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PACI F I C : Why Are Reef So Colorful? Bright patterns on reef fish are key to astound- LIZARD ingly complex strategies to attract mates, repel rivals and hide from predators by Justin Marshall

strange event, I was stunned background—and also, it would seem, mak- to realize the black dots were ing them an obvious meal. I wondered how the eyes of an enormous the environment of the reef could CAIRNS school of kyphosids swim- have given rise to the virtually invisible HERON ming past on their way to drummer and frogfish as well as the highly

ISLAND ) the reef edge. The bodies of conspicuous angelfish and butterfly fish.

globe these fish, which are also known as drummers, are Extreme about 30 centimeters (nearly 12 inches) long and are a sil- t is such questions that occupy me on

AUSTRALIA HAXBY ( ); WILLIAM F. very-blue color. When ver- Ifield trips to the University of Queens- map tical in water, they merged land’s research stations on Heron and Lizard perfectly with the dim, blue . These two islands are at either end light pervading the . of the 2,300-kilometer expanse of the Great

LAURIE GRACE ( GRACE LAURIE Here was a wonderful ex- Barrier Reef (map), which is by far the ample of camouflage under- largest reef system in the world and right- trangely enough, I became water. I was humbled by my ineptitude as fully one of its seven natural wonders. The curiousS about the colors of fish not while a predator—I allowed literally tons of fish to huge expanse is a living area of 200,000 diving in the crystal-clear waters of Aus- pass within a meter or two of me and my square kilometers consisting of some 3,000 tralia’s , surrounded by net before I even realized what they were. small reefs that include more than 400 spe- countless incredibly colorful fish. On the As a marine biologist interested in vision cies of hard and soft . For compari- contrary: I was in the murky, turbid wa- in the sea, however, I immediately thought son, a typical reef might be tens ters of Heron Island’s Coral Lagoon, of several questions. How is the skin of of kilometers long and have perhaps 40 near the southeastern edge of the reef, drummers so well adapted to merge with kinds of hard and soft corals. close to . the sea? What is it about the visual capa- Like terrestrial rain forests, coral reefs are Sitting slightly apprehensively at a depth bilities of the fish that prey on drummers isolated enclaves that are important for their of only two meters, I was trying to catch that enables them, presumably, to see the extreme biodiversity. In this respect, too, fish in a hand net. Suddenly I became dim- drummers while mine was so ineffective? the Great Barrier Reef is superlative: it is ly aware of hundreds of little black dots I noticed that many of the fish and other home to around 1,500 of fish. This shooting past me almost at the limits of my reef creatures that the school had by now huge variety is all the more surprising in vision in the silty water. Sucking air through joined were boldly colorful, their bright light of the relatively young age of the my dive regulator and pondering this patterns making them pop out from the reef. It began to form 12 to 18 million years JUSTIN MARSHALL BARBARA BURGER JUSTIN MARSHALL

54 Scientific American Presents Why Are Reef Fish So Colorful? COPYRIGHT 1998 SCIENTIFIC AMERICAN, INC. Compared with some species of fish and FISH EYE of this beaked leatherjacket sees other creatures, humans are relatively color- the light spectrum in a slightly different way blind. People have three color receptors in than a human eye does. their eyes: the blue-, green- and red-sensi- tive cones. Some reef fish (and indeed am- 57] and the school of kyphosids I saw in the phibians, reptiles, birds and insects) possess Heron Island lagoon. But to attract a mate, four or more. The record is currently held chase rivals away or provide other warn- by the mantis (a stomatopod), a reef BY JUSTIN MARSHALL PHOTOGRAPHS ings, bright colors that are easily seen un- dweller whose eyes have 12 color recep- derwater may be the of the day. In tors. With these additional receptors, the the blue waters of the reef, the colors yel- can see the region of the near ul- low and blue travel the farthest, so many traviolet, with wavelengths between about reef animals have evolved bodily patterns 350 and 400 nanometers (humans cannot of yellow and blue in striped or spotted see wavelengths shorter than about 380 combinations. Because yellow and blue nanometers). Also, they can see in greater ago and in some places is only two million are also widely separated in the spectrum, detail some of the colors humans see. years old; reefs of the western Atlantic and they offer strong contrast underwater. Such impressive visual capabilities might central Pacific formed 25 million years ago. Just what does a butterfly fish look like to seem to be unnecessary on the reef, where The diversity of colored fish and inverte- another butterfly fish? How does a drum- so many creatures have evolved bold pat- brates on the Great Barrier Reef is truly mer appear to a shark? It is this goal to un- terns that emit strong visual signals. Alterna- awe-inspiring. Yet the color patterns exhib- derstand color vision and its evolution tively, it may seem incredible that these ited by these inhabitants did not evolve for from the point of view of the animals them- brightly colored fish manage to survive human eyes. The brilliant blue spots of the selves that my colleagues and I at the Uni- with markings so striking that they would semicircle angelfish, or the contrasting yel- versity of Queensland’s Vision, Touch and seem to attract the attention of even weak- low and blue fins of the yellowtail coris Hearing Research Center are striving to- eyed predators. [see illustrations at top of pages 56 and ward at present. Our research has revolved Could it be that coral reefs are colorful, 57], are a vital component of the survival around three critical questions: One, what and therefore that colorful animals fit in and strategies of these species on the reef. are the animals’ visual capabilities? To ex- may even be camouflaged? Logical though To understand this role of color and ap- plore this matter, we are carrying out ex- it may seem, the notion does not hold up pearance requires some understanding of periments in which we are quantifying to scrutiny. A reef stripped of its fish and survival on the reef and also of the optics of colors nonsubjectively, using the world’s other mobile life-forms is actually relative- the undersea realm. At its most fundamental first underwater spot-reflectance spectro- ly monochromatic. Most of the corals are level, survival for any species de- radiometer. Two, what are the light and brown or green, their colorful splendor mands three things: eating, not being eaten surroundings like in the where these coming out only at night when the polyps and reproducing. Unfortunately for sea creatures live? Experienced divers know open or under the falsely bright illumina- creatures, the demands on appearance im- that seawater is so blue that all red light is tion of the camera strobe or video light. posed by the first two of these survival re- absorbed within 20 meters of the surface; a Another possible explanation revolves quirements conflict with those of the third. bright-red fish at this depth therefore ap- around disruptive coloration, a principle A good way to avoid being eaten, or, in- pears black. And three, under what cir- first described in detail in the 1940s and deed, to lurk undetected while waiting for cumstances, and to what other creatures, subsequently used for military camouflage. prey to swim by, is to be camouflaged to do fish show off their color patterns? The central idea is the use of large, bold pat- match the background (the scientific term Clearly, displaying bright colors to impress terns of contrasting colors that make an is “cryptic”). Masters of camouflage include a potential mate would be unwise when object blend in when viewed against an the frogfish [see illustration at bottom of page visually guided predators are lurking nearby. equally variable, contrasting background.

STRIKINGLY PATTERNED REEF FISH include (from far left) the thread- whose vertical stripes make it difficult to discern head from tail. Bright fin butterfly fish, which has a “false eye” above the caudal fin to con- patterns also appear on the dorsal fin of the yellowtail coris wrasse fuse predators; the humphead Maori wrasse; and the , (below left) and on the anal fin of the regal angelfish (below).

Why Are Reef Fish So Colorful? The 55 COPYRIGHT 1998 SCIENTIFIC AMERICAN, INC. FISH COLORS include vivid patterns, as seen above (from left to right): the midbody of a The light and dark branches, pockets and beaked leatherjacket; nose of a surf parrot fish; tail of a yellowtail coris wrasse; dorsal fin of a shafts of light on a reef provide just such a regal angelfish; midbody of a royal dottyback; fin of a regal angelfish; cheek of a harlequin background. tuskfish; dorsal fin of a harlequin tuskfish; tail of a semicircle angelfish; and another fin of a Good examples of disruptive camou- regal angelfish. Blues and yellows, which travel far underwater, are common. flage on land are the striking patterns of some snakes or the stripes of a zebra. These colorations, when viewed against the kinds are easily mistaken for eyes [see illustration on critical here; frontal regions are obscured of highly patterned backgrounds common page 54]. In patterns on other fish species, when the fish is seen from the side, in the animals’ natural , aid camou- blocks of blue match the blue of the ocean. whereas the erect-fin displayers such as the flage or at least make it difficult to see The effectiveness of highly contrasting butterfly fish will intentionally turn side- where the animal begins and ends. For ex- body stripes, spots and blotches as a means ways to present a broadside of color to a ample, zebras—like many boldly colored of reef camouflage can be fully appreciated rival or mate. fish—group together for protection. In only under natural illumination. Yet few Bright colors can also warn of toxicity. these groupings, the context against which people get to see fish this way: often reef Boxfish, blue-ringed [see illus- predators see individual patterns and colors creatures are viewed in photographs, their tration at right] and nudibranchs are all is not, typically, a natural background but colors set ablaze by the flash of a strobe known for such aposematic displays, in rather the school or herd itself, enabling and against a background that is nothing which, again, yellow and blue are a com- one animal to become lost in the swirling more than a featureless, dark field. Lit up in mon theme underwater. In contrast to mass of its neighbors. this manner, the fish are being seen as they the furtive behavior of animals that are Complicating matters is the fact that are when they are “displaying.” disruptively camou- most reef fish are capable of changing col- Fish sometimes position them- flaged by their bright ors to some degree. Some, notably the selves in shafts of sunlight to re- patterns, however, triggerfish and goatfish, can do so at nearly veal the full splendor of their col- aposematic displays the speed and complexity of chameleons. ors to a rival or potential mate. At are generally accom- In other fish, color changes may take sev- other times, even the multicol- eral seconds, may be associated with night ored harlequin tuskfish or irides- and day, or may occur during maturation. cent blue angelfish disappear under Parrot fish change color in association with the dim, highly textured illumi- a sex change, a drab female in a harem nation of the coral ledges where changing into a gaudy dominant male if they spend much of their time. the resident male is lost. Changes are also Also, just as birds will puff out known to occur with “mood”— for ex- and spread their feathers in dramat- ample, during conflicts or flight from a ic displays, some reef fish will erect predator. Although one can guess at the highly colored fins or reveal bright causes behind these and other color chang- patterns on frontal head areas or es, at present almost no convincing hy- even inside the mouth. The positioning of potheses explain their function. the fish relative to the viewer is obviously Parts of fish may be disguised by a pat- tern, such as the dark stripes that run near the eyes of the Moorish idol [see illustration REGAL ANGELFISH is one of a number of on page 54]. Similarly, colorations may reef creatures having body stripes that reflect make it difficult for a predator to deter- near-ultraviolet light (large photograph). To a mine which end is the head and which is fish whose eyes are sensitive to this higher- the tail. Many species of butterfly fish, for frequency band, the stripes that to human example, have a black dot on either side eyes seem a pale bluish-white (inset) proba-

of the body near the caudal fin; these dots bly have some particular significance. JUSTIN MARSHALL

56 Scientific American Presents Why Are Reef Fish So Colorful? COPYRIGHT 1998 SCIENTIFIC AMERICAN, INC. tary, with each color having a spec- sibly “secret waveband” remains a mystery, ) tral peak that fits neatly into the ultraviolet is in theory a good color for lo- trough of the adjacent color. Three cal signaling. The fact that ultraviolet is

years ago we began to suspect that highly scattered and attenuated by water gallery of fish colors some of these exquisitely tuned means, for example, that the visual signals combinations, not obviously con- of a sexual display could be sent to a nearby trasting to us because of the rela- potential mate—and that the signal would tively limited color perception of degrade to invisibility over the longer dis- ); JUSTIN MARSHALL ( humans, provide particularly strong tances at which predators might lurk. visual signals to certain fish species. There are many related issues about (

As noted, color vision in some which we know little. For instance, color Inc. ld, reef fish and other animals may be vision changes substantially during the life

based on four photoreceptor types spans of reef fish. For example, it appears Peter Arno rather than three, as in humans. Be- that the eyes of reef fish larvae do not block BLUE-RINGED OCTOPUS’S brilliant coloration warns cause the additional sensitivity af- ultraviolet, and yet most of the adults of forded by the extra photoreceptor is these species cannot see this part of the of toxicity. The bite of the Australian reef creature con- FRED BAVENDAM often in the ultraviolet, we became spectrum. We know that the change is to tains a poison that induces muscular weakness and, in interested in the possibility that the accommodate the demands of a new the worst cases, respiratory paralysis. visual signals sent by a select number mode of life—the emergence from the of reef fish encompass the ultraviolet , where all fish begin life. So far, panied by bold and indiscreet behavior. As as well as the colors visible to humans. however, the details of this vision change an interesting side note, evolution has pro- Using our spot-reflectance spectroradio- are known for only two of the 1,500 spe- duced aposematic animals unable to see meter, we found this indeed to be the case. cies on the Great Barrier Reef. their own beautiful colors. This is the case The advantage of this device is that it can This is just one of the mysteries that for nudibranchs and for the blue-ringed “see” colors we cannot, including both the leave vast gaps in our knowledge. We still octopus. Both these lack the near-ultraviolet and the near-infrared re- have only fragmentary ideas about what retinal features necessary to see colors, in- gions of the electromagnetic spectrum the colors of a reef mean to its inhabitants, dicating that their bright patterns evolved (with wavelengths of 300 to 400 nano- making each visit to this world of secret solely in response to their predators’ meters and 700 to 800 nanometers, re- color communication an endeavor as tan- much more capable visual systems. spectively). As a result, we can begin to talizing as it is beautiful. Whether for display or camouflage, the understand how color patterns have visual signals emanating from reef fish all evolved for animals that see these colors. JUSTIN MARSHALL is a research fel- depend strongly on contrast, and this aspect Our work has involved trying to establish low in the Vision, Touch and Hearing Re- appears to have evolved with unexpected what the various reef fish can see. Our search Center at the University of Queensland elegance. As noted earlier, yellow and blue most recent results indicate that in adult in Brisbane, Australia. are an effective combination, with peaks life, a relatively small proportion of reef fish in different parts of the spectrum. The two see the near ultraviolet. As with apose- colors are said to be complementary—ex- matic coloration, however, it is becoming hibiting a high degree of contrast—because clear that animal colors are not necessarily of this spacing of their spectral peaks. correlated with their own visual systems. The spectral characteristics of the colors Although the exact function of this pos- of several other reef fish are even more complex, with three rather than two peaks. Where this is the case—in the facial dis- FROGFISH is shown in “cryptic” mode, plays of and parrot fish, for exam- matching its background as it waits to

ple—adjacent colors are also complemen- pounce on unsuspecting prey. JUSTIN MARSHALL

Why Are Reef Fish So Colorful? The Oceans 57 COPYRIGHT 1998 SCIENTIFIC AMERICAN, INC.