Defense through sensory inactivation: sea hare ink reduces sensory and motor responses of spiny lobsters to food odors

Abstract

SUMMARYAntipredator defenses are ubiquitous and diverse. Ink secretion of sea hares (Aplysia) is an antipredator defense acting through the chemical senses of predators by different mechanisms. The most common mechanism is ink acting as an unpalatable repellent. Less common is ink secretion acting as a decoy (phagomimic) that misdirects predatorsʼ attacks. In this study, we tested another possible mechanism -sensory inactivation -in which ink inactivates the predatorʼs reception of food odors associated with would-be prey. We tested this hypothesis using spiny lobsters, Panulirus argus, as model predators. Ink secretion is composed of two glandular products, one being opaline, a viscous substance containing concentrations of hundreds of millimolar of total free amino acids. Opaline sticks to antennules, mouthparts and other chemosensory appendages of lobsters, physically blocking access of food odors to the predatorʼs chemosensors, or over-stimulating (short term) and adapting (long term) the chemosensors. We tested the sensory inactivation hypotheses by treating the antennules with opaline and mimics of its physical and/or chemical properties. We compared the effects of these treatments on responses to a food odor for chemoreceptor neurons in isolated antennules, as a measure of effect on chemosensory input, and for antennular motor responses of intact lobsters, as a measure of effect on chemically driven motor behavior. Our results indicate that opaline reduces the output of chemosensors by physically blocking reception of and response to food odors, and this has an impact on motor responses of lobsters. This is the first experimental demonstration of inactivation of peripheral sensors as an antipredatory defense. Supplementary material available online at

Free Amino Acids Mediate Association Preferences in Fish

“…For example, the secretion of free amino acid-rich ink by sea hares (Aplysia spp.) can inactivate predators' reception of prey-related odours (Love-Chezem et al 2013), while chemo-orientation to free amino acids can be used by parasites to locate hosts (K€ orner & Haas 1998). Free amino acids released by individuals (for instance via skin mucus or urine) have also been widely postulated to underpin social interactions, especially in aquatic animals (Yambe et al 2006;Kicklighter et al 2011;Ward et al 2011;Kleinhappel et al 2014b); however, to our knowledge, there is no empirical evidence to support this suggestion.…”

“…can inactivate predators’ reception of prey‐related odours (Love‐Chezem et al. ), while chemo‐orientation to free amino acids can be used by parasites to locate hosts (Körner & Haas ). Free amino acids released by individuals (for instance via skin mucus or urine) have also been widely postulated to underpin social interactions, especially in aquatic animals (Yambe et al.…”

“…The chemoreception of free amino acids (i.e. amino acids that are not bound within proteins or peptides) is known to be used across species in a range of contexts, including during predator-prey (Ferrer & Zimmer 2007;Love-Chezem et al 2013) and hostparasite interactions (K€ orner & Haas 1998). For example, the secretion of free amino acid-rich ink by sea hares (Aplysia spp.)…”

Chemical Diversity and Biological Properties of Secondary Metabolites from Sea Hares of Aplysia Genus

“…The absence of a shell as physical protection is compensated by several behavioral, anatomical and physiological adaptations [ 13 , 14 ]. However, the effective defense mechanism displayed by these organisms is the chemical and behavioral one, releasing a purple ink and opaline when attacked by predators [ 13 , 15 , 16 ]. These secretions contain some bioactive molecules acting by different mechanisms, such as feed stimulants (e.g., taurine), feed deterrents, and aversive compounds [ 6 , 13 ].…”

Ink From Longfin Inshore Squid, Doryteuthis pealeii, as a Chemical and Visual Defense Against Two Predatory Fishes, Summer Flounder, Paralichthys dentatus, and Sea Catfish, Ariopsis felis

“…However, in the single test of this idea, using Caribbean reef squid and French grunts, no support was found (Wood et al, 2010). Some have proposed that cephalopod's mucousy ink may disrupt a predator's chemical senses (MacGinitie and MacGinitie, 1968;Fox, 1974;Kittredge et al, 1974;Prota et al, 1981;Moynihan and Rodaniche, 1982) in a way that may be similar to sensory inactivation by sea hares (Love-Chezem et al, 2013), but there is no published experimental evidence to support this claim.…”