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- Identification, release and olfactory detection of bile salts in the intestinal fluid of the Senegalese sole (Solea senegalensis)Publication . Velez, Zélia; Hubbard, Peter; Welham, K.; Hardege, Jörg D.; Barata, E. N.; Canario, Adelino V. M.Olfactory sensitivity to bile salts is wide-spread in teleosts; however, which bile salts are released in suYcient quantities to be detected is unclear. The current study identiWed bile salts in the intestinal and bile Xuids of Solea senegalensis by mass spectrometry–liquid chromatography and assessed their olfactory potency by the electro-olfactogram.
- Adaptation to reduced salinity affects the olfactory sensitivity of Senegalese sole (Solea senegalensis Kaup 1858) to Ca2+ and Na+ but not amino acidsPublication . Velez, Zélia; Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.The Senegalese sole is a marine flatfish, which often penetrates into estuarine waters to feed. It cannot, however, survive in full freshwater. The current study investigated the effect of adaptation to low salinity (10‰) on olfactory responses to changes in environmental [Ca2+] and [Na+] and amino acids by the electro-encephalogram (EEG) recorded from the olfactory bulb. The sole showed olfactory responses to increases in environmental [Na+] and decreases in environmental [Ca2+]; sensitivity to Na+ was greater at 10‰ whereas sensitivity to Ca2+ was greater at 35‰. Decreased environmental [Na+] increased sensitivity to changes in [Ca2+] whereas increased environmental [Ca2+] decreased bulbar responses to changes in [Na+]. Sensitivity to amino acids was unaffected by external salinity. However, the absence of external Na+ strongly decreased bulbar responses to amino acids in fish adapted to 35‰ seawater but not in those at 10‰. The absence of external Ca2+ had no such effect at either salinity. This suggests that odorant-receptor binding and/or olfactory transduction is reliant on external Na+ (but not Ca2+) at higher salinities but the olfactory system is able to adapt to lower environmental [Na+]. Taken together, these results suggest that reductions of external salinity modulate olfactory sensitivity to environmental Ca2+ and Na+ but not amino acids. However, at low salinities, olfactory sensitivity to amino acids is maintained by decreasing reliance on external Na+.
- GABA receptors in the olfactory epithelium of the gilthead seabream (Sparus aurata)Publication . Costa, Rita; Velez, Zélia; Hubbard, PeterExposure to high PCO2/low pH seawater induces behavioural alterations in fish; a possible explanation for this is a reversal of Cl-/HCO3- currents through GABAA receptors (the GABAA receptor theory). However, the main evidence for this is that gabazine, a GABAA receptor antagonist, reverses these effects when applied to the water, assuming that exposure to systems other than the CNS would be without effect. Here, we show the expression of both metabotropic and ionotropic GABA receptors, and the presence of GABAA receptor protein, in the olfactory epithelium of gilthead seabream. Furthermore, exposure of the olfactory epithelium to muscimol (a specific GABAA receptor agonist) increases or decreases the apparent olfactory sensitivity to some odorants. Thus, although the exact function of GABAA receptors in the olfactory epithelium is not yet clear, this may complicate the interpretation of studies wherein water-borne gabazine is used to reverse the effects of high CO2 levels on olfactory-driven behaviour in fish.
- Independent effects of seawater pH and high P-CO2 on olfactory sensitivity in fish: possible role of carbonic anhydrasePublication . Velez, Zélia; Costa, Rita; Wang, Wenjing; Hubbard, PeterOcean acidificationmay alter olfactory-driven behaviour in fish by direct effects on the peripheral olfactory system; olfactory sensitivity is reduced in CO2-acidified seawater. The current study tested whether this is due to elevated P-CO2 or the consequent reduction in seawater pH and, if the former, the possible involvement of carbonic anhydrase, the enzyme responsible for the hydration of CO2 and production of carbonic acid. Olfactory sensitivity to amino acids was assessed by extracellularmulti-unit recording from the olfactory nerve of the gilthead seabream (Sparus aurata L.) in normal seawater (pH similar to 8.2), and after acute exposure to acidified seawater (pH similar to 7.7) but normal P-CO2 (similar to 340 mu atm) or to high P-CO2 seawater (similar to 1400 mu atm) at normal pH (similar to 8.2). Reduced pH in the absence of elevated P-CO2 caused a reduction in olfactory sensitivity to L-serine, L-leucine, L-arginine and L-glutamine, but not L-glutamic acid. Increased P-CO2 in the absence of changes in pH caused reduced olfactory sensitivity to L-serine, L-leucine and L-arginine, including increases in their threshold of detection, but had no effect on sensitivity to L-glutamine and L-glutamic acid. Inclusion of 1 mmol l(-1) acetazolamide (a membrane-permeant inhibitor of carbonic anhydrase) in the seawater reversed the inhibition of olfactory sensitivity to L-serine caused by high P-CO2. Ocean acidification may reduce olfactory sensitivity by reductions in seawater pH and intracellular pH (of olfactory receptor neurones); the former by reducing odorant-receptor affinity, and the latter by reducing the efficiency of olfactory transduction. The physiological role of carbonic anhydrase in the olfactory receptor neurones remains to be explored.
- Functional asymmetry in the olfactory system of a flatflish (Solea Senegalensis)Publication . Velez, Zélia; Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.The two olfactory epithelia of the family Soleidae are exposed to differentwater sources; the upper (right) epitheliumsamples thewater column whereas the lower (left) samples interstitial water. Given that one of the major prey species of the Senegalese sole (Solea senegalensis) is the ragworm Hediste diversicolor which lives in the substrate, we hypothesized that the lower epitheliummay have evolved sensitivity to odorants released by the ragworm whereas the upper epithelium may be more involved in chemical communication and therefore is more sensitive to odorants released by conspecifics.
- Evidence that 1-methyl-l-tryptophan is a food-related odorant for the Senegalese sole (Solea senegalensis)Publication . Velez, Zélia; Hubbard, Peter; Hardege, Jörg D.; Welham, K.; Barata, E. N.; Canario, Adelino V. M.Nocturnal animals often rely heavily on olfactory cues to locate their food. This is especially true for fish whose prey live buried in the substrate. The aim of the current study was to identify non-polar odorants released by the ragworm (Hediste diversicolor) that are detected by the olfactory system of the Senegalese sole (Solea senegalensis) and therefore may be food-related cues. Ragworm-conditioned water was passed through a C18 solid-phase extraction cartridge (to remove polar compounds) and the eluate fractionated by reverse phase high-performance liquid chromatography (HPLC). The fractions were then tested for olfactory activity in the sole by the electro-olfactogram (EOG). Most olfactory activity was found in the first two fractions to elute from the HPLC column (0–4 min). Liquid chromatography-mass spectrometry (LC/MS) of both fractions revealed a base peak with a molecular mass of 219.4 Da and a fragment of 205.3 Da. These data are consistent with a methylated form of tryptophan; synthetic 1-methyl-l-tryptophan had a similar HPLC retention time (2.8 min) and similar LC/MS spectra. Furthermore, sole showed olfactory sensitivity to 1-methyl-l-tryptophan with the lower (left) epithelium being more sensitive than the upper (right). Cross-adaptation (using EOG recording) suggested that the olfactory receptors responding to 1-methyl-l-tryptophan are different in the lower epithelium from the upper. These results suggest that ragworms release 1-methyl-l-tryptophan, or similar tryptophan derivative, and that sole may use this chemical cue to locate and/or identify one of their main prey species. This may help the formation of artificial feeds that are more attractive to sole.
- Olfactory transduction pathways in the Senegalese sole Solea senegalensisPublication . Velez, Zélia; Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.This study tested whether differences in sensitivity between the upper and lower olfactory epithelia of Solea senegalensis are associated with different odorant receptors and transduction pathways, using the electro-olfactogram. Receptor mechanisms were assessed by cross-adaptation with amino acids (L-cysteine, L-phenylalanine and 1-methyl-L-tryptophan) and bile acids (taurocholic acid and cholic acid). This suggested that relatively specific receptors exist for 1-methyl-L-tryptophan and Lphenylalanine (food-related odorants) in the lower epithelium, and for taurocholic acid (conspecificderived odorant) in the upper. Inhibition by U73122 [a phospholipase C (PLC) inhibitor] suggested that olfactory responses to amino acids were mediated mostly, but not entirely, by PLC-mediated transduction (IC50; 15–55 nM), whereas bile acid responses were mediated by both PLC and adenylate cyclase–cyclic adenosine monophosphate (AC–cAMP) (using SQ-22536; an AC inhibitor). Simultaneous application of both drugs rarely inhibited responses completely, suggesting possible involvement of non-PLC and non-AC mediated mechanisms. For aromatic amino acids and bile acids, there were differences in the contribution of each transduction pathway (PLC, AC and non-PLC and non-AC) between the two epithelia. These results suggest that differences in sensitivity of the two epithelia are associated with differences in odorant receptors and transduction mechanisms.
- Prey odour enhances swimming activity and feed intake in the Senegalese solePublication . Barata, E. N.; Hubert, F.; Conceição, L. E. C.; Velez, Zélia; Rema, P.; Hubbard, Peter; Canario, Adelino V. M.Olfaction is important in many aspects of the life-history of fishes including feeding, and more so in nocturnal benthic feeders. In the current study we assessed the importance of olfaction in food-search behaviour of the Senegalese sole, an economically important marine species both as farmed and wild-caught. Whole-body homogenates of the polychaete Diopatra neapolitana were fractionated by solid-phase extraction (SPE) using C18 cartridges and the olfactory potency of the resultant fractions (hydrophobic eluate and hydrophilic filtrate) was assessed by the electro-olfactogram in juvenile sole. In addition, the effect of both the homogenate and SPE fractions on sole locomotion was assessed in a flow-through tank (fluviarium). Finally, whole-body homogenate was added to commercial feed pellets and tested whether it could enhance food consumption by sole. The SPE hydrophilic filtrate contained the majority of the olfactory activity found in the whole-body homogenate. Both the homogenate and filtrate, but not the eluate, increased number of movements, time moving, linear velocity, distance travelled and time swimming upstream of sole in the fluviarium; ablation of the olfactory epithelia disrupted these behavioural responses to the homogenate. Intact sole consumed more pellets flavoured with worm homogenate than those without. These results show that olfaction plays an important role in food-search behaviour of the Senegalese sole and that the hydrophilic fraction of D. neapolitana whole-body homogenate contains key substances affecting sole search behaviour; moreover, ingestion by sole was enhanced by addition of worm homogenate to the dry feed pellets.
- The contribution of amino acids to the odour of a prey species in the Senegalese sole (Solea senegalensis)Publication . Velez, Zélia; Hubbard, Peter; Hardege, Jörg D.; Barata, E. N.; Canario, Adelino V. M.For many fish, olfaction is important in food search and consumption. Amino acids are known to elicit feeding behaviour in several species. The aim of the current study was to evaluate the contribution of amino acids to the odour of a natural prey organism of the Senegalese sole (Solea senegalensis). Both whole-body macerates and substances released to the water by living ragworms (Hediste diversicolor) were fractionated by molecular weight filtration followed by solid-phase extraction (SPE), and the olfactory activity of the resultant fractions was assessed by the electro-olfactogram (EOG) in the sole. The amino acid concentrations of the macerate and water were determined by gas chromatography and mass spectrometry (GC–MS). In the macerate, the majority of odorants were small molecular weight compounds (b500 Da) which were not retained by C-18 SPE cartridges. An artificial mixture of amino acids at the same concentrations as found in the macerate had similar olfactory potency. The odorants released to the water by living ragworms were also small molecular weight compounds (b500 Da) but the majority of olfactory activity could be extracted by C-18 SPE cartridges. The concentrations of amino acids in these samples were too low to contribute greatly to its olfactory potency. These results suggest that, whilst olfactory sensitivity to amino acids may explain most of the potency of the macerate, living ragworms are releasing additional odorants other than amino acids which may be equally important in chemosensory food location in the sole.
- Differential detection of conspecific-derived odorants by the two olfactory epithelia of the Senegalese sole (Solea senegalensis)Publication . Velez, Zélia; Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.The two olfactory epithelia of members of the family Soleidae sample two distinct water sources; the upper (right) side is in contact with the open water column whilst the lower (left) side is in contact with interstitial water. To evaluate whether there are differences in the sensitivities, and therefore functional roles, of the two epithelia the olfactory activity of conspecific-derived odorants was assessed in both using the electro-olfactogram (EOG). The upper nostril was significantly more sensitive to conspecific bile fluid, intestinal fluid and mucus than the lower nostril. Crude fractionation of these samples (solid-phase extraction with C18 and C2/ENV+ cartridges) revealed that olfactory activity in each body fluid was likely due to a mixture of compounds. In each case, the upper olfactory epithelium was significantly more sensitive than the lower. Similarly, olfactory sensitivity to a range of C24 and C27 bile acids was greater in the upper epithelium. These results suggest that intra-specific chemical communication is mediated mainly, if not entirely, by the upper olfactory epithelium. The odorants involved, and their functional roles, remain to be established.