A juvenile cuttlefish mimicking 3D white pillars, illuminated from above, against a grey background. Photo credit: Aliya El Nagar.

A juvenile cuttlefish mimicking 3D white pillars, illuminated from above, against a grey background. Photo credit: Aliya El Nagar.

When you're small and tasty, it's best to blend in with your surroundings. Stand out, and your days are likely to be numbered. Many creatures have mastered the art of disguise, mimicking thorns and leaves or rippling bark and submerged marine landscapes. But a few camouflage rock stars take dissembling to a whole other dimension, actively adjusting their appearance to match their background. ‘Cuttlefish can very quickly change their appearance in response to what they see at any time’, says Aliya El Nagar, from the University of Leeds, UK, explaining that the versatile cephalopods can adjust the pattern on their backs instantly: which is fantastic when you want to merge in against a flat sandy surface. But how well do these visual virtuosos cope when the surroundings are more 3-dimensional? Cuttlefish can't contort their bodies like octopuses to recreate contours, so they must find other ways of mimicking the light and shade cues that imply height and depth.

El Nagar joined Daniel Osorio at the University of Sussex, UK, to find out how well cuttlefish youngsters could match themselves to a grid of pillars and which aspects of the scene the cephalopods call on when attempting to merge with their surroundings. She arranged 15 mm high white clay cylinders in a grid on a grey background. Then, El Nagar gave the youngsters time to settle in and do their best to blend in with the pillars as she illuminated them from above, or from the side – to cast a shadow – and waited to see how the youngsters responded. In addition, she tested the cuttlefish's responses to grey cylinders that stood out less well from the background, 30 mm tall white cylinders that cast even longer shadows, as well as recreating the 3D world in 2D by printing white dots on a grey background and adding black crescents to reproduce the shadows cast by the short and tall cylinders.

So how did the cuttlefish react? Having blended in well with a plain grey background, the youngsters displayed a white patch in their backs when mimicking the white dots, but when impersonating the 15 mm tall white cylinders, they added a black bar behind the white patch. The cephalopods produced a unique camouflage pattern, which scientists hadn't noticed before, when they were trying to hide within the cylinder grid, regardless of how well the white or grey cylinders stood out from the background. ‘The animals are displaying a pattern that matches a three-dimensional environment, and not one that just matches the exact two-dimensional (flat) image that is on the retina in their eyes’, says El Nagar.

However, the shadows cast by the cylinders had no effect on the cuttlefish's disguise, until the shadows were at their longest, matching the printed spots with the widest black crescents. Then, the animals resorted to a style of pattern that breaks up their outline to help them blend in. ‘This suggests that the cuttlefish perceive the real stationary shadows not as complementary depth cues, but purely as darker areas’, says El Nagar.

She and her colleagues, Osorio, Sarah Zyinski (Bangor University, UK) and Steven Sait (University of Leeds), suspect that the master mimics first assess their surroundings and then select the most appropriate camouflage pattern from a catalogue of appearances that they can assume. For now, the visual characteristics that provide cuttlefish with a 3D sense of the world mostly remain a mystery, but the shadows cast by objects appear not to be one of them.

El Nagar
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Zylinski
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and
Sait
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(
2021
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Visual perception and camouflage response to 3D backgrounds and cast shadows in the European cuttlefish, Sepia officinalis
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J. Exp. Biol.
224
,
jeb238717
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