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17th September 2015
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Masters of disguise

Kathryn Roberts, 17/09/2015

EU cuttlefish

Camouflage has always been central to warfare; but the need for camouflage goes beyond the protection of the armed forces. The ability to replicate animal and environmental colours and patterns could enable a robot to blend into its environment for more effective monitoring, for example, and the concept can be exploited in the design of smart materials that respond to social, medical and even emergency situations.

Nature has already provided many examples of successful camouflage – think of the dazzling geometry of zebra stripes in bright sunshine and the changing colours of the chameleon, for example. But it seems she still holds a ‘trump’ card.

In the oceans of Europe and Australasia live over 100 species of cuttlefish. These flesh-eating cephalopods can change the colour, pattern and even shape of their skin, in milliseconds, to blend in with their surroundings to protect themselves from predators or to attract a mate or repel a rival; either way, it is an amazing sight. Their closely related cousins, squids and octopuses, are similarly talented.

According to Roger Hanlon, a marine biologist at the Woods Hole Marine Biological Laboratory in Massachusetts, US, who has spent many years studying these molluscs: ‘There is no skin on Earth like that of the cuttlefish. The diversity is fantastic; chameleons are boring by comparison. This is fast, sophisticated and adaptable camouflage.’

The secret to this incredible skill lies in the various layers of the cuttlefish skin.1 The top layer comprises layers of yellow, red and brown pigmented cells or ‘chromatophores’. Underneath these chromatophores lies a layer of reflecting cells – iridophores – that contain the protein reflectin; these cells reflect colours such as blue and green along with red and pink. The luminous colours of these ‘iridescent’ cells can appear to change colour when viewed from different angles, providing a beautiful shimmering effect. A base layer made up of bright white ‘leucophores’ completes the cuttlefish palette.

The cells – chromatophores, iridophores and leucophores – work together to provide the colour, pattern and brightness of cephalopod skins: the chromatophores control the transmission of light; the iridophores and leucophores control the reflection of light. ‘There is no limit to the colours they can show in their skin. It’s really marvellous,’ says Hanlon. ‘Along with colour and pattern changes, the skin can also change its texture, pushing up bumps along its surface, all of which means that the cuttlefish can fool just about any visual predator,’ he says.

To mimic their surroundings in an instant, the cuttlefish relies on its acute eyesight, which is also sensitive to polarised light. Visual cues go straight to the brain and the brain in turn sends instructions to the skin cells – it is very quick, explains Hanlon. ‘The cuttlefish seems to have evolved a short-cut of sorts to quickly analyse such complex backgrounds, such as coral reefs – it appears to use just a few visual cues to make its decision for which camouflage pattern to deploy.’

Biomimetic research

Not surprisingly, these masters of illusion have attracted the attention of researchers looking to mimic their camouflage properties to create a host of smart materials.

Professor of chemical engineering and materials science, Alon Gorodetsky and his team at the University of California, Irvine, US, for example, took their inspiration from the iridophores contained in the squid (Doryteuthis (Loligo) pealeii) skin.

In 2010, Daniel Morse at the University of California, Santa Barbara, US, had discovered that iridophores contain deep pleats within the cell membrane, which extend into the body of the cell. ‘The pleats essentially consist of alternating layers of a membrane enclosed protein – reflectin – and extracellular space,’ explains Gorodetsky.2 This structure forms a tuneable Bragg reflector, ie it reflects light in a regular and predictable way. Morse showed that reversible phosphorylation of reflectin inside the iridophores changes the size and spacing of between the alternating layers, modulating the reflectance in the process.3

Long Phan, graduate research assistant in the Gorodetsky group, explains: ‘When the cephalopod skin decides it needs to change colour, acetylcholine is released, which causes a cascade of chemical reactions that ultimately cause the release of protein kinases and protein phosphatases that either phosphorylate or de-phosphorylate the reflectin. This changes the thickness of the reflectin layer and consequently the reflected colour of light.’

Speaking at the ACS meeting in Denver earlier in 2015, Gorodetsky explained how his team first engineered E. coli bacteria to produce reflectin in large quantities. They obtained 1g of the pure (99%) protein per litre of E. coli. They then coated the protein onto a polymeric flexible film, more specifically fluorinated ethylene propylene (FEP), to make what he called ‘invisibility stickers’. A thin (<5nm) graphene oxide layer helps the protein adhere to the tape. FEP was chosen, he said, because it is cheap, chemically inert and transparent, and is available as a sticky tape, making it easy to bond to a variety of different surfaces.

‘The great thing about these films,’ said Gorodetsky, ‘is that they can be manipulated into just about any colour by changing their thickness. Thin films of the order of ca65nm, appear blue, while thicker ones appear orange.’ Their proof-of-concept experiments showed that the films can also be tuned to reflect in the near infrared, by simply increasing their thickness to around 163nm. This property would be particularly useful for disguising soldiers vulnerable to active infrared cameras. ‘The stickers,’ said Gorodetsky, ‘could be stuck onto soldiers’ uniforms and equipment, and act as camouflage.’

In their initial experiments, the team found they could change the thickness of the films by using chemical means, ie exposure to acetic acid fumes. More recently, they have shown that a simple mechanical stimulus, ie stretching the film, causes the colour to change, which avoids the need for harsh chemicals.

However, the technology isn’t quite ready for field use yet; the researchers still have to work out a way of increasing the brightness of the stickers and get multiple stickers to respond in the same way at the same time as part of an adaptive camouflage system. ‘The way we plan to increase the brightness is to make multilayer structures similar to the structure of cephalopod skins – after all they produce bright shimmering colours.’ Ultimately, he said, they want to make their tape easy to use and completely disposable.

Meanwhile, researchers from the University of Bristol, UK, have focused their attention on the pigment-carrying chromatophores found in the skin not only of cephalopods, such as the squid, but also in the zebrafish in an attempt to make camouflaging smart materials.

A chromatophore in squid skin comprises a central sac containing granules of pigment, which is attached to surrounding muscles that can pull the sac out radially into a disc of colour. When the cell needs to change colour, the brain sends a signal to the muscles to contract, which results in the sac expanding and generating an optical effect – the squid skin changes colour.

In contrast, the chromatophores in the zebrafish have a fixed shape and sit in the sub-dermal layer. They contain a reservoir of black pigmented fluid, which when activated – by the presence of certain hormones, for example, during a mating period – travels to the skin surface and spreads out. The original dark spots on the surface of the zebrafish get bigger, creating an optical effect, which can help the fish fend off predators or attract a mate.

The Bristol research is being led by Jonathan Rossiter, professor of robotics in the department of engineering mathematics, and Andrew Conn in the department of mechanical engineering; a key research collaborator on the project is Amy Winters of Rainbow Winters, a London-based firm that merges technology with fashion.

Conn explains: ‘We are developing artificial chromatophores for soft and flexible colour changing smart skins. We are investigating artificial muscle technologies based on polymers to create smart skins that modulate reflected light and are largely independent of light level and viewing angle – this is an extremely attractive property for reflective displays, smart clothing and active camouflage.’

The Bristol researchers have already created artificial chromatophores based on the two different models. In experiments done in 2012, Conn says they demonstrated the first smart material structures capable of mimicking the muscular expansions of biological chromatophores.

To copy the camouflaging properties of squid’s chromophore sac, the team used a soft electroactive polymer – a 500µm thick polyacrylate film – that is capable of taking strain in a similar way to the biological muscle with the same fast response times. Initially, they made a single spot chromophore of ca19mm diameter, which was connected to a high voltage supply via copper electrodes.

Two states were observed – voltage on, which resulted in an increase in the area of the sac; and voltage off and the sac contracts – similar behaviour to the biological chromatophore. They then made a series of multispot chromophores, arranged in groups of three to mimic more closely those found in the cephalopod’s skin. These structures again showed a significant response to electrical stimuli with the associated optical changes, specifically optical reflectivity and opacity.

Around the same time, in separate experiments, the researchers made an artificial ink-cell similar to that found in the zebrafish skin. The cell consisted of two glass microscope slides with a moulded silicone chamber between them; two pumps, made from electroactive polymers, were positioned either side of the chamber. In between the pumps and microscope slide are two syringes, one containing a clear organic solvent, such as white spirit, and the other containing an opaque water-based ink, ie black inkjet ink.

According to the researchers: ‘Since the two liquids are immiscible, the phase interface between the two liquids corresponds to a discrete change in opacity. By hydraulic pumping of the fluid, the opacity of the ink cell can be reversibly switched from completely transparent to completely opaque.’4 They had achieved a monochromatic colour change and provided a potential means of creating an artificial camouflage skin.

Since then, the Bristol researchers have developed more complex arrays of multi-coloured chromophores that are even closer to mimicking the actual layers of chromophores found in the biological skins. Conn explains: ‘By layering arrays of polychromatic active chromophores, the overall colour and pattern of the skin can be controlled.’

In the most recent development, Rossiter and his team have demonstrated, by using mathematical modelling, that such an artificial skin can indeed mimic the complex, dynamic patterns generated in nature by cephalopods, such as cuttlefish, for camouflaging and signalling.5

For the immediate future, Conn says the benefactors of their technology are likely to be the consumer electronics industries, including fashion and defence industries which need coatings that can actively change their optical properties – not just visible colour, but also thermal characteristics and more complex optical transformations such as polarisation and iridescence.

Kathryn Roberts is a science writer based in London, UK

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