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. T raditionally, the sense of smell has been regarded as a distance sense (like vision), whereas the sense of taste has been treated as a contact sense (like touch). This classification of the chemical senses (olfaction and gustation) based on their spatial range persists in contemporary literature. Accordingly, biomolecules smaller than ∼300 Da, which can be transported through air, and which finally bind to odorant receptors expressed in olfactory neurons, are generally considered odorant molecules. Conversely, the molecules sensed by taste have to be in solution and in contact with the receptor (1). However, the claim that "only olfaction can provide information on the identity of the water mass encountered" by marine organisms (2) implies that water-soluble compounds, which are typically "tasted" by the tongues of terrestrial animals, act as olfactory cues in aquatic environments. Consequently, it may be asked how typical odorant molecules such as small terpenes from plants and marine sponges that combine high volatility in air with insolubility in water can produce olfactory sensations in marine organisms, thereby giving protection from predators and cues to finding food and mates.
The surface of many marine organisms is colonized by complex communities of microbes, yet our understanding of the diversity and role of host-associated microbes is still limited. We investigated the association between Ectopleura crocea (a colonial hydroid distributed worldwide in temperate waters) and prokaryotic assemblages colonizing the hydranth surface. We used, for the first time on a marine hydroid, a combination of electron and epifluorescence microscopy and 16S rDNA tag pyrosequencing to investigate the associated prokaryotic diversity. Dense assemblages of prokaryotes were associated with the hydrant surface. Two microbial morphotypes were observed: one horseshoe-shaped and one fusiform, worm-like. These prokaryotes were observed on the hydrozoan epidermis, but not in the portions covered by the perisarcal exoskeleton, and their abundance was higher in March while decreased in late spring. Molecular analyses showed that assemblages were dominated by Bacteria rather than Archaea. Bacterial assemblages were highly diversified, with up to 113 genera and 570 Operational Taxonomic Units (OTUs), many of which were rare and contributed to <0.4%. The two most abundant OTUs, likely corresponding to the two morphotypes present on the epidermis, were distantly related to Comamonadaceae (genus Delftia ) and to Flavobacteriaceae (genus Polaribacter ). Epibiontic bacteria were found on E. crocea from different geographic areas but not in other hydroid species in the same areas, suggesting that the host-microbe association is species-specific. This is the first detailed report of bacteria living on the hydrozoan epidermis, and indeed the first study reporting bacteria associated with the epithelium of E. crocea . Our results provide a starting point for future studies aiming at clarifying the role of this peculiar hydrozoan-bacterial association.
Ectopleura crocea is an Anthomedusan hydroid, frequently recorded and abundant on artificial substrates. Here we examine whether the abundance of this species varies seasonally on a shipwreck in the Northern Adriatic at a depth of 10–12 m. Individuals were first found in late autumn when temperatures had dropped below 15 °C, forming scattered colonies composed of a few, small hydranths bearing immature gonophores. Substratum cover and density increased throughout late winter and spring, reaching a peak in April. At temperatures of about 19 °C, colonies were no longer present in June and remained absent throughout the summer. The polyp gut contents comprised mostly crustaceans.
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