The Secret to the Sea Hare's Sticky Defense

Don't underestimate the sea hare. It might be soft, slow, and limbless, but it makes up for all that with an arsenal of antipredatory defenses. Now, scientists have figured out how one of these defenses — a sticky, milky-white substance called opaline — deters hungry spiny lobsters. Opaline works via sensory inactivation, blocking the lobsters' sense of smell.Sea hares (genus Aplysia) are soft-bodied marine mollusks, closely related to sea slugs and nudibranchs. They get their common name from a pair of large sensory rhinophores, chemical receptors that project from atop their heads like bunny ears.Because they lack a protective outer shell, sea hares are equipped with a diverse array of antipredatory defenses, including cryptic coloring and shape and a coating of toxic mucus. When attacked by a predator or manhandled by scientists, sea hares can also release a mixture of secretions from ink and opaline glands (see video at end of post). The two glands are under separate neural control and can release their secretions independently or together. Most sea hare ink is a deep purple due to pigments found in their diet of red algae. Opaline is a clear-to white liquid that becomes viscous upon contact with water, and its production and color do not depend on the sea hare's diet.Charles Derby, a biologist at Georgia State University, has studied what makes this ink mixture so effective against predators for nearly a decade. He and his colleagues previously discovered that spiny lobsters (Panulirus interruptus) actually find the ink secretion attractive. High levels of amino acids in the ink mimic the stimulatory properties of food, so when the lobsters encounter the secretion, they drop the sea hare and instead try to eat the ink. The ink acts as a "phagomimetic decoy," distracting the lobsters and allowing the sea hares to make a getaway.However, Derby and his colleagues weren't sure how opaline fit into the picture. During these experiments, they noticed the spiny lobsters grooming their antennules (the first pair of antennae that act as their nose) when they came into contact with the opaline secretion. This suggested that it could be affecting the lobsters' ability to taste and smell. But how? Opaline could contain chemicals that interfere with the lobster's sensory system, or the sticky nature of the secretion could be gunking up the lobster's receptors, giving it the equivalent of a stuffy nose. So Derby, with Tiffany Love-Chezem and Juan Aggio, decided to separate opaline's stickiness and its chemicals and test their effects independently on spiny lobsters.First, the researchers extracted the water-soluble portion of the sea hare's opaline. The resulting substance had the stickiness and other physical properties of opaline, but lacked the amino acids and other chemical attractants. Then they painted the substance onto spiny lobsters' antennules and presented them with delicious (to spiny lobsters, anyway) shrimp juice. Unlike the control lobsters with clean antennules, the lobsters with opaline-coated antennules didn't respond to the smell of food right in front of them, and the electrical activity in their chemosensory and motor neurons was significantly reduced.Next, the researchers tested a mixture of the most prominent amino acids found in opaline. This time, the lobsters' neurons fired away in response to the shrimp juice. When the amino acid solution was mixed with a chemical called carboxymethylcellulose, which mimics the physical properties of opaline, neuronal firing was again inhibited. The final test, a coating of carboxymethylcellulose alone, also stopped the neurons from firing.The scientists concluded that it's opaline's stickiness, rather than its component chemicals, that is responsible for blocking the lobsters' sense of smell. Derby and his colleagues  say the experiments “provide strong support that the sensory inactivation is principally due to the secretion physically covering the antennule and thus blocking chemicals from accessing chemosensory neurons.” They suggest that with their sense of smell plugged up, the lobsters might lose their appetite or become disoriented. As they attempt to clean their antennules of the gooey coating, the sea hare makes its escape.Video. Attack on Sea Hare by Spiny Lobster Results in the Chemosensory Organs of Spiny Lobster Becoming Coated with Sticky Ink Secretion.  The attack on a sea hare by a spiny lobster (at 5 s) causes release of the whitish opaline (at 16 s), followed the co-release of both opaline and ink (at 21 s). The subsequent close-up view of the antennules (from 31 s until the end of the video) shows the olfactory organs of the spiny lobster coated with secretion. (Courtesy of Paul M. Johnson).[youtube]http://www.youtube.com/watch?v=zvzE9NgKEvc[/youtube] References:Derby, C.D. 2007. Escape by inking and secreting: marine molluscs avoid predators through a rich array of chemicals and mechanisms. Biol Bull. Dec; 213(3):274-89.Kicklighter, C., Shabani, S., Johnson, P., and Derby, C. 2005. Sea Hares Use Novel Antipredatory Chemical Defenses. Curr. Biol. 15(6):549-554 DOI: 10.1016/j.cub.2005.01.057Love-Chezem, T., Aggio, J. F. and Derby, C. D. 2013. Defense through sensory inactivation: sea hare ink reduces sensory and motor responses of spiny lobsters to food odors. J. Exp. Biol. 216(8):1364-1372. DOI: 10.1242/jeb.081828