On the face of it, what Nico Michiels did was rather pointless and a bit dangerous. Michiels, an evolutionary ecologist from the University of Tübingen in Germany, spends part of each year in Egypt where he dives in the Red Sea, observing life on its coral reefs. In September 2007 he decided to find out how far red light could penetrate the depths, so he attached a piece of red filter foil to his dive mask and began to descend. In theory, once he reached about 15 metres, he should have been plunged into darkness. Instead, something totally unexpected happened.

Like any experienced diver, Michiels knew that seawater selectively absorbs longer wavelengths of light so that somewhere below about 10 to 15 metres - depending on the clarity of the water - red light is all but extinguished, and anything that looks red at the surface fades to grey or black. His red filter would block out all wavelengths except red, revealing the depth at which red disappeared on this particular reef. Sure enough, 20 metres down it was as dark as night and quite disorienting. "All the fish disappeared. With no light from the surface they were effectively black and had become invisible," he says. But it didn't stay black for long. "Then I saw a group of gobies with bright red eyes lit up against the background. After that red spots began to show up all over the reef."

Through his red filter, the red flashes stood out in the gloom like glowing embers. Even without it, Michiels could pick them out without much trouble once his eyes grew accustomed to the gloom. Now, though, they were more orangey-red or brownish-red or purplish - a mix of wavelengths, but always including red. It seems strange that no one had spotted all this red before but as Michiels points out, no one saw it because no one expected to see it.

See the gobies under natural light and through the red filter

Image
© UnknownSeeing red on a Red Sea reef
"We knew we had something interesting," he says. For fish living in these waters, red should be irrelevant. Yet on that one dive Michiels discovered three fish species with prominent red markings, and he has found many others since. "Giving off red light is very strange for animals that aren't supposed to be able to see it. It would be odd if it had no function." If the fish could see what he was seeing, marine biologists might have to rethink their ideas about the colour red. Michiels now believes that many fish use red as part of a private system of communication that is proof against eavesdroppers.

But how can fish appear red where there's no red light? Ordinary red pigments look red because they reflect red light while absorbing all other wavelengths. At 20 metres down, there had to be some other explanation for the red Michiels was seeing. He suspected fluorescence. Fluorescent pigments behave differently from ordinary ones: incoming light of one wavelength excites fluorescent pigment molecules, causing them to emit light of a longer wavelength. On the reef during daytime, the most likely explanation was that the predominantly blue and green wavelengths at depth triggered the emission of fluorescent red.

With only a week left in Egypt, and lacking the equipment to confirm that the fish were fluorescent, Michiels observed and photographed as many of them as he could. Once back in Germany, he bought an assortment of tropical fish, including species he had seen in Egypt and some of their relatives he suspected might fluoresce, and installed them in his lab.

With the aid of colleagues from the university's chemistry department, armed with fluorescence microscopes, laser pointers and spectrometers, he confirmed that the fish did indeed fluoresce. Blue and green wavelengths both produced red fluorescence, with emissions mainly in the orangey part of the spectrum but extending well into the deep red region. In most of the fish they looked at, the fluorescence could be traced to specialised pigment cells called iridophores that lie in the skin beneath the scales. These cells contain guanine crystals, which scatter light to give fish their silvery sheen. However, Michiels says they are still not sure exactly what is fluorescing. "It's not the guanine crystals themselves. It's probably a fluorescent protein built into the crystals, and we have a suspicion that it might be made by bacteria and then harnessed by the fish." The only exceptions were two species of wrasse that glowed red all over. Their fluorescence is associated with the bony tissue of scales and fin rays, though again the exact source of the colour remains elusive.

Image
© UnknownWithout a light source, fin waving would be impossible for other fish to see
Intrigued by the existence of something that shouldn't be there, Michiels began a systematic search for red fluorescence in reef fish. He has been back to the Red Sea twice to hunt for more species, while his colleagues Nils Anthes and Dennis Sprenger searched around Lizard Island on the Great Barrier Reef. Between them they have identified some 50 species with pronounced red fluorescence, belonging to 24 genera and 12 families.

The most common markings tend to be towards the head and around the eyes. Some gobies have fluorescent anal fins while triplefin blennies have a red patch on their first dorsal fin. Most striking, perhaps, is the distinctive red tail fin sported by two species of pipefish, relatives of the seahorses. To Michiels, the distribution of these markings is one of the strongest indications that red fluorescence has a very specific function: communication with other members of the species (BMC Ecology, vol 8, p 16).

See a pipefish's distinctive markings

According to several recent studies, a whole range of animals, from birds and spiders to shrimp, employ fluorescence as a natural highlighter to boost the visibility of body parts they use in signalling, either to ward off enemies or to attract a mate (see "Day-glo animals"). In reef fish, the red tends to be confined to parts of the body used in signalling, suggesting that these markings serve a similar purpose. But instead of highlighting an existing colour, the fluorescence gives the fish a colour that otherwise wouldn't exist.

Triplefin blennies, for instance, flip their first dorsal fin back and forth when excited (see image). "You see something red going up and down rapidly," says Michiels. Pipefish wave their tail fins during courtship (see image). And fish commonly use eye rings to signal their presence and direction of gaze (see image). "Red-eyed gobies swim around in little swarms, and we think they use signals to indicate where they are and keep the swarm together."

Red light, whatever its source, doesn't travel far through water, which suggests these communications are intended to be private, seen only by nearby fish of the right species. There are several lines of evidence to support this, says Michiels. "Most of these fish are small and live at the bottom in pairs or groups. They are generally quite cryptic but often have conspicuous behaviours characteristic of the species. And there's obvious variation in markings between closely related species, which suggests they might be important in species recognition."

It all sounds very plausible. "The idea of red-light private communication channels is intriguing," says Julian Partridge, head of the Ecology of Vision group at the University of Bristol, UK. He says that if a fish can signal important things without being noticed, there can be big pay-offs. "Long-wave light doesn't travel far under water, so a male fish can wave its red sexy bits at a female and not be noticed by animals further away. Not only will that reduce his chances of being eaten while distracted with flirtation, but it will also make him less likely to be beaten up by a rival."

Michiels suspects that red fluorescence has another important role for some reef fish: helping them blend in with their background rather than making themselves seen. During his first dive with the red filter over his mask, he noticed that reef corals and algae glow a dark but faint red too, with brighter patches here and there. Against this irregular red background, a fish that glows red all over, like the small wrasse, would be hard to spot.

More compelling for Michiels is the case of the scorpionfish, a highly camouflaged ambush predator. The scorpionfish lies perfectly still until prey comes close and then sucks in the unwary animal in a split second. Michiels and his colleagues have found five species of scorpionfish that fluoresce red. "They have a faint glow all over the body with some bright patches here and there - very much like their background," says Michiels.

Yet if red plays any part in a fish's life then it must be able to see it - and that's where the jury is still out. Fish that live in a world dominated by blue-green light are assumed to have eyes tuned to those wavelengths, and most marine fish that have been studied are thought incapable of seeing red. One exception is the seahorse family, whose eyes are sensitive to red. That suggests pipefish can see red. As for the others, it remains to be seen. "As far as we know, none of the fish we found to fluoresce red has been investigated," says Michiels.

He has made a start. Preliminary studies of the visual pigments of the red-fluorescent goby Eviota pellucida show that there is considerable overlap between the wavelengths it can see and those it emits. "It's highly likely that this species can see its own fluorescence," says Michiels. He has also found that in the lab, red fluorescent fish respond to a dot of light from a red laser pointer, while non-fluorescent ones ignore it. "The fluorescent fish appear to chase the dot." Although that's only anecdotal, it does suggest they can see it.

"We still don't know for sure what exactly the fish see," Michiels admits. "If these fish do indeed see their own fluorescence, then in most cases we suspect they see it as enhanced contrast involving pink, red-brown or other red-containing colours in an otherwise blue-green environment."

See Eviota pellucida

Justin Marshall, head of the sensory neurobiology group at the University of Queensland in Brisbane, Australia, does not dismiss Michiels's idea but wants more evidence that the fish can see red and respond to it in a meaningful way before he is convinced. He believes the ultimate test is behavioural. "If they can show that female pipefish require a red fluorescent blob before a male pipefish takes any interest, or that males with normal tails are more successful than males with the red blob blanked out, that will be another tick in the box."

Michiels has already begun these experiments. He accepts that until he has shown that fluorescent fish see red and that it affects their behaviour, his thesis will remain unproven. Nevertheless, he believes his serendipitous discovery back in September 2007 should be a lesson to all who make assumptions about the natural world and the way other animals perceive it. "The fact that red fluorescence is there changes our thinking," he says.