Multi-component chemical defense in seahares (Gastropoda:Opisthobranchia): antipredator compounds act as both honest and deceptive signals to multiple predator species

Thesis (Ph. D.)--University of Washington, 2002Many organisms produce chemical defenses to deter predation, yet the behavioral, neurophysiological, and cellular mechanisms of chemical defenses are largely unexplored. Animals do not face a single hypothetical predator, but rather a diversity of predators whose behaviors and sensory systems can be highly divergent. Do prey chemical defenses function differently versus different predator species? Can chemical defenses be honest signals to some species and deceitful to others? These issues were examined using seahares (Aplysia spp. and Stylocheilus spp.) and their cnidarian, crustacean, and vertebrate predators. Seahares release defensive secretions called ink and opaline from independent glands. In behavioral assays, seahares with full glands versus those with depleted glands had a significant survival advantage against sea anemones, crabs, and lobsters, but not against fishes. Isolated secretions and their components were used to explore mechanisms of defense against sea anemones and lobsters. A 60 kDa glycoprotein from ink was isolated, cloned, sequenced, and expressed. This protein ("escapin") was responsible for the aversive reaction of sea anemones to ink via lysis of anemone cells. It also had antibacterial effects against Gram positive and negative bacteria. Escapin is the first reported antipredator protein of any organism.Ink and opaline protected seahares against crustaceans in a different and unusual way---by stimulating them to feed. Opaline was as stimulatory as homogenates of squid and shrimp in behavioral studies and electrophysiological assays of chemosensory neurons of lobsters. The attractiveness of opaline and ink is likely due to extremely high levels of free amino acids. In particular the highly stimulatory amino acid, taurine, is three orders of magnitude more concentrated in opaline than seahare haemolymph. These secretions are a supernormal feeding stimulus that can act as a sensory trap, exploiting the chemosensory systems of crustaceans. Via this novel chemical defense "phagomimicry", crustaceans are deceived into attending to a false food stimulus from the secretions while dropping the seahare and thereby incurring a nutritional cost. Thus chemical defenses can function differently versus different predator species, acting as honest signals (as escapin does to sea anemones) to some and deceitful signals (as phagomimicry does to crustaceans) to others