Cephalopod Color and Skin discoveries

DWhatley

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Squid skin and ceph adaptive coloration have become an on going news item since the military (navy) has shown interest in learning the secrets of ceph camouflage. Use this topic to collect the latest articles uncovered.

Here is a list of papers on the topic from the Woods Hole Research Library
 
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A Squid’s Switchable Cells Offer Key to Camouflage - Danna Staaf October 2013

A dissected female squid mantle showing iridescent and white stripes (right side of image). Credit: Daniel DeMartini

Market squid are known in California as the state’s largest fishery and as the basis for those little fried calamari rings. New research, published October 1 in the Journal of Experimental Biology, shows that they may also have something to offer the engineering sector: skin cells that can switch between transparent and white. Humans could use these cells to develop new bio-inspired materials; squid probably use them for cross-dressing.
Danny DeMartini, a graduate student at the University of California, Santa Barbara, and lead author of the study, started out working on a kind of cell called an iridocyte. As the name implies, these cells produce iridescent colors, like beetle wings or a peacock tail. But squid iridocytes are adaptive–unlike other animals, the squid can actively control their hue and brightness.
Super-bright iridescent stripe in the skin of a female market squid. Credit: Daniel DeMartini

DeMartini’s work took a leap forward when he noticed that female market squid have an unusually bright stripe of iridocytes on each side of their body. The super-bright cells from this stripe were easier to study, and he was able to determine the specific proteins that permit adaptive color-changing.
Then he noticed that the female squid also had a white stripe on their backs, composed of leucophores–a kind of skin cell that scientists always considered to be statically white. But DeMartini found that they contained the same proteins he’d identified in the iridocytes.
“I went home fairly depressed that day,” he says. If these proteins were present in supposedly static cells, then how could they be the key to changing color, as he’d thought? “Then I began to wonder if leucophores are adaptive. And in fact they are.”
He went on to discover that leucophores and iridocytes use the same proteins in different ways. Iridocytes pack theirs into folds in the cell membrane. When the squid’s brain sends a signal, the proteins condense, drawing the folds closer. The distance between the folds determines the wavelength of light reflected, allowing iridocytes to “tune” their color from red to blue.
Meanwhile, leucophores keep their proteins in membrane-enclosed spheres of many sizes. Before the signal to condense, the proteins are too dispersed to reflect light, and the leucophore is transparent. After condensation, the assorted spheres reflect all available wavelengths, making the leucophore appear white.
Market squid mating and spawning party. I mean aggregation. Credit: Jesse Claggett.

Such sophisticated color-changing abilities tempt imitation. Military applications are particularly obvious, and indeed, DeMartini’s work is funded by a Navy grant, though he says, “I don’t think we’re going to be stapling squid skin to soldiers anytime soon.” He also points out that the principles being discovered could find use in fields such as optical communication.
What about applications for the squid themselves? Why are the switchable white cells only found in females? Definitive answers await behavioral studies, but DeMartini theorizes that the white and rainbow stripes together could mimic the appearance of a male squid’s testis. This option would give females a tool (ahem) for discouraging unwanted attention.


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[h=3]About the Author (Author Profile)[/h] Danna is a marine biologist, a science writer, a novelist, an artist, and an educator. She helped found the outreach program Squids4Kids, illustrated The Game of Science, and has blogged at Squid A Day since 2009. She holds a BA in Creative Studies from the University of California, Santa Barbara, and a PhD in Baby Squid from Stanford. She lives in San Jose with her husband, daughter, and cats.

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Comparative morphology of changeable skin papillae in octopus and cuttlefish
Justine J. Allen, George R. R. Bell,Alan M. Kuzirian, Sachin S. Velankar,Roger T. Hanlon 2013 (subscription)

ABSTRACT
A major component of cephalopod adaptive camouflage behavior has rarely been studied: their ability to change the three-dimensionality of their skin by morphing their malleable dermal papillae. Recent work has established that simple, conical papillae in cuttlefish (Sepia officinalis) function as muscular hydrostats; that is, the muscles that extend a papilla also provide its structural support. We used brightfield and scanning electron microscopy to investigate and compare the functional morphology of nine types of papillae of different shapes, sizes and complexity in six species: S. officinalis small dorsal papillae, Octopus vulgaris small dorsal and ventral eye papillae,Macrotritopus defilippi dorsal eye papillae, Abdopus aculeatus major mantle papillae, O. bimaculoides arm, minor mantle, and dorsal eye papillae, and S. apama face ridge papillae. Most papillae have two sets of muscles responsible for extension: circular dermal erector muscles arranged in a concentric pattern to lift the papilla away from the body surface and horizontal dermal erector muscles to pull the papilla's perimeter toward its core and determine shape. A third set of muscles, retractors, appears to be responsible for pulling a papilla's apex down toward the body surface while stretching out its base. Connective tissue infiltrated with mucopolysaccharides assists with structural support. S. apama face ridge papillae are different: the contraction of erector muscles perpendicular to the ridge causes overlying tissues to buckle. In this case, mucopolysaccharide-rich connective tissue provides structural support. These six species possess changeable papillae that are diverse in size and shape, yet with one exception they share somewhat similar functional morphologies. Future research on papilla morphology, biomechanics and neural control in the many unexamined species of octopus and cuttlefish may uncover new principles of actuation in soft, flexible tissue. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.
 
Microanatomy and ultrastructure of outer mantle epidermis of the cuttlefish, Sepia esculenta (Cephalopoda: Sepiidae)
Dong Geun Lee, Min Woo Park, Byeong Hak Kim, Hyejin Kim, Mi Ae Jeon, Jung Sick Lee 2013 (subscription)

Abstract
This study describes the ultrastructural characteristics of external epidermis of mantle of Sepia esculentausing light and electron microscopy. The epidermis was thicker on the ventral surface than on the dorsal surface, with a higher secretory cell distribution on the ventral surface than on the dorsal surface. The epidermis was a single layer composed of epithelial cells, secretory cells, ciliated cells and neuroglial cells. Epithelial cells were columnar with well-developed microvilli on the free surface, and the microvilli were covered with glycocalyx. The epithelial cells were connected to the neighboring cells by tight junctions and membrane interdigitations of the apico-frontal surface. Well-developed microfilaments were arranged in a vertical direction in the cortical cytoplasm. The secretory cells were categorized into three types (A, B and C) in accordance with the light microscopical characteristics and ultrastructures of the secretory granules. The distribution of these cells was in the following order: Type A > Type B > Type C. SEM observation revealed that the secretory pore size of the Type A secretory cells was approximately 8.6 × 12.2 μm2. Cytoplasm displayed a red color as the result of Masson's trichrome stain and H-E stain, and contained polygonal granules of approximately 1.2 μm2 with a high electron density. The secretory pore size of the Type B secretory cells was approximately 10.1 × 12.1 μm2. As the results of AB-PAS (pH 2.5) and AF-AB (pH 2.5) reactions, the cytoplasm displayed a red color. The cells contained membrane bounded secretory granules with very low electron density. The secretory pore of the Type C secretory cells was circular shape, and approximately 5.5 × 5.5 μm2. Cytoplasm was found to be homogeneous under H-E stain and Masson's trichrome stain, and displayed a red color. As the result of AB-PAS (pH 2.5) reaction, the cytoplasm displayed a red color. The electron density of the secretory substance was the highest among the three types of secretory cells. The ciliated cells had a ciliary tuft on the free surface and were distributed throughout the mantle with the exception of the adhesive organs. Neuroglial cells were connected to the basal membrane, epithelial cells, secretory cells and nerve fibers through cytoplasmic process, and contained neurosecretory granules with high electron density within the cytoplasm.
 
Chameleon of the sea' reveals its secrets: Cuttlefish may offer model for bioinspired human camouflage and color-changing products Cambridge, MA | Posted on January 28th, 2014
More on the research coming from the US Army grant.


Chromatophores were previously thought to be simply sacs of pigment that acted as filters; scientists have now discovered that nanostructures (labeled here as "granules") within the cells are capable of fluorescing.

Abstract:
Scientists at Harvard University and the Marine Biological Laboratory (MBL) hope new understanding of the natural nanoscale photonic device that enables a small marine animal to dynamically change its colors will inspire improved protective camouflage for soldiers on the battlefield.

The cuttlefish, known as the "chameleon of the sea," can rapidly alter both the color and pattern of its skin, helping it blend in with its surroundings and avoid predators. In a paper published January 29 in the Journal of the Royal Society Interface, the Harvard-MBL team reports new details on the sophisticated biomolecular nanophotonic system underlying the cuttlefish's color-changing ways.

"Nature solved the riddle of adaptive camouflage a long time ago," said Kevin Kit Parker, Tarr Family Professor of Bioengineering and Applied Physics at the Harvard School of Engineering and Applied Sciences (SEAS) and core faculty member at the Wyss Institute for Biologically Inspired Engineering at Harvard. "Now the challenge is to reverse-engineer this system in a cost-efficient, synthetic system that is amenable to mass manufacturing."

In addition to textiles for military camouflage, the findings could also have applications in materials for paints, cosmetics, and consumer electronics.

The cuttlefish (Sepia officinalis) is a cephalopod, like squid and octopuses. Neurally controlled, pigmented organs called chromatophores allow it to change its appearance in response to visual clues, but scientists have had an incomplete understanding of the biological, chemical, and optical functions that make this adaptive coloration possible.

To regulate its color, the cuttlefish relies on a vertically arranged assembly of three optical components: the leucophore, a near-perfect light scatterer that reflects light uniformly over the entire visible spectrum; the iridophore, a reflector comprising a stack of thin films; and the chromatophore. This layering enables the skin of the animal to selectively absorb or reflect light of different colors, said coauthor Leila F. Deravi, a research associate in bioengineering at Harvard SEAS.

"Chromatophores were previously considered to be pigmentary organs that acted simply as selective color filters," Deravi said. "But our results suggest that they play a more complex role; they contain luminescent protein nanostructures that enable the cuttlefish to make quick and elaborate changes in its skin pigmentation."

When the cuttlefish actuates its coloration system, each chromatophore expands; the surface area can change as much as 500 percent. The Harvard-MBL team showed that within the chromatophore, tethered pigment granules regulate light through absorbance, reflection, and fluorescence, in effect functioning as nanoscale photonic elements, even as the chromatophore changes in size.

"The cuttlefish uses an ingenious approach to materials composition and structure, one that we have never employed in our engineered displays," said coauthor Evelyn Hu, Tarr-Coyne Professor of Applied Physics and of Electrical Engineering at SEAS. "It is extremely challenging for us to replicate the mechanisms that the cuttlefish uses. For example, we cannot yet engineer materials that have the elasticity to expand 500 times in surface area. And were we able to do so, the richness of color of the expanded and unexpanded material would be dramatically different—think of stretching and shrinking a balloon. The cuttlefish may have found a way to compensate for this change in richness of color by being an 'active' light emitter (fluorescent), not simply modulating light through passive reflection."

The team also included Roger Hanlon and his colleagues at the Marine Biological Laboratory in Woods Hole, Mass. Hanlon's lab has examined adaptive coloration in the cuttlefish and other invertebrates for many years.

"Cuttlefish skin is unique for its dynamic patterning and speed of change," Hanlon said. "Deciphering the relative roles of pigments and reflectors in soft, flexible skin is a key step to translating the principles of actuation to materials science and engineering. This collaborative project expanded our breadth of inquiry and uncovered several useful surprises, such as the tether system that connects the individual pigment granules."

For Parker, an Army reservist who completed two tours of duty in Afghanistan, using the cuttlefish to find a biologically inspired design for new types of military camouflage is more than an academic pursuit. He understands first-hand that poor camouflage patterns can cost lives on the battlefield.

"Throughout history, people have dreamed of having an 'invisible suit,'" Parker said. "Nature solved that problem, and now it's up to us to replicate this genius so, like the cuttlefish, we can avoid our predators."

In addition to Parker, Hu, Hanlon, and Deravi, the coauthors of the Interface paper are: Andrew P. Magyar, a former postdoctoral student in Hu's group; Sean P. Sheehy, a graduate student in Parker's group; and George R. R. Bell, Lydia M. Mäthger, Stephen L. Senft, Trevor J. Wardill, and Alan M. Kuzirian, who all work with Hanlon in the Program in Sensory Physiology and Behavior at the Marine Biological Laboratory.
 
The structure–function relationships of a natural nanoscale photonic device in cuttlefish chromatophores
Leila F. Deravi,Andrew P. Magyar,Sean P. Sheehy,George R. R. Bell, Lydia M. Mäthger, Stephen L. Senft,Trevor J. Wardill, William S. Lane, Alan M. Kuzirian,Roger T. Hanlon, Evelyn L. Hu,Kevin Kit Parker 2014 (subscription)
Abstract
Cuttlefish, Sepia officinalis, possess neurally controlled, pigmented chromatophore organs that allow rapid changes in skin patterning and coloration in response to visual cues. This process of adaptive coloration is enabled by the 500% change in chromatophore surface area during actuation. We report two adaptations that help to explain how colour intensity is maintained in a fully expanded chromatophore when the pigment granules are distributed maximally: (i) pigment layers as thin as three granules that maintain optical effectiveness and (ii) the presence of high-refractive-index proteins—reflectin and crystallin—in granules. The latter discovery, combined with our finding that isolated chromatophore pigment granules fluoresce between 650 and 720 nm, refutes the prevailing hypothesis that cephalopod chromatophores are exclusively pigmentary organs composed solely of ommochromes. Perturbations to granular architecture alter optical properties, illustrating a role for nanostructure in the agile, optical responses of chromatophores. Our results suggest that cephalopod chromatophore pigment granules are more complex than homogeneous clusters of chromogenic pigments. They are luminescent protein nanostructures that facilitate the rapid and sophisticated changes exhibited in dermal pigmentation.
 
Colour gamuts in polychromatic dielectric elastomer artificial chromatophores
Jonathan Rossiter ; Andrew Conn ; Antonio Cerruto ; Amy Winters ; Calum Roke

abstract
Chromatophores are the colour changing organelles in the skins of animals including fish and cephalopods. The ability of cephalopods in particular to rapidly change their colouration in response to environmental changes, for example to camouflage against a new background, and in social situations, for example to attract a mate or repel a rival, is extremely attractive for engineering, medical, active clothing and biomimetic robotic applications. The rapid response of these chromatophores is possible by the direct coupling of fast acting muscle and pigmented saccules. In artificial chromatophores we are able to mimic this structure using electroactive polymer artificial muscles. In contrast to prior research which has demonstrated monochromatic artificial chromatophores, here we consider a novel multi-colour, multi-layer, artificial chromatophore structure inspired by the complex dermal chromatophore unit in nature and which exploits dielectric elastomer artificial muscles as the electroactive actuation mechanism. We investigate the optical properties of this chromatophore unit and explore the range of colours and effects that a single unit and a matrix of chromatophores can produce. The colour gamut of the multi-colour chromatophore is analysed and shows its suitability for practical display and camouflage applications. It is demonstrated how, by varying actuator strain and chromatophore base colour, the gamut can be shifted through colour space, thereby tuning the artificial chromatophore to a specific environment or application. © (2014) COPYRIGHT Society of Photo-Optical Instrumentation Engineers (SPIE). Downloading of the abstract is permitted for personal use only.
 
Expression of squid iridescence depends on environmental luminance and peripheral ganglion control
P. T. Gonzalez-Bellido, T. J. Wardill, K. C. Buresch, K. M. Ulmerand, R. T. Hanlon 2013 (subscription)

Squid display impressive changes in body coloration that are afforded by two types of dynamic skin elements: structural iridophores (which produce iridescence) and pigmented chromatophores. Both color elements are neurally controlled, but nothing is known about the iridescence circuit, or the environmental cues, that elicit iridescence expression. To tackle this knowledge gap, we performed denervation, electrical stimulation and behavioral experiments using the long-fin squid, Doryteuthis pealeii. We show that while the pigmentary and iridescence circuits originate in the brain, they are wired differently in the periphery: (1) the iridescence signals are routed through a peripheral center called the stellate ganglion and (2) the iridescence motor neurons likely originate within this ganglion (as revealed by nerve fluorescence dye fills). Cutting the inputs to the stellate ganglion that descend from the brain shifts highly reflective iridophores into a transparent state. Taken together, these findings suggest that although brain commands are necessary for expression of iridescence, integration with peripheral information in the stellate ganglion could modulate the final output. We also demonstrate that squid change their iridescence brightness in response to environmental luminance; such changes are robust but slow (minutes to hours). The squid's ability to alter its iridescence levels may improve camouflage under different lighting intensities.
 
Proteinaceous light diffusers and dynamic 3-D skin texture in cephalopods
PI: Roger T. Hanlon 2014 (pdf)

Executive Summary
This project discovered fundamental and novel mechanisms of structural coloration in cephalopods as well as the biomechanics of dynamic skin papillae that produce morphing soft skin. Two mechanisms of producing whiteness in flexible skin were revealed. First, spherical proteinaceous leucosomes produce uniform and highly efficient whiteness in all directions and from all viewing angles. Second, proteinaceous platelets in specific arrangements can also produce diffuse whiteness, but not with the efficiency of spherical leucosomes. Skin papillae that dynamically produce morphing 3D skin were also characterized biomechanically via gross and fine morphology; they are basically constructed as a muscular hydrostat (similar to a human tongue, elephant trunk, or octopus arm). For each research project, sufficient modeling of the structures and
spectrometry was accomplished and published to enable initial stages of transfer to materials science. An additional project involved dynamic structural coloration of iridophores; the neurophysiological control of iridescence was discovered to involve aspects of peripheral control (as opposed to solely brain control). In addition to biological achievements, this grant developed new methodology for high-resolution imaging of
coloration elements in biological tissue.
 
Wow- amazing article on lizards! So incredible! Cephalopods have opsins in the skin that are mentioned to possibly offer some degree of light sensing ability but the degree to which this actually helps camouflage (I think) is unknown.
 
Nice to know that there are similar physical properties. Maybe this study will encourage (or expose one already done) ceph experimentation. I remember @robyn creating a blindfold of sorts for squid for one of her pain experiments (I don't think it totally removed sight though - sadly the blogs did not survive the softward upgrade so I can't find the images or post) but coming up with something for octopuses or cuttles that does not involve permanent blinding would be difficult.
 
Behavioral Analysis of Cuttlefish Traveling Waves and Its Implications for Neural Control
Andres Laan, Tamar Gutnick, Michael J. Kuba1, Gilles Laurent 2014 (subscription)

Summary
Traveling waves (from action potential propagation to swimming body motions or intestinal peristalsis) are ubiquitous phenomena in biological systems and yet are diverse in form, function, and mechanism. An interesting such phenomenon occurs in cephalopod skin, in the form of moving pigmentation patterns called “passing clouds” [1]. These dynamic pigmentation patterns result from the coordinated activation of large chromatophore arrays [2]. Here, we introduce a new model system for the study of passing clouds, Metasepia tullbergi, in which wave displays are very frequent and thus amenable to laboratory investigations. The mantle of Metasepia contains four main regions of wave travel, each supporting a different propagation direction. The four regions are not always active simultaneously, but those that are show synchronized activity and maintain a constant wavelength and a period-independent duty cycle, despite a large range of possible periods (from 1.5 s to 10 s). The wave patterns can be superposed on a variety of other ongoing textural and chromatic patterns of the skin. Finally, a traveling wave can even disappear transiently and reappear in a different position (“blink”), revealing ongoing but invisible propagation. Our findings provide useful clues about classes of likely mechanisms for the generation and propagation of these traveling waves. They rule out wave propagation mechanisms based on delayed excitation from a pacemaker [ 3] but are consistent with two other alternatives, such as coupled arrays of central pattern generators [ 3] and dynamic attractors on a network with circular topology [ 4].
 
Octopus-inspired sensor can detect colours

New York: In a first, researchers have created a light detector that responds to red, green and blue light like the human eye does.
The researchers from Rice University were inspired by the skin of cephalopods like octopus and squid, which they believe, can detect colour directly through their skin. The sensor they have created uses complementary metal-oxide semi-conductor (CMOS) technology and can fit on a self contained chip.
"Today's colour filtering mechanisms often involve materials that are not CMOS-compatible, but this new approach has advantages beyond on-chip integration," said Naomi Halas from Rice University.
It is also more compact and simple and more closely mimics the way living organisms see colours, Halas added.
The sensor is a result of a $6 million research programme funded by the US Office of Naval Research that aimed to mimic cephalopod skin using metamaterials - compounds that blur the line between material and machine.

Cephalopods like octopus and squid are masters of camouflage but they are also colour blind.
Based on this hypothesis, Rice University student Bob Zheng designed a photonic system that could detect coloured light.
"Bob has created a biomimetic detector that emulates what we are hypothesising the squid skin sees," Halas added.
The research was published in the journal Advanced Materials.
 

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