Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments.

Giordano, Giuseppe, Carbone, Marianna, Ciavatta, Maria Letizia, Silvano, Eleonora, Gavagnin, Margherita, Garson, Mary J., Cheney, Karen L., Mudianta, I Wayan, Russo, Giovanni Fulvio, Villani, Guido, Magliozzi, Laura, Polese, Gianluca, Zidorn, Christian, Cutignano, Adele, Fontana, Angelo, Ghiselin, Michael T. and Mollo, Ernesto (2017) Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments. Proceedings of the National Academy of Sciences, 114 (13). pp. 3451-3456. DOI 10.1073/pnas.1614655114.

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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.

Document Type: Article
Keywords: avoidance learning; chemical defense; marine chemical ecology; olfactory aposematism; volatile terpenes
Research affiliation: Kiel University > Kiel Marine Science
OceanRep > The Future Ocean - Cluster of Excellence
Refereed: Yes
Open Access Journal?: No
DOI etc.: 10.1073/pnas.1614655114
ISSN: 0027-8424
Projects: Future Ocean
Date Deposited: 08 Jan 2018 13:14
Last Modified: 24 Apr 2019 13:38
URI: http://oceanrep.geomar.de/id/eprint/41285

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