title: Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments.
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 octocoralMaasella edwardsiand its specialist predator, the nudibranch gastropodTritonia striata, from potential predators. Food treated with the terpenes elicited avoidance responses in the cooccurring shrimpPalaemon elegansRejection 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.
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.|Department of Science and Technology, Parthenope University of Naples, Naples 80143, Italy.
authors.forename: Giuseppe
authors.initials: G
authors.lastname: Giordano
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Marianna
authors.initials: M
authors.lastname: Carbone
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Maria Letizia
authors.initials: ML
authors.lastname: Ciavatta
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.|Department of Biology, Federico II University of Naples, Naples 80126, Italy.
authors.forename: Eleonora
authors.initials: E
authors.lastname: Silvano
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Margherita
authors.initials: M
authors.lastname: Gavagnin
authors.affiliation: School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia.
authors.forename: Mary J
authors.initials: MJ
authors.lastname: Garson
authors.affiliation: School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia.
authors.forename: Karen L
authors.initials: KL
authors.lastname: Cheney
authors.affiliation: Department of Analytical Chemistry, Universitas Pendidikan Ganesha, 81116 Bali, Indonesia.
authors.forename: I Wayan
authors.initials: IW
authors.lastname: Mudianta
authors.affiliation: Department of Science and Technology, Parthenope University of Naples, Naples 80143, Italy.
authors.forename: Giovanni Fulvio
authors.initials: GF
authors.lastname: Russo
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Guido
authors.initials: G
authors.lastname: Villani
authors.affiliation: Department of Biology, Federico II University of Naples, Naples 80126, Italy.
authors.forename: Laura
authors.initials: L
authors.lastname: Magliozzi
authors.affiliation: Department of Biology, Federico II University of Naples, Naples 80126, Italy.
authors.forename: Gianluca
authors.identifier: 0000-0002-6322-7769
authors.initials: G
authors.lastname: Polese
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.|Pharmazeutisches Institut, Christian-Albrechts-Universität zu Kiel, Kiel 24118, Germany.
authors.forename: Christian
authors.initials: C
authors.lastname: Zidorn
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Adele
authors.initials: A
authors.lastname: Cutignano
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy.
authors.forename: Angelo
authors.initials: A
authors.lastname: Fontana
authors.affiliation: Department of Invertebrate Zoology, California Academy of Sciences, San Francisco, CA 94118.
authors.forename: Michael T
authors.initials: MT
authors.lastname: Ghiselin
authors.affiliation: Institute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy; emollo@icb.cnr.it.
authors.forename: Ernesto
authors.identifier: 0000-0001-7379-1788
authors.initials: E
authors.lastname: Mollo
mesh_terms: D000818:Animals; D059001:Aquatic Organisms / Q000502:physiology*; D001522:Behavior, Animal; D049851:Gastropoda / Q000502:physiology*; D009812:Odorants / Q000032:analysis; D064210:Secondary Metabolism; D012903:Smell; D055549:Volatile Organic Compounds / Q000737:chemistry / Q000378:metabolism*; D015027:Zebrafish / Q000502:physiology*
chemical_list: D055549:Volatile Organic Compounds
keywords: avoidance learning; chemical defense; marine chemical ecology; olfactory aposematism; volatile terpenes