavelength, incident angle and e-vector angle of the incoming light. In
principle, a dielectric surface has the highest efficiency of separating light
of different e-vector angles when light is incident and reflected at
Brewster's angle (the angle at which reflected light is fully polarized), and
the partial polarization of the reflected light changes as the angle of
incidence (and therefore reflection) changes. Furthermore, while Brewster's
angle varies with the wavelength of light, multilayer reflector-based
polarizers are usually wavelength selective
(Kliger et al., 1990).
Therefore, a multilayer device could reflect highly polarized light in a
particular wavelength range and relatively un-polarized light for all other
wavelengths of light. This effect could explain why we found maximum
polarization reflections from iridophores primarily at medium to short
wavelengths (e.g. bluish), but when the arm stripes preferentially reflected
long-wavelength light (when they appeared to be pink and when light arrived
from 45°), polarization was extremely weak. The reflectance spectra of the
two types of reflection complement each other (compare
Fig. 3A with
Fig. 6B or
Fig. 3B with
Fig. 7B). That is to say,
whatever mechanism the reflector might be based on, it separates the incoming
light into polarized light of shorter wavelengths and non-polarized light of
longer wavelengths. Considering the ultrastructure of cephalopod skin
(Cloney and Brocco, 1983), it
is most likely that the non-polarized pink reflection is the result of light
reflected or scattered from tissues underneath the iridophore layer.
It has long been suspected that, at least in squid, light reflections from
arm stripes are based not purely on multilayer reflections but also on
wavelength-specific scattering of light
(Hanlon and Cooper, 1983). In
addition, and contrary to the properties of typical multilayer reflectors, we
found that the light reflected from the arm stripes of cuttlefish or squid did
not show any obvious relationship between orientation and polarization
properties. In both species, neither the peak wavelengths of the reflectance
spectra, nor the partial polarization values, nor the e-vector angles of the
reflected light are greatly affected by varying the orientation of the arm
stripes (Figs 4,
5,
6,
7).
While these results are qualitatively similar to the polarization of light
caused by Rayleigh scatter, Rayleigh scattering is strongly
wavelength-dependent; the shorter the wavelength, the stronger the scatter. As
a result, higher reflectance values are to be expected at shorter wavelengths.
Obviously, our results (Figs 6,
7) do not comply with this
prediction. Our EM work instead suggests that the iridosomes in the arm
stripes act as multilayer reflectors (Fig.
10). Although it is unclear what refractive indices the iridophore
plates have, they are almost certainly made of a protein called reflectin
(Crookes et al., 2004).
Reflectin has a refractive index of 1.59, which is the highest refractive
index ever found in any naturally occurring protein
(Kramer et al., 2007). When
light is reflected from the interface between a layer of reflectin and
cytoplasm (refractive index=1.33), Brewster's angle occurs at 50.09°. If
there are other proteins present in the reflecting plates in addition to the
reflectin, the refractive index of the plates could be slightly lower than
predicted above, making Brewster's angle nearer to 45°. Thus, the greatest
values of partial polarization will always occur when the incident light is
nearly perpendicular to the reflected light, so that the angles of incidence
and reflection are both near 45° (i.e. as in illumination Position 1). In
principle, one could use Fresnel's equations
(Feynman et al., 1963)
together with measurements of polarization at many angles of incidence and
reflection to compute the true values of the refractive indices of these
structures; however, these properties of the iridophore plates are beyond the
scope of this paper. Furthermore, because of the stacking of large numbers of
plates and their complex orientations, it is unlikely that the results of such
measurements would be meaningful.
Characteristic multilayer reflection has been found from iridophores in the
mantles of several squid species
(Mäthger and Denton,
2001; Mäthger and Hanlon,
2007). However, our results from the iridophores of cephalopod arm
stripes do not entirely reproduce the properties of typical multilayer
reflections. Plates within the iridophores of the mantle surface or other
iridescent regions on the bodies of squids and cuttlefishes are generally
parallel throughout the entire cell, thus producing characteristic features of
standard multilayer reflectors (Cooper et
al., 1990; Hanlon et al.,
1990). In contrast, we found that the orientations of the plates
(as well as the number and thicknesses of the plates) in iridophores of the
arm stripes vary. It seems likely that the arm stripes of cuttlefish and squid
use multilayer reflectors with their surfaces arranged over various angles to
produce uniquely constant polarized light reflection properties. Thus, while
the tilt or rotation angle of the sample changes, one particular subset of the
iridosomes (and their sets of parallel plates) is always favorably
illuminated. As a result, the incident angle and thus the properties of the
reflected polarized light are essentially constant across various tilt and
rotation angles. In this way, any changes in the position of the arms of
signaling squid of cuttlefish will affect the signal's polarization appearance
only minimally. Consequently, a unique, reliable, and highly conspicuous
signal can be produced.
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Acknowledgments |
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