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Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments
Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved February 14, 2017 (received for review September 7, 2016)

Significance
This report gives empirical evidence indicating that chemoreception of volatile/odorant lipophilic compounds, almost insoluble in water, can occur in aquatic environments, by means of “tactile” forms of olfaction. This thesis has been proved by exploring the defensive role of terpenes isolated from benthic invertebrates. The isolated metabolites were found to act both as defensive toxic weapons and as olfactory signals. In addition, the most abundant compound induced avoidance learning in crustaceans and fish that experienced postingestive negative effects.
Abstract
Olfaction is considered a distance sense; hence, aquatic olfaction is thought to be mediated only by molecules dissolved in water. Here, we challenge this view by showing that shrimp and fish can recognize the presence of hydrophobic olfactory cues by a “tactile” form of chemoreception. We found that odiferous furanosesquiterpenes protect both the Mediterranean octocoral Maasella edwardsi and its specialist predator, the nudibranch gastropod Tritonia striata, from potential predators. Food treated with the terpenes elicited avoidance responses in the cooccurring shrimp Palaemon elegans. Rejection was also induced in the shrimp by the memory recall of postingestive aversive effects (vomiting), evoked by repeatedly touching the food with chemosensory mouthparts. Consistent with their emetic properties once ingested, the compounds were highly toxic to brine shrimp. Further experiments on the zebrafish showed that this vertebrate aquatic model also avoids food treated with one of the terpenes, after having experienced gastrointestinal malaise. The fish refused the food after repeatedly touching it with their mouths. The compounds studied thus act simultaneously as (i) toxins, (ii) avoidance-learning inducers, and (iii) aposematic odorant cues. Although they produce a characteristic smell when exposed to air, the compounds are detected by direct contact with the emitter in aquatic environments and are perceived at high doses that are not compatible with their transport in water. The mouthparts of both the shrimp and the fish have thus been shown to act as “aquatic noses,” supporting a substantial revision of the current definition of the chemical senses based upon spatial criteria.
Footnotes
- ↵1To whom correspondence should be addressed. Email: emollo{at}icb.cnr.it.
Author contributions: E.M. designed research; G.G., M.C., M.L.C., E.S., I W.M., G.V., L.M., G.P., A.C., A.F., and E.M. performed research; E.M. contributed new reagents/analytic tools; G.G., M.C., M.L.C., M.G., M.J.G., K.L.C., I W.M., G.F.R., C.Z., A.C., A.F., M.T.G., and E.M. analyzed data; and G.G., M.T.G., and E.M. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1614655114/-/DCSupplemental.