Hidden in Plain Sight - Scientific American

ONE OF THE MAIN FUNCTIONS of visual perception is to detect objects in the environment as a prelude to identifying them as prey, predators or mates. Not surprisingly, both prey and predators go to enormous lengths to conceal their physical boundaries by blending in with the color and texture of their surroundings. Indeed, we can almost think of higher visual processing in the brain as having mainly evolved to defeat camouflage. Studying the strategies of camouflage can therefore indirectly also tell us a great deal about the mechanisms of vision.
American painter and amateur naturalist Abbott Handerson Thayer speculated that animals developed “protective coloration.” As his theory held, “animals are painted by nature darkest on those parts which tend to be most lighted by the sun’s light, and vice versa.” He was surely right about this effect (scientists now call it “countershading”). But then he went on, even suggesting that peacocks’ tails match foliage and that flamingos are pink to allow them to blend in with the sunset (a)!
To modern scientists, Thayer obviously got a bit carried away. Yet as the saying goes, “fact is stranger than fiction.” Some animals, such as cuttlefish, octopuses and flounder, can alter their markings and hues to suit whatever surface they happen to land on. Although chameleons are often credited with this skill, they are actually quite bad at it; most of their color changes are reserved mainly to attract mates and protect their territories and are thus unrelated to camouflage.
Biologist Francis B. Sumner, one of the founders (but not the sole flounder) of the Scripps Institution of Oceanography, showed nearly a century ago that cold-water flounder have an amazing capacity to match the “graininess” of their skin surface markings with gravel or pebbles in their background. Sumner’s work was supplemented by the experiments of S. O. Mast, who in the early 20th century showed that the matching depends on vision; blinded flounder do not change.
Sumner’s findings made a big splash when he published them. But they were later challenged by neurobiologist William M. Saidel, now at Rutgers University at Camden. Saidel claimed that the markings on flounder changed only slightly but that they had a kind of “universal” texture that allowed them to blend in with most backgrounds. So, he argued, in a sense it was the viewer’s eye that was doing the blending—not the flounder itself.
Cold-water flounder live in a rather drab, monotonous sandy environment. It occurred to us that this fact could account for the poor show put on by Saidel’s flounder, which would not have had the evolutionary pressures to adapt to a greater range of backgrounds; unlike the cold-water locations, the tropical environment contains more varied surfaces. In collaboration with Christopher W. Tyler, Richard L. Gregory and Chandramani Ramachandran, we therefore decided to experiment with the tropical reef flounder Bothus ocellatus, commonly known as the eyed flounder.
We obtained six specimens from an aquarist. After the fish had adapted to a “neutral,” beige-colored fine gravel floor in a holding tank (b), we moved them into small experimental tanks that each had different patterns on their floors. We selected patterns that, though not found in nature, would clearly demonstrate the limits of the fish’s ability to adapt actively, or dynamically, to their surrounding environment.
The results were remarkable. In every case, the fish were able to achieve an impressively good match when “plaiced” on various backgrounds of coarse check patterns (c), medium and fine checks (d), pebbles (e, next page) or fine gravel. Even more startling, we found that the fish transformed in just two to eight seconds—not the several minutes that Mast and Sumner had implied. We knew then that there must be a neural “reflex” at work. The reaction was too fast to be hormonal.
The fish’s eyes, we determined, must be getting a highly foreshortened, distorted view of the background, given their vantage point at the bottom and the distortions of its optics. The fish have turretlike eyes mounted on stalks, with which they quickly scan the surrounding floor texture. Our colleagues are often very puzzled that the fidelity of matching is so precise given these distortions. But this conformity is no more unexpected to neuroscientists like ourselves than is the fact that we do not see the world upside down, even though the retinal image is. Because no actual cinema screen with a picture exists in the brain, the question of “correction” does not even arise; the brain encodes visual information in such a way that the correction for a flawed or noisy sensory input is already implied in the code itself. In much the same way, the fish’s brains must make adjustments so that the camouflage pattern is produced accurately.
How do the fish achieve such dynamic camouflage? Examination through the dissecting microscope revealed that the skin has clusters of cells containing the dark pigment melanin, called melanophores. By varying the dispersal of melanin pigment granules in these cells, the fish can alter the contrast of small patches of skin. In addition, we saw what appeared to be at least four classes of clusters of different sizes and a single isolated cluster on the middle of the fish. By independently varying the contrast of these four types of clusters—a bit like dialing up the contrast knob on an old television set—the fish can vary the ratio of different pixel types and achieve a reasonable facsimile of the most commonly encountered textures on the ocean floor where they live. This system is analogous to the manner in which one can use just three “primary” wavelengths in various ratios to produce any conceivable color that the eye can see. By analyzing the the pattern on the fish and corresponding background with a mathematical technique called principle component analysis, we were able to establish that the fish have independent visual control of each set of markings.
Just for the halibut, we tried putting the fish on a background of polka dots. Amazingly, their entire skin went pale and became homogeneous except for one small conspicuous black dot right on the center of the body (f, next page). The fish were making a valiant attempt to match the polka dots! See if you can spot the fish in the photograph.
Flounder also use other visual tricks to deceive predators. When we approached one menacingly with an aquarium net, it would move forward and stir up the sand, “pretending” to bury itself in one location while it actually retreated at lightning speed and buried itself elsewhere.
Squid, cuttlefish and octopuses (g, next page) are also masters of camouflage. Yet instead of dispersing pigments, they simply open or close opaque “shutters” across skin patches. Even more intriguing, they match not only the color and texture of the background but the shapes of objects in the vicinity as well (h)—as elegantly shown by Roger T. Hanlon and his colleagues at the Marine Biological Laboratory in Woods Hole, Mass. Octopuses can distort their forms to mimic various poisonous sea creatures, such as snakes and lionfish. The mechanism is not known. Nerve cells—called mirror neurons—have been identified in the brains of primates that may be involved in mimicry of the postures and actions of others. We suggest that analogous cells have evolved in the brains of cephalopods through convergent evolution—which would be astonishing given that vertebrates diverged from invertebrates over 60 million years ago.
Figuring out the mechanisms of dynamic camouflage in flounder may have obvious military applications. Taking a lesson from the fish, the military could use a small number of changing pigmented splotches to “match” a tank to its background far better than a static paint scheme. Such experiments, far from being just a fishing expedition, can give us vital clues about the evolution of visual perception.
This article was originally published with the title "Illusions: Hidden in Plain Sight" in SA Mind 16, 4, 16-18 (December 2005)
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