1. Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments
- Author
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Giuseppe Giordano, Angelo Fontana, Ernesto Mollo, Guido Villani, Christian Zidorn, I. Wayan Mudianta, Margherita Gavagnin, Karen L. Cheney, Laura Magliozzi, Mary J. Garson, Maria Letizia Ciavatta, Marianna Carbone, Giovanni Fulvio Russo, Eleonora Silvano, Adele Cutignano, Michael T. Ghiselin, Gianluca Polese, 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
- Subjects
0301 basic medicine ,Aquatic Organisms ,animal structures ,Gastropoda ,Secondary Metabolism ,Brine shrimp ,Aposematism ,Olfaction ,Avoidance learning ,Chemical defense ,Marine chemical ecology ,Olfactory aposematism ,Volatile terpenes ,Multidisciplinary ,Biology ,Palaemon elegans ,01 natural sciences ,03 medical and health sciences ,marine chemical ecology, chemical defence, olfactory aposematism, avoidance learning, volatile terpenes ,marine chemical ecology ,chemical defense ,Animals ,Zebrafish ,Volatile Organic Compounds ,Behavior, Animal ,olfactory aposematism ,010405 organic chemistry ,Ecology ,fungi ,Nudibranch ,Biological Sciences ,biology.organism_classification ,Tritonia striata ,Arthropod mouthparts ,0104 chemical sciences ,Shrimp ,Smell ,030104 developmental biology ,volatile terpenes ,Odorants ,avoidance learning - 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 furanosesquiter- penes 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.
- Published
- 2017
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