Weird pupils let octopuses see their colorful gardens

Octopuses, squid and other cephalopods are colorblind - their eyes see only black and white - but their weirdly shaped pupils may allow them to detect color and mimic the colors of their background, according to a father/son team of researchers from the University of California, Berkeley, and Harvard University.

For decades, biologists have puzzled over the paradox that, despite their brilliantly colored skin and ability to rapidly change color to blend into the background, cephalopods have eyes containing only one type of light receptor, which basically means they see only black and white.

Why would a male risk flashing its bright colors during a mating dance if the female couldn't even see him but a nearby fish could - and quickly gulp him down? And how could these animals match the color of their skin with their surroundings as camouflage if they can't actually see the colors?

According to UC Berkeley graduate student Alexander Stubbs, cephalopods may actually be able to see color - just differently from any other animal.

The key is an unusual pupil - U-shaped, W-shaped or dumbbell-shaped - that allows light to enter the eye through the lens from many directions, rather than just straight into the retina.

Human and other mammalian eyes have round pupils that contract to pinholes to give us sharp vision, with all colors focused on the same spot. But as anyone who's been to the eye doctor knows, dilated pupils not only make everything blurry, but create colorful fringes around objects, what is known as chromatic aberration.

This is because the transparent lens of the eye - which in humans changes shape to focus light on the retina - acts like a prism and splits white light into its component colors. The larger the pupillary area through which light enters, the more the colors are spread out. The smaller our pupil, the less the chromatic aberration. Camera and telescope lenses similarly suffer from chromatic aberration, which is why photographers stop down their lenses to get the sharpest image with the least color blurring.

Cephalopods, however, evolved wide pupils that accentuate the chromatic aberration, Stubbs said, and might have the ability to judge color by bringing specific wavelengths to a focus on the retina, much the way animals like chameleons judge distance by using relative focus. They focus these wavelengths by changing the depth of their eyeball, altering the distance between the lens and the retina, and moving the pupil around to changes its off-axis location and thus the amount of chromatic blur.

"We propose that these creatures might exploit a ubiquitous source of image degradation in animal eyes, turning a bug into a feature," Stubbs said. "While most organisms evolve ways to minimize this effect, the U-shaped pupils of octopus and their squid and cuttlefish relatives actually maximize this imperfection in their visual system while minimizing other sources of image error, blurring their view of the world but in a color-dependent way and opening the possibility for them to obtain color information."

U-shaped pupils

Stubbs has been fascinated by the color blind/camouflage paradox since he read about it in high school, and during diving excursions to Indonesia and elsewhere experienced firsthand how colorful cuttlefish, squid and octopus - and their surroundings - are.

He came up with the idea that cephalopods could use chromatic aberration to see color after photographing lizards that display with ultraviolet light, and noticing that UV cameras suffer from chromatic aberration. He teamed up with his father, Harvard astrophysicist Christopher Stubbs, to develop a computer simulation to model how cephalopod eyes might use this to sense color. The two will publish their hypothesis online this week in the journal Proceedings of the National Academy of Sciences.

They concluded that a U-shaped pupil like that of squid and cuttlefish would allow the animals to determine the color based on whether or not it was focused on its retina. The dumbbell-shaped pupils of many octopuses work similarly, since they're wrapped around the eyeball in a U shape and produce a similar effect when looking down. This may even be the basis of color vision in dolphins, which have U-shaped pupils when contracted, and jumping spiders.

"Their vision is blurry, but the blurriness depends on the color," Stubbs said. "They would be comparatively bad at resolving white objects, which reflect all wavelengths of light. But they could fairly precisely focus on objects that are purer colors, like yellow or blue, which are common on coral reefs and rocks and algae. It seems they pay a steep price for their pupil shape but may be willing to live with reduced visual acuity to maintain chromatically-dependent blurring, and this might allow color vision in these organisms."

"We carried out extensive computer modeling of the optical system of these animals, and were surprised at how strongly image contrast depends on color," said Harvard's Stubbs, a professor of physics and of astronomy. "It would be a shame if nature didn't take advantage of this."

The younger Stubbs extensively surveyed 60 years of studies of color vision in cephalopods, and discovered that, while some biologists had reported an ability to distinguish colors, others reported the opposite. The negative studies, however, often tested the animal's ability to see solid colors or edges between two colors of equal brightness, which is hard for this type of eye because, as with a camera, it's hard to focus on a solid color with no contrast. Cephalopods are best at distinguishing the edges between dark and bright colors, and in fact, their display patterns are typically regions of color separated by black bars.

"We believe we have found an elegant mechanism that could allow these cephalopods to determine the color of their surroundings, despite having a single visual pigment in their retina," he said. "This is an entirely different scheme than the multi-color visual pigments that are common in humans and many other animals. We hope this study will spur additional behavioral experiments by the cephalopod community."

Stubbs noted that cephalopods may not be losing much color information by having only one type of photoreceptor, since red colors are blocked by water so that only a reduced range of optical light actually penetrates to the shallow depths where they live. Having one photoreceptor that responds to a broad range of colors at that depth would allow them to see in dim light with their pupil fully dilated, while the off-axis pupil maintains the potential for spectral discrimination in high-light conditions.

Intriguingly, using chromatic aberration to detect color is more computationally intensive than other types of color vision, such as our own, and likely requires a lot of brainpower, Stubbs said. This may explain, in part, why cephalopods are the most intelligent invertebrates on Earth.

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The work was supported by UC Berkeley's Museum of Vertebrate Zoology, a Graduate Research Fellow Program grant to Alexander Stubbs, and Harvard University.

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