The purple pigment aplysioviolin in sea hare ink deters predatory blue crabs through their chemical senses
ABSTRACT Sea hares release an ink secretion composed of purple ink and white opaline as a potential chemical defence against predators. The aim of our study was to identify deterrent molecules in the ink of Aplysia californica against an allopatric generalist crustacean predator, the blue crab Callinectes sapidus, and to define the mechanisms of action of the deterrents against crabs. We used two behavioural assays, a squirting assay and an ingestion assay, to show that ink is highly effective and that opaline is moderately effective in suppressing feeding of crabs. Results with reversibly blinded crabs demonstrate that the deterrence is mediated through the crabs’ chemical senses. We used bioassay-guided fractionation to identify the purple molecules aplysioviolin and phycoerythrobilin as a major and minor deterrent, respectively, in ink against crabs. These molecules derive from a light-harvesting protein in the photosynthetic system of dietary algae. This is the first demonstration of an animal converting a photosynthetic pigment into a chemical deterrent. Mixing opaline and ink enzymatically produces hydrogen peroxide, which also functions as a chemical deterrent against crabs. Our results and those of other studies show that sea hares use a diversity of molecules in their skin, mucus and ink secretion to chemically defend themselves against their potential predators. Aplysioviolin, phycoerythrobilin and hydrogen peroxide also exist in ink secretion of Aplysia dactylomela, a sea hare sympatric to blue crabs, and thus we posit that these molecules are potentially effective in ecologically relevant predator–prey interactions and need to be scrutinized in more ecologically relevant experiments.
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ABSTRACT: Sea hares of the genus Aplysia rely on an array of behavioral and chemical defenses, including the release of ink and opaline, to protect themselves from predation. While many studies have demonstrated that ink and opaline are repellent to predators, very little is known about which components of these secretions are active against predators. Ink was previously shown to facilitate the escape of Aplysia from predatory anemones (Anthopleura) by eliciting tentacle retraction and/or shriveling, and gastrovascular eversion, but the metabolites mediating this interaction were not identified. We investigated the metabolites in Aplysia californica secretions that were aversive to the anemone Anthopleura sola, as demonstrated by tentacle shriveling and/or retraction. We found that ink elicited tentacle shriveling and/or retraction, while opaline elicited a feeding response. The active components in ink do not appear to be diet-dependent, as ink was aversive regardless of diet (natural seaweed diet vs. Gracilaria ferox). Furthermore, metabolites extracted from G. ferox were not aversive, suggesting that the aversive components are produced by the sea hares. We then examined escapin, a protein in ink with antimicrobial properties. Escapin quickly forms reaction products when mixed with the amino acids l-lysine and l-arginine, which would occur when ink and opaline are released into the sea hare mantle cavity. Neither escapin alone nor escapin mixed with its amino acid substrate l-lysine elicited aversive behaviors either immediately before or 2 min before applying to the tentacles. In addition, escapin mixed with opaline and applied to tentacles after 2 min did not elicit a significant aversive response. Using bioassay-guided fractionation, we attempted to isolate the components in A. californica ink that are aversive to A. sola. We determined that multiple components in ink, including both lipophilic and hydrophilic constituents, elicited aversive responses. We hypothesize that these components may facilitate A. californica's escape from A. sola by eliciting tentacle shriveling and/or retraction, which lead to anemones dropping ensnared sea hares.Journal of Experimental Marine Biology and Ecology. 01/2006;
- American Zoologist - AMER ZOOL. 01/2001; 41(1):17-26.
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ABSTRACT: An evolutionary scenario incorporating recent advances in phylogenetic research begins with an opisthobranch-pulmonate common ancestor that was herbivorous and had some diet-derived chemical defense. The Nudibranchia and their closest relatives, the Notaspidea, form a lineage the ancestors of which had switched to feeding upon sponges and deriving protection from metabolites contained in them. Subsequently there have been repeated shifts in food and defensive metabolites, and trends are evident in the ability to detoxify, sequester and utilize metabolites from food, as well as to synthesize defensive compounds de novo. The Notaspidea display a minor adaptive radiation that foreshadows a more extensive one in the various lineages of nudibranchs. This review emphasizes changes that have occurred within the Holohepatica, or dorid nudibranchs (order Doridacea). Their sister-group, the Cladohepatica, consists of three other orders, Dendronotacea, Arminacea, and Aeolidiacea, in which there has been a shift from sponges to Cnidaria as food. The Dendronotacea often feed upon Octocorallia, which combine spicules, chemical defense, and stinging capsules and thereby suggest a transition from feeding on sponges. A previous diet of Octocorallia is suggested by the defensive use of prostaglandins in the dendronotacean Tethys fimbria, which eats crustaceans. A shift to bryozoans in some Arminacea is accompanied by use of different metabolites. Dorid nudibranchs evidently began as sponge-feeders, but some lineages have shifted to a variety of other food organisms, and others have specialized in the kind of sponges they feed on and how they do it. There have been shifts to bryozoans (Ectoprocta) and ascidians (Chordata: Urochordata) that track metabolites rather than the taxonomy of the food. There is a crude correlation between the genealogy and the defensive metabolites of the sponge-feeding dorids. De novo synthesis is well documented in this order and the metabolites are appropriately positioned so as to have an adaptive effect. The hypothesis that the capacity for de novo synthesis was acquired by gene transfer across lineages is rejected, partly on the basis of different chirality of metabolites in the nudibranchs and their food organisms. Instead it is proposed that there has been a preadaptive phase followed by evolution in a retrosynthetic mode, with selection favoring enzymes that enhance the yield of end products that are already present in the food.Chemoecology 01/1999; 9(4):187-207. · 1.95 Impact Factor