Eyes can be beautiful. Mysterious. Alluring. They can also be deceptive, no more so than in the animal kingdom, where a range of species display fake eyes on their bodies.

Such eyespots, which appear on fish, frogs, butterflies and birds and insects among others, have fascinated natural historians for centuries, and a fresh look at the science of eyespots reveals some modern surprises.

A caterpillar with a snake’s stare

Though it’s clear that eyespots often deter predators, it is not so obvious why, and why different designs have evolved.

For a start it remains unclear to what degree eyespots actually mimic real eyes, and whether other animals see eyespots in the same way as humans do.

Plenty of species appear to use eyespots as a warning signal to predators, helping to deter, prevent or delay their attacks. That could be due to the unfamiliarity of the shape to predators, or because eyespots fool predators into thinking they are staring at the face of an even bigger, more dangerous creature than themselves.

But few had checked rigorously - unbiased by our own human perception of these markings as “eyes” - until Dr John Skelhorn at Newcastle University, UK examined how birds responded to a series of fake caterpillars with snake’s eyes.

Lots of caterpillar species sport eyespots, so Dr Skelhorn’s team created plump, realistic caterpillars from edible pastry, then painted them with eyespots on different parts of their body. They reasoned that birds would reject caterpillars that sported eyespots at their fronts, where an eye would normally be, thinking the insect was actually a snake. But they wouldn’t be deterred by caterpillars with eyespots elsewhere.

Their research supported their hypothesis; birds were more reluctant to attack caterpillars that had eyespots in the right place to mimic a snake’s head.

Butterflies that flutter their eyes

But other studies have shown the opposite; that butterflies use eyespots as conspicuous, disorientating patterns that put off predators, rather than to mimic the eyes of other animals.

Eyespots are also surprisingly common on butterfly wings, for example. Yet they vary in size and brightness, and it was unclear why.

To investigate, Dr Martin Stevens at the University of Exeter, UK examined how birds actually see butterflies, which they often like to eat.

Affixing fake butterflies to tree trunks, Stevens’ team presented wild woodland birds with spots of different shapes, sizes, and contrasts, in order to manipulate the level of eye-likeness. They predicted that if eye mimicry is important, birds should be more wary of spots with a black centre and white surround, compared with the inverse arrangement. They found that the two patterns were equally avoided.

Eyespots have attracted a substantial amount of experimental work but there’s still a great deal left to understand about them

Retaining the size of the colour pattern on the fake butterflies, they changed the shape from circular to rectangular, and again didn't find any difference in birds’ avoidance. Contrast did matter though. When test patterns had higher contrast against the background, those areas of the fake wing were more likely to be avoided.

The results suggest that it is conspicuousness, not necessarily eye mimicry, that matters.

“We don’t have the complete picture yet,” says Stevens.

His experiments were with fake, stationary butterflies, and the spots and contrast patterns were continuously visible. In nature, butterflies and moths often flash open their wings to reveal their eyespots, “and no one has done an experiment yet doing these kind of manipulations with a startle display,” he says. But his work thus far suggests that birds will avoid conspicuous patterns when they are bigger and more contrasting, whereas shape doesn't seem to matter.

“Eyespots have attracted a substantial amount of experimental work but there’s still a great deal left to understand about them, and why they’re so diverse,” says Stevens.

The frog with a toxic look

As well as sporting large eyes, some animals can inflate their eyespots, in a bid to stare down, and intimidate their enemies.

One frog that inhabits the savannah of Brazil, called either Physalaemus nattereri or Eupemphix nattereri, has eye-like markings just above its hind legs. And they appear to come in useful when the frog is attacked by birds, or the fearsome giant water bug, an insect voracious enough it can eat adult amphibians.

When approached the frogs puff up their body and raise their hind quarters to flaunt their large, false ‘black eyes.’

But these false eyes are only part of the frog’s defence strategy. At the centre of each false eye is a black disc, which contains a gland that produces a toxin.

The chemical is so potent that a single gland can produce enough to kill 150 mice, and owls have been known to regurgitate whole frogs, such is the toxin’s power. So if the glare of the frog’s false eyes doesn’t put off a predator, their nasty taste might.

Fish that misdirect their enemies

New discoveries about why animals use eyespots aren’t just limited to those we can easily see. And they also suggest that eyespots might not always deter attacks, but intentionally misdirect them.

Fish have a profusion of eyespots, often at the opposite end from their real eyes.

Until recently, few studies had investigated why eyespots might be beneficial underwater. One idea is that they divert predator attacks – either completely, or by misdirecting the predator to a less vulnerable part of the prey’s body. Although proposed over a century ago, solid support for the idea is still scarce, and direct tests are scarcer still.

That momentary bamboozlement could give prey a brief but valuable fraction of time to escape the attack

In 2013, Dr Sami Merilaita of Åbo Akademi University in Turku, Finland tested the idea using stickleback fish, a visual predator.

They created fake prey, and painted on eyespots on one side of the prey's body, leaving the other unaffected, to see how the sticklebacks would react.

The fish attacked the fake eyes more often, the scientists found.

The researchers suspect that the eyespots pattern manipulates the predatory fish into attacking what it thinks is the prey’s head.

If eyespots are confused with the head region, the predator might expect the prey to escape in one direction, when in fact it quickly slips off via the other. That momentary bamboozlement could give prey “a brief but valuable fraction of time to escape the attack,” says Merilaita.

The peacock spider’s irresistible display

Eyespots aren’t always designed to avoid being eaten. Sometimes they are used for sex.

Spiders have eyes; and a lot of them. But one spider also has a series of fake eyes that adorn its abdomen. Much like the peacock bird that it’s named after, the male Australian peacock spider has bright eyespots that it uses to attract a mate.

But it does more than simply flash its eyespots in a bid to impress. Male peacock spiders create a mesmerising display that’s part hip-hop, part disco, replete with irresistible eyes, rhythmic leg movements and colourful costumes. Entomologist Jurgen Otto has captured this behaviour up close in a series of exquisite short films.

Males “raise their abdomen and display to the female in what we call a fan dance,” says Dr David E. Hill, editor of Peckhamia, a journal about jumping spiders, the group to which the peacock spider Maratus speciosus belongs.

People don't expect this kind of sophisticated communication in such small creatures

Despite being just 4mm long, male peacock spiders make a big impact.

During courtship, a male peacock spider unfurls brightly coloured flaps usually kept tucked away. They then wave this structure, which resembles a peacock’s fan, at a female. At the same time, they also wave pair of specially adorned legs.

Dr Madeline Girard at the University of California, Berkeley, US and colleagues there and at the University of New South Wales in Sydney, Australia, investigated this elaborate courtship by observing wild-caught spiders displaying in the lab.

Male peacock spiders spend up to 50 minutes courting females, unveiling a host of moves including the pedipalp flicker, Elvis-like abdomen bobbing, the 3rd leg wave, swaying like a metronome, fan-flapping, and the pre-mount display - a rehearsal for real sex. They also vibrate, using particular sequences the researchers dub ‘rumble-rumps’, ‘crunch-rolls’, and ‘grind-revs’.

“What amazes people is that they don't expect this kind of sophisticated communication in such small creatures,” says Hill.

The peacock’s seductive tail patches

We can’t mention the peacock spider without referencing the peacock itself, perhaps the most well-known animal to use eyespots. And like the peacock spider, the peacock also uses its fake eyes for sex.

“Peacocks are the poster boy of sexual selection,” says Dr Bob Montgomerie, professor of biology at Queen’s University in Kingston, Ontario, Canada.

With colleague Dr Roslyn Dakin, he investigated what it is about a peacock’s flashy tails that so fascinates females.

Peacocks have more than 150 feathers, each sporting an iridescent eye-like pattern towards the tip. Each eyespot has a dark purple–black centre, surrounded by concentric rings of blue-green and bronze-gold. Radiating out even further are narrow bands of green and purplish hues.

What produces the amazing colour, sheen, and iridescence of peacock feathers and their eyespots is not just the chemical properties of pigments, such as dark melanin. The physical structure of feathers, particularly at the nanoscale, refract light, producing deep greens and blues.

The researchers observed 34 displaying males. Determining each male’s mating success, they probed what aspects of eyes turned females on.

Peahens, they discovered, were partial to a particular portion of each eyespot - the blue-green patches that form the second ring out from the central purple black region. When males had up to 170 of their eyespots covered up by black or white stickers, their success with the peahens declined to almost zero.