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2017 ; 114
(13
): 3451-3456
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Volatile secondary metabolites as aposematic olfactory signals and defensive
weapons in aquatic environments
#MMPMID28289233
Giordano G
; Carbone M
; Ciavatta ML
; Silvano E
; Gavagnin M
; Garson MJ
; Cheney KL
; Mudianta IW
; Russo GF
; Villani G
; Magliozzi L
; Polese G
; Zidorn C
; Cutignano A
; Fontana A
; Ghiselin MT
; Mollo E
Proc Natl Acad Sci U S A
2017[Mar]; 114
(13
): 3451-3456
PMID28289233
show ga
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.