Pufferfish are the only bony fish that can close their eyes, and now we know how they do it. They sink their eyeballs deep into their sockets and then pucker the skin surrounding the eye together, like a camera’s aperture closing.

Also known as blowfish, pufferfish produce a blink-like response when researchers direct gentle jets of water towards their eyes. But instead of relying on eyelids that slide vertically or horizontally – blinking as we know it – their eyes close in a circular way towards the centre, says Keisuke Ogimoto at the Shimonoseki Marine Science Museum in Japan.

The findings resolve “a great mystery hidden in the long-known behaviour of [these] familiar fish”, he says.

The pufferfish’s eye-closing ability is something that Japanese fishermen and chefs have long noticed when catching or preparing the fish for gourmet dishes, which are popular among diners despite the risk of toxicity.

But scientists had never followed up on these industry-level observations, until Ogimoto witnessed the behaviour with his own eyes – and fell in love with it.

“The first time I saw a pufferfish close its eyes in my aquarium, I was so moved by its cuteness that I decided to investigate,” he says.

Read more: Zoologger: The most kick-ass fish in the sea

Ogimoto and his fellow researchers at both the Shimonoseki Marine Science Museum and the Okinawa Churashima Research Centre, Japan, studied two fine-patterned puffers (Takifugu flavipterus) living in an aquarium at the Shimonoseki museum.

The team took video and still images of the fish’s eyes as handlers gently squirted warm seawater into them, and collected ultrasound recordings of eyeball movement. The researchers also dissected and ran experiments on the eyes of two other fine-patterned puffers that had died of natural causes.

They found that the skin around the fish’s eye squeezes over the middle of the eyeball with a sphincter-like movement, resembling an iris constricting over a pupil in bright light. Just before the skin moves, the eyeball sinks into the head to a depth of 70 per cent of the eye’s full diameter – among the greatest eye-sinking depths ever recorded in an animal.

While examining the dead fish, the researchers found a sheet of muscle underlying the skin around the eye that contracts in response to an electric shock in a way that is surprisingly similar to mammalian eyelid mechanisms, says Ogimoto.

“The various aspects of this eye-closing behaviour were revealed one after another, and it was a continuous surprise,” he says. “It’s exciting to ponder the mystery of the evolution of this similar-but-different eye-closing behaviour.”

Some sharks, which are fish with a cartilage skeleton instead of bones, can close their eyes with a single eyelid that moves over the eye. The manatee, a marine mammal, also closes its eyes radially like the pufferfish. But because the pufferfish and the manatee are related only very distantly, the scientists believe the animals evolved the trait independently of each other.

Journal reference: Zoology, DOI: 10.1016/j.zool.2021.125894