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- Effect of acute copper sulfate exposure on olfactory responses to amino acids and pheromones in goldfish (Carassius auratus)Publication . Kolmakov, Nikolai N.; Hubbard, Peter; Lopes, Orlando; Canario, Adelino V. M.Exposure of olfactory epithelium to environmentally relevant concentrations of copper disrupts olfaction in fish. To examine the dynamics of recovery at both functional and morphological levels after acute copper exposure, unilateral exposure of goldfish olfactory epithelia to 100 μM CuSO4 (10 min) was followed by electro-olfactogram (EOG) recording and scanning electron microscopy. Sensitivity to amino acids (L-arginine and L-serine), generally considered food-related odorants, recovered most rapidly (three days), followed by that to catecholamines(3-O-methoxytyramine),bileacids(taurolithocholic acid) and the steroid pheromone, 17,20 -dihydroxy-4-pregnen- 3-one 20-sulfate, which took 28 days to reach full recovery. Sensitivity to the postovulatory pheromone prostaglandin F2R had not fully recovered even at 28 days. These changes in sensitivity were correlated with changes in the recovery of ciliated and microvillous receptor cell types. Microvillous cells appeared largely unaffected by CuSO4 treatment. Cilia in ciliated receptor neurones, however, appeared damaged one day post-treatment and were virtually absent after three days but had begun to recover after 14 days. Together, these results support the hypothesis that microvillous receptor neurones detect amino acids whereas ciliated receptor neurones were not functional and are responsible for detection of social stimuli (bile acidsandpheromones).Furthermore, differences in sensitivity to copper may be due to different transduction pathways in the different cell types.
- Evidence that olfactory sensitivities to calcium and sodium are mediated by different mechanisms in the goldfish Carassius auratusPublication . Hubbard, Peter; Canario, Adelino V. M.The current study investigated whether the olfactory sensitivity to Ca2+ and Na+ is mediated by the same mechanism in the goldfish, a freshwater teleost. The olfactory responses, as assessed by recording the electro-encephalogram (EEG) from the olfactory bulb, to changes in external [Ca2+] and to [Na+] were recorded in the absence and presence of increasing concentrations of the other ion. Low concentrations of Na+ (0–1.0 mM) had no significant effects on the olfactory response to changes in [Ca2+] in terms of EC50, Imax or Hill co-efficient (n = 8). A relatively high concentration of Na+ (10 mM) significantly reduced the Imax and increased the EC50. One hundred millimolars Na+reduced the olfactory response to Ca2+ to undetectable levels. Conversely, low concentrations of Ca2+ (0.1 and 1.0 mM) significantly attenuated the olfactory response to changes in environmental [Na+], reducing the amplitude of response and increasing the threshold of detection (n = 7). However, a high concentration of Ca2+ (10 mM) failed to attenuate the olfactory response to Na+ completely. Taken together, these results suggest that, at normal environmental concentrations of these ions, Ca2+ and Na+ are detected by distinct and separate cellular mechanisms. However, there seems to be a degree of overlap between the two mechanisms. The exact mechanisms involved, and their biological roles, remain to be established.
- Behavioral and olfactory responses of female Salaria pavo (Pisces : Blenniidae) to a putative multi-component male pheromonePublication . 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.
- 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 conspecific bile fluid and skin mucus in the European eel Anguilla anguilla (L.)Publication . Huertas, Mar; Hubbard, Peter; Canario, Adelino V. M.; Cerda, J.The present study assessed the olfactory potency of conspecific bile fluid and skin mucus in the European eel Anguilla anguilla by the electro-olfactogram. Immature males showed high olfactory sensitivity to conspecific bile, giving large amplitude responses in a concentrationdependent manner with estimated thresholds of detection of <1:107 (n = 6). Mucus also proved to contain highly potent odorants with thresholds of detection of c. 1:106 (n = 6). Crude solidphase extraction of bile fluid (C-18 and C-2/ENV+ cartridges) showed that the majority of olfactory activity in bile fluid was contained in the eluate of C-18 cartridges (n = 6). There were quantitative differences, however, between the sexes; female bile fluid had a higher proportion of activity in this fraction. Similar solid-phase extraction of mucus showed that it contains a higher proportion of odorants in the C-18 filtrate than bile fluid. Mucus from mature eels, however, had a higher proportion of olfactory activity in the eluate than immature fish (n = 6). Cross-adaptation experiments suggest that there are qualitative differences in the odorants contained in bile and mucus depending on both the sex and state of sexual maturation of the donor (n = 6). These results are consistent with a role for chemical communication in the reproduction of the European eel and suggest that both bile and mucus are potential sources of the odorants involved.
- 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+.
- 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.
- Follow your nose: chemical communication throughout the European eel (Anguilla anguilla, L.) life-cyclePublication . Huertas, Mar; Canario, Adelino V. M.; Hubbard, PeterEuropean eels are important in both scientific and economic terms. Unfortunately, current populations are becoming increasingly endangered and urgentmanagement is needed. Several aspects of eel biology, together with their highly developed sense of smell, suggest that chemical communication could be involved at key stages of their life-history. Thus, advances in this area could generate novel tools for stock management.
- Seasonal cell differentiation and olfactory potency of secretions by the anal glands of male peacock blenny Salaria PavoPublication . 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.
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