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.2017 Mar 28;114(13):3451-3456.
doi: 10.1073/pnas.1614655114. Epub 2017 Mar 13.

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

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

Giuseppe Giordano et al. Proc Natl Acad Sci U S A..

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 edwardsi and its specialist predator, the nudibranch gastropodTritonia striata, from potential predators. Food treated with the terpenes elicited avoidance responses in the cooccurring shrimpPalaemon 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.

Keywords: avoidance learning; chemical defense; marine chemical ecology; olfactory aposematism; volatile terpenes.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Metabolites fromM. edwardsi. (A) Chemical structures of isofuranodiene (1), atractylon (2), isoatractylon (3), edwardsiolide A (4), edwardsiolide B (5), and edwardsiolide C (6). (B) Detail of the analytical AgNO3-treated TLC plate revealing the occurrence of bands corresponding to furanosesquiterpenes1–3 in the crude diethyl ether extract ofM. edwardsi (MAAS), after spraying with Ehrlich’s reagent. Eluent isn-hexane/diethylether 95:5.
Fig. 2.
Fig. 2.
Studied animals. (A)M. edwardsi; (B)T. striata; (C) yellow arrows indicate egg masses ofT. striata onM. edwarsdi (in retracted state). (Scale bars, 5 mm.) (D)T. striata larvae inside its egg mass.
Fig. S1.
Fig. S1.
(A) The modular system of tanks (Upper), and the filtering sump (Lower). (B) The sampling sites along the coast of the Campania region (Italy).
Fig. 3.
Fig. 3.
Quantification of the metabolites and evaluation of their biological activity. (A andB) Concentration of compounds1–3 quantified by (A) GC-MS and (B)1H NMR. Values shown are means and SDs from triplicate extractions from different colonies/individuals. (C,E, andG) Feeding deterrence dose–response curves againstP. elegans. The significant differences were evaluated using the two-tailed Fisher's exact test (n = 10 for each tested concentration,α = 0.05). (D,F, andH) Dose–response curves of toxicity toA. salina. The results are shown as the means and SDs of triplicate wells. Because deaths also occurred in the control (vehicle DMSO only), percentages of deaths were corrected by using Abbott’s formula (dashed lines).
Fig. 4.
Fig. 4.
Avoidance learning assay onP. elegans. Recorded responses: green, food acceptance (as shown in Movie S1); yellow, food rejection after touching (as shown in Movie S2); and red, vomiting (as shown in Movie S3). (A) Response from the whole sample (n = 15) to food containing (−)-isoatractylon at a concentration of 4.0 mg/mL (step I, step II) and untreated plain food (step III). (B) Response from the subgroup of the vomiting shrimp (n = 5).P values are calculated using the two-tailed Fisher's exact test (α = 0.05).
Fig. 5.
Fig. 5.
Avoidance learning in the zebrafish. Recorded responses: green, food acceptance; yellow, food rejection after touching (as shown in Movie S4); gray, rejection without touching; and violet, evacuation of fecal bolus. (A) Time-dependent responses to food containing (−)-isoatractylon (3) followed by responses to nontreated plain food, and to commercial granular pellets (ordinary food). (B) Responses to plain food.P values are calculated using the two-tailed Fisher's exact test (n.s. = not significant;n = 8;α = 0.05).
Fig. 6.
Fig. 6.
Proposed multiple ecological roles of furanosesquiterpenes1–3. (Scale bars, 10 mm.)
Fig. S2.
Fig. S2.
(A)M. edwardsi (surface brooding). Retracted pedicels covered with eggs. (B) Fully developed planula. (Scale bar, 1 mm.) (C) Contracted planula.
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