The gooey ink secretions of sea hares do more than just repel or distract their predators; scientists have discovered that this sticky substance can also mask their senses of smell and taste.

Sea hares (genus Aplysia) are large, herbivorous mollusks that are closely related to sea slugs and nudibranchs. The largest sea hare, Aplysia vaccaria, can grow up to 75 cm long and 2 kg in weight. Sea hares have a great sense of smell thanks to a pair of large sensory rhinophores that sit erect on their heads like bunny ears. Their colouring, ranging from light grey, green and red to dark purple with white spots, helps them to camouflage, as it is determined by the colour of the seaweed they eat and live nearby.

Because they don't have a protective shell, sea hares have equipped with a whole bunch of defence mechanisms to keep predators away from their soft flesh, which contains toxins as a last resort. They have two defensive glands in their mantle cavity; the ink gland sits on the roof of the cavity above the gill and produces a purple ink, and the opaline gland, which is located on the floor of the cavity under the gill, produces a milky white, viscous secretion called opaline. If a sea hare is threatened or attacked, a siphon inside its mantle cavity will pump one or both of these secretions out into the surrounding water. Research has shown that these secretions can act as a decoy in response to predators such as sea anemones, crustaceans and fish, leading them to misdirect their attacks. It also commonly works as a repellent, prompting tentacle shrivelling in predatory sea anemones.

Because it is so well defended, the sea hare doesn't have a lot of predators to worry about, but California spiny lobsters, (Panulirus interruptus) are known to take their chances on them occasionally. So in 2005, Charles Derby and Cynthia Kicklighter from the Neuroscience Institute and Department of Biology at Georgia State University in the US decided to use the spiny lobster to test the effects of the sea hare's ink secretions. They found that the high levels of amino acids in the ink secretion mimicked the stimulatory properties of food, so when the lobsters came in contact with the secretion, they would leave the sea hare alone and try to eat the ink instead. The spiny lobsters would start "digging with the legs into the substrate covered by the secretion ("digging") and moving the first two pairs of legs to the mouth (“grabbing”), behaviours similar to that produced when spiny lobsters are chemically stimulated to search for and sample food items", the team reported in a 2005 issue of Current Biology (PDF). This form of chemical defence, which has a similar result to a lizard discarding its tail to distract a predator, is known as 'phagomimicry'. The team concluded that, "The detection of high concentrations of free amino acids typically signals to spiny lobsters the presence of food. Sea hares exploit this property of their predator’s nervous system by releasing secretions that mimic stimulatory properties of food and thereby divert the attention of the attacker. The highly viscous nature of opaline may create a tactile sensation of food, contributing to the mimicry."

During this experiment, Derby and colleagues noticed that the spiny lobsters would also habitually groom their antennules (small antennae that act as the 'nose') and mouthparts when they came into contact with the opaline secretion, which suggested that it could be hindering their ability to taste and smell. So more recently, Derby joined Tiffany Love-Chezem and Juan Aggio from Georgia State to test if it was the chemical composition or the stickiness of the opaline secretion that was achieving this effect.

First they extracted the water-soluble fraction of the opaline, which leaves behind the amino acids and other chemical attractants but keeps the stickiness, and painted it onto the tips of the spiny lobsters' antennules. The lobsters were then offered delicious smelling 'shrimp juice' and the researchers measured the electrical activity in both their chemosensory (odour detection) and motor neurons. Reporting in Experimental Biology this week, the researchers reveal that unlike the control lobsters that had clean antennules and hence no problem sniffing out the shrimp juice, the lobsters with opaline solution on their antennules failed to get excited by food right in front of them, their chemosensory and motor neurons have been significantly reduced.

But when the researchers applied a solution of amino acids found in opaline to see if its chemical composition affected the neuronal activity of the lobsters, they found that the lobsters reacted normally to the shrimp juice. This means that the thick, sticky texture of the opaline is the key to physically blocking the ability of the sea hare's predator to identify it as food. "Our 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," the researchers conclude. "Our experiments do not provide evidence for the chemical properties of opaline, either excitatory or suppressive, contributing to the inactivating effect, but experimental design issues allow that there might be some chemical effect that we could not resolve."

The researchers compare this newly discovered mechanism with a defensive behaviour found in some species of moths, whose ultrasonic emissions can 'jam' the echolocation of predatory bats, thereby masking the moth's whereabouts. However, the say that this is the first time that an organism has been proven to inactivate the senses of its predators through a chemical mechanism.

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Papers cited:

Kicklighter, C., & Derby, C. (2006). Multiple components in ink of the sea hare Aplysia californica are aversive to the sea anemone Anthopleura sola Journal of Experimental Marine Biology and Ecology, 334 (2), 256-268 DOI: 10.1016/j.jembe.2006.02.002

Kicklighter, C., Shabani, S., Johnson, P., & Derby, C. (2005). Sea Hares Use Novel Antipredatory Chemical Defenses Current Biology, 15 (6), 549-554 DOI: 10.1016/j.cub.2005.01.057

Love-Chezem, T., Aggio, J., & Derby, C. (2013). Defense through sensory inactivation: sea hare ink reduces sensory and motor responses of spiny lobsters to food odors Journal of Experimental Biology, 216 (8), 1364-1372 DOI: 10.1242/jeb.081828


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