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Research Article

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

Giuseppe Giordano, Marianna Carbone, Maria Letizia Ciavatta, Eleonora Silvano, Margherita Gavagnin, Mary J. Garson, Karen L. Cheney, I Wayan Mudianta, Giovanni Fulvio Russo, Guido Villani, Laura Magliozzi, View ORCID ProfileGianluca Polese, Christian Zidorn, Adele Cutignano, Angelo Fontana, Michael T. Ghiselin, and View ORCID ProfileErnesto Mollo
PNAS March 28, 2017 114 (13) 3451-3456; first published March 13, 2017; https://doi.org/10.1073/pnas.1614655114
Giuseppe Giordano
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
bDepartment of Science and Technology, Parthenope University of Naples, Naples 80143, Italy;
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Marianna Carbone
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Maria Letizia Ciavatta
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Eleonora Silvano
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
cDepartment of Biology, Federico II University of Naples, Naples 80126, Italy;
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Margherita Gavagnin
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Mary J. Garson
dSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Karen L. Cheney
eSchool of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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I Wayan Mudianta
fDepartment of Analytical Chemistry, Universitas Pendidikan Ganesha, 81116 Bali, Indonesia;
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Giovanni Fulvio Russo
bDepartment of Science and Technology, Parthenope University of Naples, Naples 80143, Italy;
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Guido Villani
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Laura Magliozzi
cDepartment of Biology, Federico II University of Naples, Naples 80126, Italy;
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Gianluca Polese
cDepartment of Biology, Federico II University of Naples, Naples 80126, Italy;
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  • ORCID record for Gianluca Polese
Christian Zidorn
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
gPharmazeutisches Institut, Christian-Albrechts-Universität zu Kiel, Kiel 24118, Germany;
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Adele Cutignano
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Angelo Fontana
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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Michael T. Ghiselin
hDepartment of Invertebrate Zoology, California Academy of Sciences, San Francisco, CA 94118
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Ernesto Mollo
aInstitute of Biomolecular Chemistry, National Research Council of Italy, 80078 Pozzuoli, Italy;
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  • ORCID record for Ernesto Mollo
  • For correspondence: emollo@icb.cnr.it
  1. Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved February 14, 2017 (received for review September 7, 2016)

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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.

  • marine chemical ecology
  • chemical defense
  • olfactory aposematism
  • avoidance learning
  • volatile terpenes

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.

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A tactile form of olfaction
Giuseppe Giordano, Marianna Carbone, Maria Letizia Ciavatta, Eleonora Silvano, Margherita Gavagnin, Mary J. Garson, Karen L. Cheney, I Wayan Mudianta, Giovanni Fulvio Russo, Guido Villani, Laura Magliozzi, Gianluca Polese, Christian Zidorn, Adele Cutignano, Angelo Fontana, Michael T. Ghiselin, Ernesto Mollo
Proceedings of the National Academy of Sciences Mar 2017, 114 (13) 3451-3456; DOI: 10.1073/pnas.1614655114

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A tactile form of olfaction
Giuseppe Giordano, Marianna Carbone, Maria Letizia Ciavatta, Eleonora Silvano, Margherita Gavagnin, Mary J. Garson, Karen L. Cheney, I Wayan Mudianta, Giovanni Fulvio Russo, Guido Villani, Laura Magliozzi, Gianluca Polese, Christian Zidorn, Adele Cutignano, Angelo Fontana, Michael T. Ghiselin, Ernesto Mollo
Proceedings of the National Academy of Sciences Mar 2017, 114 (13) 3451-3456; DOI: 10.1073/pnas.1614655114
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