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Barata, Eduardo Nuno

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  • Behavioral and olfactory responses of female Salaria pavo (Pisces : Blenniidae) to a putative multi-component male pheromone
    Publication . Serrano, Rui M.; Barata, E. N.; Birkett, Michael A.; Hubbard, Peter; Guerreiro, Patrícia; Canario, Adelino V. M.
    The peacock blenny, Salaria pavo (Risso 1810), typically breeds in rocky shores of the Mediterranean and adjacent Atlantic coast. Males defend a territory around a hole or cavity wherein females deposit eggs that the male guards until hatching. A pair of exocrine glands on the anal fin (anal glands) of males produces a putative pheromone involved in attraction of reproductively competent females to the nest. We used behavioral assays to assess speciesspecific attraction of reproductively competent females to putative male pheromones, including the anal gland pheromone. Additionally, chromatographic fractions of anal glands and male-conditioned water were tested for olfactory potency in females by electro-olfactogram analysis (EOG). In a flow-through tank or fluviarium, reproductive females were attracted to male-conditioned water and to the anal gland macerate from conspecifics but not to those of a closely related heterospecific. In addition, attraction of reproductive females to conspecific anal gland macerate occurred only during their initial upstream movement in the fluviarium; this was an ephemeral response when compared with the response to male-conditioned water that attracted females throughout the entire period of observation (5 min). Reproductive females also were attracted during the entire period of observation to water-conditioned by conspecific males whose anal glands had been removed. However, the attraction was more variable than that to water conditioned by intact males. Moreover, females were not attracted to male (without anal glands) odor during their initial upstream movement in the fluviarium. Finally, non-reproductive females were not attracted to the conspecific anal gland macerate. The EOG responses of females to molecular weight fractions and solid-phase extraction and high-performance liquid chromatography fractions of anal gland macerates and male-conditio ned water (with and without anal glands) suggest that the anal glands release hydrophilic odorants that consist mainly of molecules smaller than 500 Da. Furthermore, males released potent odorants that do not originate from the anal glands. We hypothesize that females respond to a multi-component male pheromone to find mates. The putative anal gland pheromone is possibly comprised of hydrophilic odorants, whereas the other component(s), presumably of gonadal origin, may be less water-soluble.
  • 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.
  • Possible disruption of pheromonal communication by humic acid in the goldfish, Carassius auratus
    Publication . Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.
    Humic acids are large, complex, organic molecules which are ubiquitous components of aquatic environments as products of degradation of plant material. In aqueous solution they form microvesicles. As many teleost pheromones are steroidal in nature, we hypothesised that they would preferentially dissolve in the organic, hydrophobic core of these vesicles instead of in water and therefore be unavailable for detection. This would have obvious and profound effects on many aspects of fish biology. To test this hypothesis we recorded electro-olfactogram (EOG) response of the goldfish (Carassius auratus) olfactory epithelium to the pheromones 17α,20β-dihydroxy-4-pregnen-3-one (17,20β-P), its sulphated conjugate (17,20β-P-SO4) and prostaglandin F2α (PGF2α), all at 10−11 to 10−8 M, in the absence and presence of humic acids (1–1000 mg l−1). At nearly all concentrations of humic acid tested, there was a significant attenuation of the amplitude of the initial (phasic) response to 17,20β-P compared to 17,20β-P alone. At higher concentrations of humic acid, the EOG response to 17,20β-P was often completely obliterated, suggesting that the concentration of the pheromone available to the olfactory epithelium was below the threshold of detection. Exposure of the olfactory epithelium to humic acid did not cause any short-term loss of sensitivity to 17,20β-P per se. Furthermore, simultaneous recording of electro-encephalograms from the olfactory bulb demonstrated that the nervous activity evoked by the same concentration of 17,20β-P was less intense in the presence of humic acid than its absence. PGF2α is non-steroidal and much more soluble in water. In contrast to 17,20β-P, only the higher concentrations of humic acid (100 and 1000 mg l−1) significantly diminished the EOG amplitude. 17,20β-P-SO4 is detected via a distinct olfactory mechanism to the free form. Given that the sulphate group increases the water solubility, we predicted that the effect of humic acid would be reduced. However, the effect of humic acid on EOG amplitude in response to 17,20β-P-SO4 was similar to that of the free form. We suggest that the steroid portion of the molecule adsorbs onto the surface of the humic acid microvesicles and is still effectively unavailable for olfactory detection. In conclusion, humic acid may significantly reduce the concentration of 17,20β-P and 17,20β-P-SO4 available for detection by Carassius auratus in natural environments. Furthermore, as many teleost pheromones are steroid derivatives, this phenomenon may be applicable to chemical communication systems in teleosts in general.
  • The role of male visual and chemical cues on the activation of female courtship behaviour in the sex-role reversed peacock blenny
    Publication . Gonçalves, D. M.; Barata, E. N.; Oliveira, R. F.; Canario, Adelino V. M.
    Chemical cues during courtship in peacock blenny Salaria pavo did not add significantly to the response of visual stimuli and females did not court when a male was not visible. The results showed that female S. pavo courtship behaviour was elicited exclusively by male visual features and not by a multicomponent signal in different sensory modalities. The time spent by females courting the male and exhibiting the nuptial colouration during visual trials correlated with the size of the male’s crest, suggesting a signalling function for this trait. Alternative hypothesis for the function of the putative pheromones released by the male’s anal gland are discussed. Evidence that female sexual motivation decreases towards the end of the breeding season is also provided, which should be considered in future mate choice experiments.
  • Urine as a social signal in the Mozambique tilapia (Oreochromis mossambicus)
    Publication . Almeida, O. G.; Miranda, A.; Frade, P.; Hubbard, P. C.; Barata, E. N.; Canario, A.V.M.
  • Olfactory sensitivity to catecholamines and their metabolites in the goldfish
    Publication . Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.
    The current study assessed the olfactory sensitivity of the goldfish (Carassius auratus L.) to the catecholamines, their immediate precursors and metabolites by use of the electro-olfactogram (EOG). The olfactory system of the goldfish was found to be sensitive to both adrenaline and dopamine with thresholds of detection of 10–7.8 and 10–7.9 M respectively, but less so to noradrenaline (threshold of detection 10–6.3 M). The 3-O-methoxy metabolites (metadrenaline, normetadrenaline and 3-O-methoxytyramine) evoked larger amplitude EOGs than the non-metabolized form with lower thresholds of detection. However, the olfactory system was less sensitive to the amino acid precursors L-tyrosine and L-DOPA, and markedly less so to the α-deaminated metabolites (3,4-dihydroxyphenyl glycol, 3,4-dihydroxy mandelic acid and dihydroxyphenyacetic acid). Sensitivity to metabolites, both α-deaminated and 3-O-methoxylated, was similar to the α-deaminated forms. Crossadaptation studies suggested that, while there is some degree of commonality of the receptor mechanisms with L-tyrosine and L-serine, a proportion of the response to the catecholamines is due to distinct receptor subtypes. Similarly, the 3-O-methoxy metabolites also had (a) separate receptor mechanism(s), although, again, there was overlap with the adrenaline/dopamine receptor site(s). Presence of the α-adrenoreceptor antagonist prazosin or the peripheral DA2 dopamine receptor antagonist domperidone caused partial attenuation of the EOG responses to adrenaline and dopamine, but had much less effect on the responses to their 3-O-methoxy metabolites. The β-adrenoreceptor antagonist sotalol had no such effect. This suggests that the olfactory catecholamine receptors are structurally and functionally distinct from systemic adreno- and dopamine receptors. The current study raises the possibility that release of catecholamines or their 3-O-methoxy metabolites to the water may play a role in chemical communication.
  • Adaptation to reduced salinity affects the olfactory sensitivity of Senegalese sole (Solea senegalensis Kaup 1858) to Ca2+ and Na+ but not amino acids
    Publication . 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+.
  • Olfactory discrimination of female reproductive status by male tilapia (Oreochromis mossambicus)
    Publication . Miranda, A.; Almeida, O. G.; Hubbard, Peter; Barata, E. N.; Canario, Adelino V. M.
    The current study investigated whether discrimination of sexual status of female tilapia by males is mediated by olfaction. Size-matched groups of female tilapia were assigned as pre- or post-ovulatory according to the time since their last ovulation (15–19·days pre-ovulatory, N=7; 1–3·days post-ovulatory, N=8). Female-conditioned water and body fluids (urine, bile, faeces and plasma) were assessed for olfactory potency in males by recording the electro-olfactogram (EOG). Water extracts, urine and faeces from pre-ovulatory females all evoked significantly larger amplitude EOGs in male fish (N=6), with correspondingly lower thresholds of detection, than those from post-ovulatory females. Plasma and bile evoked very large amplitude EOGs in males but with no differences between the two groups of females. Anosmic males (N=6) did not behave differently towards pre- or post-ovulatory females, while sham-operated males (N=6) showed a marked increase in urination rate towards pre-ovulatory females. We conclude that the ability of male tilapia to discriminate between females of differing reproductive status is mediated by odorants released into the water, probably via the urine and faeces, by pre-ovulatory females.
  • Social odors conveying dominance and reproductive information induce rapid physiological and neuromolecular changes in a cichlid fish
    Publication . Simões, José M.; Barata, Eduardo Nuno; Harris, Rayna M.; O'Connell, Lauren A.; Hofmann, Hans A.; Oliveira, Rui F.
    Background: Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and this ability has an impact in their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. Results: We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Conclusions: Our results show that different olfactory stimuli from conspecifics' have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioral plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment.
  • Seasonal cell differentiation and olfactory potency of secretions by the anal glands of male peacock blenny Salaria Pavo
    Publication . Serrano, Rui M.; Lopes, Orlando; Hubbard, Peter; Araújo, J.; Canario, Adelino V. M.; Barata, E. N.
    The current study shows cytological differences between the anal glands of pre-spawning and spawning peacock blennies Salaria pavo. The cytological differences in the anal gland coincide with higher olfactory potency of their secretions in spawning males, suggesting that seasonal differentiation of cell clusters secreting neutral mucins is related to the production and release of the putative sex pheromone.