Beneficial self-harming: Sea slugs protect themselves by self-cutting

Unbeknownst to the sea slug, a crab approaches and reaches out a wicked claw to grab one of the many plate-like appendages running along the slug's back. A snap of a claw and the plate comes free -- not torn away by the crab, but rather cut free by the sea slug itself, as it swims away completely unscathed.

This is a scenario studied by University of Victoria developmental biologist Louise Page, who has been fascinated by this process of self-cutting, or autotomy, in the hooded sea slug ever since she was a master's student. A colleague was culturing these odd creatures at the University of Washington's Friday Harbor Marine Laboratory, and Page was so taken with their unique anatomy and behaviors, studying them became a focus of her career.

"It's a remarkable animal, I'm happy to ride on its coattails," she enthuses.

Melibe leonina is a species of nudibranch, a marine snail that has no shell. Nudibranchs come in many shapes, sizes and colors, but Melibe (pronounced "mel-uh-bee") stands out due to its large oral hood, which resembles a translucent sea anemone, and the large, paddle-shaped appendages on its back. Many nudibranchs have these back appendages, known as 'cerata' (singular = 'ceras'). For most nudibranchs, cerata are long and slender, but those of Melibe are different, resembling the broad back plates of a stegosaurus.

But perhaps most unique is what Melibe does with these appendages. "When they are handled roughly or pinched, the tissue at the base of the cerata seems to melt away, and they just pop off," Page says.

She thinks that this self-cutting behavior is a defensive mechanism for escaping predators, similar to how some lizards and amphibians shed their tails when caught.

"I've often wondered if the cerata may be acting as a decoy, to attract the first attack from a fish or a crab, to deflect it away from the hood, because the oral hood is so vulnerable," she says.

"Autotomy is a voluntary loss of an appendage, and animals must also have a way to seal off the wound so they don't bleed to death," she explains. Page has devoted a great deal of research to solving this physiological puzzle.

She began by taking an in-depth look at the area at the base of the ceras, known as the autotomy plane. She discovered several special structures there, including two muscular sphincters, a set of longitudinal muscles, and special granule-filled cells that are directly connected to nerves. These cells are found nowhere else in the animal.

"It looks suspiciously like these cells may be involved in releasing something that is breaking down connective tissue," Page muses. This would make the tissue at the base of the ceras much easier to pull apart.

She studied the nerve signals involved in initiating autotomy, and came up with a model of the sequence of events involved in the process. Her hypothesis: during autotomy, the longitudinal muscles contract strongly and put tension on the autotomy plane. The granulated material is released, breaking down connective tissues, and the sphincters contract to cut the ceras and close the wound.

Recently, Page and a team of undergraduate researchers have been pursuing new ideas to better understand autotomy in Melibe. The behavior is first exhibited in juveniles at a particular developmental stage, so she hypothesized that the structures most critical to this behavior must also first develop at that time.

They collected Melibe eggs from their natural habitat and hatched and cultured larvae in the laboratory. Once they reached the correct developmental stages, Page's team used special stains to identify nerves and muscle tissue in the autotomy plane. They discovered that while the granule-filled cells are already abundant before the stage where self-cutting is first exhibited, the sphincter muscles first differentiate at this stage. This suggests to Page that the sphincters are critical to the autotomy process.

Page intends to continue exploring the mechanism of autotomy in Melibe, and suggests it may have wider implications than just a better understanding of this charismatic animal.

"What Melibe has here is some mechanism to drastically reduce the tensile strength of connective tissues," she says, noting that dense connective tissues in scars can be a problem in wound healing.

"Maybe this could be a platform for research into things that have medical applications," she muses.

Page and her students presented their research at the 2016 annual meeting of the Society for Comparative and Integrative Biology in Portland, Oregon.