This fish has legs — and it uses them for more than just walking

“New things came from old parts,” says David Kingsley, a developmental biologist at Stanford University. A walking fish with taste organs on its limbs may look “really new and cool and different, but when you dig in… the new things have come by taking a tool kit of preexisting genes and deploying them in new ways.”

Northern sea robins (Prionotus carolinus) are skilled at finding buried crabs or shrimp to snag a meal. So skilled, in fact, that other fish seem to follow along to take advantage of any spoils. Previous studies suggested that northern sea robin legs could pick up chemical cues, but it was unclear if the limbs could sense anything as they dug into the seafloor.

Fish have taste buds in their mouths, and some fish even have taste buds on the outside of their bodies, says Peihua Jiang, a neurobiologist at the Monell Chemical Senses Center in Philadelphia who was not involved in the work. So while it doesn’t surprise him that northern sea robins have an exterior sense of taste, it’s “actually quite amazing” that their legs have become sensory organs, he says. “That’s completely a new feature [for fish], not what we typically see for how you detect or process taste information.”

It’s hard to define what taste is for many water-living creatures in part because some chemicals diffuse easily in water, but there are other aquatic animals that also use appendages to sense food, says Nicholas Bellono, a physiologist at Harvard University. Octopuses, for instance, use their arms to detect greasy molecules sticking to the shells of prey (SN: 4/18/23).

For both studies, Kingsley, Bellono and colleagues used a diverse mix of experiments to explore how northern sea robins excavate food. Behavioral tests showed that fish swimming in tanks home in on extract from store-bought mussels as they sift through sand with legs that end in a shovel-like structure. Close-up images revealed small sensory mounds called papillae that cover the legs, like the taste buds that cover tongues.

At first, the team wasn’t sure whether the papillae might be sensing chemicals in a manner like smelling or tasting, or whether the fish were doing something new, says Corey Allard, a biologist at Harvard University. “We found it’s a combination. [A sea robin leg] uses a lot of the same receptors that taste does, but repurposed and arranged in a way that’s very different” from the taste buds in the mouth.

Additional genetic and physiological experiments found that the papillae have touch-sensitive nerve cells and taste sensors that help these sea robins figure out where to dig. The researchers detected high levels of activity from a gene called t1r3 — which provides the instructions to make a receptor found in mammalian sweet-detecting taste buds — at the tips of each leg. What’s more, an ancient gene called tbx3a that drives limb development in many animals, including people and chickens, was crucial for not only sea robin leg formation but also in forming the papillae and driving the digging behavior.

Most sea robins, including a non-digging species called the striped sea robin (P. evolans), have smooth, rod-shaped legs that probably can’t taste, the team discovered. That difference suggests that northern sea robins and another digging relative, the leopard sea robin (P. scitulus), are among a few species benefitting from an “evolutionary innovation,” says Amy Herbert, a developmental biologist at Stanford University.

Though the legs aren’t technically legs, Herbert notes. While the fishes do use the appendages for moving around — which prompted the team to call them legs — their position on a sea robin’s body is more akin to using arms to walk.

Whether arms or legs, Jiang wonders whether the limbs’ papillae can sense bitter compounds that don’t signal food but instead tell sea robins when they’ve found something that they want to avoid. He also wants to know if the taste buds in sea robin mouths detect the same tastes that their legs do. “Once they actually find food, what’s the next step?”