When Robert Heathcote dips his head into the rivers of Trinidad, he’ll often see little black dots moving through the water, even when it’s murky. Those dots are the eyes of small, inch-long fish called guppies. And those guppies are angry.
Guppies are among the most popular aquarium fish in the world, but they originally hail from the Caribbean. In Trinidad, some populations live upstream of waterfalls, which separate them from predators. In these safe havens, guppies flourish in such numbers that they compete intensely for food. They’ll guard any fruit that drops from overhanging trees with a ferocity that belies their puny size. Tail smacks are common, as are biting and ramming.
“You’ll see these little angry fish swimming over food patches, attacking anything coming over them,” says Heathcote. “We study guppies because they’re the archetypal rubbish animal that gets eaten by everything else, so seeing them display aggressive behavior is really cool.”
Heathcote and his colleagues, led by Darren Croft from the University of Exeter, noticed that when the guppies get aggressive, their eyes go black. Specifically, their irises—the colored rings around their pupils—change from a silvery color to a jet black. The change is extremely fast. “Sometimes, I’ll be watching a fish and I’ll blink and it’s got a completely different eye color,” says Heathcote.
It’s not clear exactly how the guppies darken their eyes. There are cells in their irises that contain dark pigment; it’s likely that their nervous systems can issue commands that change the size of those cells.“We have embarrassingly little idea about the mechanism,” says Heathcote. But here’s a twist: Even though black is the rarer color, it’s the default one. When Heathcote anesthetizes guppies, their irises always go dark. It seems that they’re constantly suppressing that darkness, and then releasing it when it’s time for a fight.
Scientists first described the black eyes in the 1980s, and suggested that they were signals of dominance and aggression, like a gorilla beating its chest or a dog baring its teeth. Heathcote’s team certainly saw that black-eyed guppies were far more likely to perform aggressive behaviors than to receive them. But in those conflicts, eye color could be incidental. To truly see if black eyes are a signal, the team needed to do an experiment. Somehow, they had to manipulate the color of a fish’s eyes to see how other guppies would react.
“We thought about sticking contact lenses on them for probably more time than we’d like to admit,” says Heathcote. When that failed, they tried making animated guppies on an iPad. But tablets are tuned to human eyes, and since guppy eyes see the world very differently, the fish completely ignored their virtual avatars. Heathcote was lamenting this second failure in a pub, when his drinking companion and colleague Jolyon Troscianko, who studies animal camouflage, suggested making a robot.
The team pressed a dead fish into some resin, to make a silicone mold that could churn out model guppies. They then photographed live fish with black and silver eyes, recalibrated the images for guppy vision, and printed them onto sheets of clingfilm. They stretched the colored sheets over the silicone models, which they attached to a fishing line on a motor. And voila: a robo-guppy of bespoke eyes and size, which could be made to angrily thrash over a bit of food.
The team found that guppies were more likely to go for food that was guarded by a silver-eyed robot than an otherwise identical black-eyed one—but only if the robots were bigger than them. If the robots were smaller, the guppies were more likely to try and loot the black-eyed one’s hoard.
This confirms not only that the dark irises are signals of aggression—but that they’re honest signals. They say that a guppy is prepared to fight, but they also tell rivals that there’s something to fight for. If the signaler doesn’t have the buff to back up its bluff, it will pay the price. Or, in other words, “wimpy fish that act strong get beaten up,” says Elizabeth Tibbetts from the University of Michigan, who studies the evolution of social signals.
Many other fish can change the color of their eyes, including distant relatives of guppies like salmon and tilapia. In those cases, it’s the subordinates who have black irises, and the dominant individuals who go silver. Heathcote thinks that these changes might be more common and more important than previously thought. After all, “many animals, predators and prey, are so attuned to looking for eyes,” he says. So if a species wants to send a clear message, why not do it through what is already one of the most conspicuous billboards on their body? Some researchers have even suggested that the whites of human eyes are social signals too, allowing us to more easily work out what our peers are looking at.
And yet, beyond a handful of other studies involving jackdaws and sticklebacks, scientists have done surprisingly little work on the communicative potential of eye color. “If you look at coral-reef fish, many of them have brightly colored eyes. Why?” says Heathcote. “A lot of birds also seem to have these brightly colored eyes and no one knows why. Almost nothing has been done on this.”
That’s partly because, as Heathcote found, eye color is very hard to manipulate in experiments. But perhaps it’s also because eyes, despite being the focus of animals’ attention, are less flashy or impressive than antlers, wings, or tails. “Eye color is one of those traits that's easy for us to ignore because it isn’t as dramatic as huge sexual ornaments,” says Tibbetts. “There is a whole world of animal social signals that humans overlook.”