TWENTY metres underwater, off the coast of north-west Spain, biologist Roger Hanlon is stalking his prey. His camera is trained on a subject that has painted itself beige, grey and white to match the gravelly seabed. It perambulates towards a clump of kelp and, settling itself amid the fronds, quickly deepens its complexion to match their rich red-brown. This colour craft is impressive, but for Hanlon it is also baffling. He knows the common octopus is colour blind.
At least, that is what the textbooks tell us. In his own recent book, Hanlon lists multiple arguments for the cephalopods – octopuses, squid and cuttlefish – seeing in monochrome. Yet if you ask him casually, he remains unconvinced: “I would tend to think that cephalopods are able to sense and match colour somehow.”
Quite how they do it has confounded biologists for more than a century, though they have come up with some strange ideas to explain the conundrum. Now we are whittling down the spectrum of possibilities – in the hope of gaining an unprecedented insight into how these most alien of creatures see the world.
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Like Hanlon, the Nobel prize-winning zoologist Karl von Frisch didn’t believe cephalopods were colour blind. In the 1910s, he and the ophthalmologist Carl von Hess . Hess tested the vision of squid and cuttlefish by trapping the animals in tanks so small they could barely move and flashing coloured lights at them. He noted how their pupils responded to the lights and if they tried, unsuccessfully, to swim away. Their reactions, he concluded, mirrored patterns seen when people who are colour blind are shown coloured lights.
Frisch disliked such unnatural test conditions. He had already done experiments training minnows to expect food when shown a yellow card, and set out in a letter how he planned to train cephalopods to expect food from a red test tube. The results never surfaced, and the debate rumbled on, sometimes in dubious fashion. In 1950, zoologist Alfred KĂĽhn showed that if he kept hitting an octopus with a stick after flashing a coloured light at it, the animal learned to treat that colour as a warning and swam away. They . But in the 1970s, John Messenger, now based at the University of Cambridge, got the opposite result. He trained octopuses to attack coloured plastic rectangles for a reward of sardines. They knew black from white, but of equal brightness.
The eyes don’t have it
Any doubt that cephalopods were colour blind seemed to evaporate when we finally got to look at the biology behind their vision. As scientists dissected the eyes of more cephalopod species, they kept finding only one type of light-detecting protein, and nothing like the cone cells humans use for colour vision. By the 1980s, it was clear that this was true for almost all species, a strong pointer that they only see in black and white.
That just deepened the mystery of cephalopod camouflaging capabilities. We know the animals can match their skin tones to colours in their environment. We also know they signal to one another by creating vivid patterns on their skin. That is risky behaviour with predators out to eat you, so the idea that they only see the patterns in greyscale seems absurd. “Almost anyone who works in the field has a hard time believing it,” says at the University of California, Santa Barbara.
Meanwhile, Morse and Hanlon’s research teams have spent years demystifying the biomachinery in cephalopod skin responsible for body patterning. It is a sophisticated system, composed of at least two layers, with sacs of pigments in the upper one and tunable structures for iridescence in the lower. Yet Hanlon, who works at the Marine Biological Laboratory in Massachusetts, found himself returning to the colour vision mystery and feeling that he must be missing something. Eventually, he hit on an idea: if cephalopods don’t see colour with their eyes, perhaps they see it with their skin.
It wasn’t as bizarre as it sounds. At the time, other researchers were starting to discover that some species have light-detecting proteins called opsins in their skin. These are the same family of molecules that detect light in eyes, and we recently discovered that they appear in human skin too (see “The skin’s mystery sense”).
Hanlon did a quick search of the proteins in cuttlefish skin – and found . That 2010 discovery led to a whole new line of research. He teamed up with vision scientist and Alexandra Kingston, both at the University of Maryland, hoping to find out how the opsins were organised and whether they were connected to the skin’s colour-changing apparatus. If cephalopods were reacting directly to colour through connections in the skin without involving the brain, that might explain why they appeared incapable of consciously discriminating colour in behavioural studies.
The team spent five years shining lights on squid and cuttlefish skin, uncovering opsins here, there and everywhere. But the proteins seemed disorganised and apparently lacked any connection to the colour-changing systems. The researchers even found a slew of other molecules in the skin that are involved in processing signals from light. But “we never found anything that showed that this photosystem was doing anything”, says Cronin. “Although we have no doubt that it is.”
At the same time, Todd Oakley and Desmond Ramirez, then also at the University of California, Santa Barbara, were having more success with two-spot octopuses. They took pea-sized pieces of skin and placed them under a microscope to see the pigment sacs, then shone light on them. “There was a little bit of a delay and then this dramatic expansion,” says Oakley. This sac opening is one way cephalopods create colour. But though the experiment showed that , it didn’t explain how or why, nor whether opsins were involved.
“Cephalopods have three hearts and multiple brains – so why not alien senses?”
Recently, a new idea has started ruffling tentacles. Biologist Alexander Stubbs at the University of California, Berkeley, and his father , a Harvard physicist, turned to maths to solve the colour blindness problem. Their proposal, first published in 2016, centres on chromatic aberration, an effect where different wavelengths or colours of light come into focus at different distances from a lens. This happens in cameras and human eyes, but it is maximised in off-centre pupils – which cephalopods have. The pair calculated that this to distinguish colour with their eyes, without the need for dedicated colour-receptor molecules. “Think of having to bring different colours in and out of focus all the time, that’s kind of what their perception of the environment must be like,” says Alexander.
He says it is “just physically true” that the animals do this. Whether they use the information to discern colour is unclear. Alexander has mapped out experiments to test the idea, but he needs a collaborator to carry them out. Hanlon believes these experiments are worth doing, but he won’t buy the idea until he sees more than equations. “There’s not an ounce of data yet,” he says.
Meanwhile, the skin-sensing researchers are grappling with their own problems. One sticking point is that the opsins found in cephalopod skin are the same as those in their eyes. Given the evidence that the animals can’t see colour with their eyes, it looks as though they would need more than those same opsins to see it with their skin. Hanlon suggests that pigment sacs in the skin could act as crude filters for the opsins, so that two components can detect colour in tandem. Or perhaps there are undiscovered opsins in the skin. Screening the genomes of the animals should give an answer. Hanlon’s own institution, as it happens, is just finishing sequencing the squid genome.
Cronin is adamant the opsins aren’t redundant. “Oh, they’re doing something,” he says. “The fact that we didn’t find it just means it’s more obscure than we expected.” And maybe that obscurity shouldn’t be a surprise. Cephalopods have three hearts and multiple brains. Why should their senses be any less alien than the rest of their physiology?
The same goes for plenty of creatures that share their world. Some of their predators, such as diving birds, have colour-rich vision that makes a mockery of our own red-green-blue limitations. So although an octopus looks the same colour as its background when Hanlon peers through his camera, to a diving bird it might not.
To get around this, Hanlon is developing a hyper-spectral camera with 16 colour channels. “No one’s got a camera like this,” he says. And with no way for humans to see all the colours, he is having to invent ways to analyse the results. If they confirm that an octopus’s disguise is effective in the eyes of its predators, that would snuff out any doubts that they truly do colour-match. And how do they do it? Like everything else about the cephalopods, says Hanlon, the answer is going to be weird.
The skin’s mystery sense
The molecules in our eyes’ rod and cone cells that respond to light and help us see are called opsins. Over the past few years, we have found these proteins cropping up in all sorts of places other than the eyes. Which makes you wonder: what they are doing there?
Take tilapia fish, the fins of which take on a red hue in spawning season. In 2015, a study by researchers at Queen’s University in Canada showed that opsins in their skin seem to respond to seasonal changes in the colour of sunlight. Ultraviolet light tickles the opsins, which in turn prompts pigments in the skin to clump together, changing the colour.
In other animals, opsins outside the eyes probably play a role in setting circadian rhythms. But the case of the mantis shrimp is stranger. One species has opsins in a light-detecting organ attached to its brain. The shrimp has no eyes and may to sense danger.
Since the 1990s, we have known that opsins are also , including our own. In 2015, Elena Oancea at Brown University in Rhode Island was part of a team that discovered that we also , just as squid do. What they do there is far from clear, especially as unpublished research has found that at least one of these molecules has chemical tweaks that mean it doesn’t in fact respond to light. “We were very excited to find them and I would have predicted that in a couple of years we would have figured out what they do,” says Oancea. “But we don’t know.”
This article appeared in print under the headline “Sight unseen”
