Journal of Comparative Physiology A

, Volume 197, Issue 8, pp 839–849 | Cite as

Olfactory sensitivity to amino acids in the blackspot sea bream (Pagellus bogaraveo): a comparison between olfactory receptor recording techniques in seawater

  • Peter C. HubbardEmail author
  • Eduardo N. Barata
  • Rodrigo O. A. Ozório
  • Luisa M. P. Valente
  • Adelino V. M. Canário
Original Paper


The current study investigated the olfactory sensitivity of the blackspot sea bream to amino acids, odorants associated with food detection in fish, and compared the efficacy of two different experimental methods: multi-unit recording from the olfactory nerve and the electro-olfactogram (EOG). Twenty essential amino acids plus l-DOPA evoked clear, concentration-dependent olfactory responses using both methods, with estimated thresholds of 10−8.5–10−6.2 M (nerve recording) and 10−7.5–10−4.8 M (EOG). The most potent amino acids were l-cysteine, l-methionine (both sulphur-containing), l-alanine, l-leucine (both neutral), l-glutamine (amide-containing) and l-serine (hydroxyl-containing). The least potent were l-proline (secondary α-amino group), the aromatic amino acids and glycine (simplest). Although the rank order of olfactory potency was similar for the two methods used, and the calculated thresholds given by the two methods were positively correlated, the sensitivity of the EOG was consistently lower than multi-unit recording by approximately one order of magnitude, presumably due to the electrical shunting effect of seawater. As in freshwater, the EOG could be a valid method for comparing olfactory potency of different odorants in stenohaline marine fish; however, for absolute ‘biological’ thresholds, a more invasive recording technique, such as multi-unit recording from the olfactory nerve, should be used.


Olfaction Amino acid Sea bream Electro-olfactogram (EOG) Electrophysiology 



Analysis of variance








Ethyl-3-aminobenzoate methanesulfonate salt


Personal computer



This research was supported by the Pluriannual Funding Program of the Science and Technology Foundation (FCT), Portugal. Fish care and experimentation complied with the “Principles of animal care” (No. 86-23, revised 1985) of the National Institute of Health (USA) and Portuguese national laws.


  1. Brünnich MT (1768) Ichthyologia massiliensis. Roth & Proft, CopenhagenGoogle Scholar
  2. Byrd RP Jr, Caprio J (1982) Comparison of olfactory receptor (EOG) and bulbar (EEG) responses to amino acids in the catfish, Ictalurus punctatus. Brain Res 249:73–80PubMedCrossRefGoogle Scholar
  3. Caprio J (1978) Olfaction and taste in the channel catfish: an electrophysiological study of the responses to amino acids and derivatives. J Comp Physiol A 123:357–371CrossRefGoogle Scholar
  4. Caprio J, Derby CD (2008) Aquatic animal models in the study of chemoreception. In: Basbum AI, Kaneko A, Shepherd GM, Westheimer G (eds) Olfaction and taste, vol 4. Academic Press, San Diego, pp 97–134Google Scholar
  5. Carr WES, Netherton JC III, Gleeson RA, Derby CD (1996) Stimulants of feeding behavior in fish: analyses of tissues of diverse marine organisms. Biol Bull 190:149–160CrossRefGoogle Scholar
  6. Figueiredo-Silva AC, Corraze G, Kaushik S, Peleteiro JB, Valente LMP (2010) Modulation of blackspot seabream (Pagellus bogaraveo) intermediary metabolic pathways by dispensable amino acids. Amino Acids 39:1401–1416. doi: 10.1007/s00726-010-0599-y PubMedCrossRefGoogle Scholar
  7. Friedrich RW, Korsching SI (1997) Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging. Neuron 18:737–752PubMedCrossRefGoogle Scholar
  8. Friedrich RW, Korsching SI (1998) Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J Neurosci 18:9977–9988PubMedGoogle Scholar
  9. Goh Y, Tamura T, Kobayashi H (1979) Olfactory responses to amino acids in marine teleosts. Comp Biochem Physiol A-Physiol 62A:863–868CrossRefGoogle Scholar
  10. Hamdani EH, Døving KB (2007) The functional organization of the fish olfactory system. Prog Neurobiol 82:80–86. doi: 10.1016/j.pneurobio.2007.02.007 CrossRefGoogle Scholar
  11. Hanson LR, Sorensen PW, Cohen Y (1998) Sex pheromones and amino acids evoke distinctly different spatial patterns of electrical activity in the goldfish olfactory bulb. In: Murphy C (ed) Olfaction and taste Xii—an international symposium, vol 855. New York Acad Sciences, New York, pp 521–524Google Scholar
  12. Hara TJ (1994) The diversity of chemical stimulation in fish olfaction and gustation. Rev Fish Biol Fish 4:1–35CrossRefGoogle Scholar
  13. Hubbard PC, Barata EN, Canário AVM (2000) Olfactory sensitivity to changes in environmental [Ca2+] in the marine teleost Sparus aurata. J Exp Biol 203:3821–3829PubMedGoogle Scholar
  14. Hubbard PC, Barata EN, Canário AVM (2003a) Olfactory sensitivity of the gilthead seabream (Sparus auratus L.) to conspecific body fluids. J Chem Ecol 29:2481–2498PubMedCrossRefGoogle Scholar
  15. Hubbard PC, Barata EN, Canário AVM (2003b) Olfactory sensitivity to catecholamines and their metabolites in the goldfish. Chem Senses 28:207–218PubMedCrossRefGoogle Scholar
  16. Ishida Y, Kobayashi H (1992) Stimulatory effectiveness of amino acids on the olfactory response in an algivorous marine teleost, the rabbitfish Siganus fuscescens Houttuyn. J Fish Biol 41:737–748. doi: 10.1111/j.1095-8649.1992.tb02703.x CrossRefGoogle Scholar
  17. Kang J, Caprio J (1991) Electro-olfactogram and multiunit olfactory receptor responses to complex mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 98:699–721PubMedCrossRefGoogle Scholar
  18. Kobayashi H, Goh Y (1985) Comparison of the olfactory responses to amino acids obtained from receptor and bulbar levels in a marine teleost. Exp Biol 44:199–210PubMedGoogle Scholar
  19. Lucero MT, Farrington H, Gilly WF (1994) Quantification of l-DOPA and dopamine in squid ink: implications for chemoreception. Biol Bull 187:55–63CrossRefGoogle Scholar
  20. Meredith TL, Kajiura SM (2010) Olfactory morphology and physiology of elasmobranchs. J Exp Biol 213:3449–3456. doi: 10.1242/jeb.045849 PubMedCrossRefGoogle Scholar
  21. Ngai J, Chess A, Dowling MM, Necles N, Macagno ER, Axel R (1993) Coding of olfactory information: topography of odorant receptor expression in the catfish olfactory epithelium. Cell 72:667–680PubMedCrossRefGoogle Scholar
  22. Ozório ROD, Andrade C, Timoteo VMFA, da Conceição LEC, Valente LMP (2009) Effects of feeding levels on growth response, body composition, and energy expenditure in blackspot seabream, Pagellus bogaraveo, juveniles. J World Aquacult Soc 40:95–103CrossRefGoogle Scholar
  23. Scott JW, Scott-Johnson PE (2002) The electoolfactogram: a review of its history and uses. Microsc Res Tech 58:152–160. doi: 10.1002/jemt.10133 PubMedCrossRefGoogle Scholar
  24. Serrano RM, Barata EN, Birkett MA, Hubbard PC, Guerreiro PS, Canario AVM (2008) Behavioural and olfactory responses of female Salaria pavo (Pisces: Blenniidae) to a putative multi-component male pheromone. J Chem Ecol 34:647–658PubMedCrossRefGoogle Scholar
  25. Silver WL (1982) Electrophysiological responses from the peripheral olfactory system of the American eel, Anguilla rostrata. J Comp Physiol A 148:379–388CrossRefGoogle Scholar
  26. Silver WL, Caprio J, Blackwell JF, Tucker D (1976) The underwater electro-olfactogram: a tool for the study of the sense of smell of marine fishes. Experimentia 32:1216–1217CrossRefGoogle Scholar
  27. Tricas TC, Kajiura SM, Summers AP (2009) Response of the hammerhead shark olfactory epithelium to amino acid stimuli. J Comp Physiol A-Neuroethol Sens Neural Behav Physiol 195:947–954. doi: 10.1007/s00359-009-0470-3 PubMedCrossRefGoogle Scholar
  28. Valentincic T, Wegert S, Caprio J (1994) Learned olfactory discrimination versus innate taste responses to amino acids in channel catfish (Ictalurus punctatus). Physiol Behav 55:865–873PubMedCrossRefGoogle Scholar
  29. Velez Z, Hubbard PC, Barata EN, Canário AVM (2005) Evidence for functional asymmetry in the olfactory system of the Senegalese sole (Solea sensgalensis). Physiol Biochem Zool 78:756–765PubMedCrossRefGoogle Scholar
  30. Velez Z, Hubbard PC, Hardege JD, Barata EN, Canário AVM (2007) The contribution of amino acids to the odour of a prey species in the Senegalese sole (Solea senegalensis). Aquaculture 265:336–342. doi: 10.1016/j.aquaculture.2007.02.029 CrossRefGoogle Scholar
  31. Velez Z, Hubbard PC, Barata EN, Canário AVM (2009) Adaptation to reduced salinity affects the olfactory sensitivity of Senegalese sole (Solea senegalensis) to Ca2+ and Na+ but not amino acids. J Exp Biol 212:2532–2540. doi: 10.1242/jeb.030775 PubMedCrossRefGoogle Scholar
  32. Wheeler A (1978) Key to the fishes of Northern Europe. Frederick Warne Publishers Ltd, LondonGoogle Scholar
  33. Yacoob SY, Browman HI (2007) Olfactory and gustatory sensitivity to some feed-related chemicals in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture 263:303–309. doi: 10.1016/j.aquaculture.2006.11.005 CrossRefGoogle Scholar
  34. Yacoob SY, Browman HI, Jensen PA (2004) Electroencephalogram recordings from the olfactory bulb of juvenile (0 year) Atlantic cod in response to amino acids. J Fish Biol 65:1657–1664. doi: 10.1111/j.1095-8649.2004.00574.x CrossRefGoogle Scholar
  35. Yamamoto Y, Ueda H (2009) Behavioral responses by migratory chum salmon to amino acids in natal stream water. Zool Sci 26:778–782. doi: 10.2108/zsj.26.778 PubMedCrossRefGoogle Scholar
  36. Yamamoto Y, Hino H, Ueda H (2010) Olfactory imprinting of amino acids in lacustrine sockeye salmon. PLoS One 5:e8633. doi: 10.1371/journal.pone.0008633 PubMedCrossRefGoogle Scholar
  37. Yambe H, Kitamura S, Kamio M, Yamada M, Matsunaga S, Fusetani N, Yamazaki F (2006) L-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc Natl Acad Sci USA 103:15370–15374PubMedCrossRefGoogle Scholar
  38. Zar JH (1996) Biostatistical analysis. Pearson Higher Education, New JerseyGoogle Scholar
  39. Zielinski BS, Hara TJ (2006) Olfaction. In: Hara TJ, Zielinski BS (eds) Sensory systems neuroscience, vol 25. Elsevier, New York, pp 1–43Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Peter C. Hubbard
    • 1
    Email author
  • Eduardo N. Barata
    • 1
    • 2
  • Rodrigo O. A. Ozório
    • 3
  • Luisa M. P. Valente
    • 3
    • 4
  • Adelino V. M. Canário
    • 1
  1. 1.Centro de Ciências do MarUniversidade do AlgarveFaroPortugal
  2. 2.Departamento de BiologiaUniversidade de ÉvoraÉvoraPortugal
  3. 3.CIMAR/CIIMAR Centro Interdisciplinar de Investigação Marinha e AmbientalUniversidade do PortoPortoPortugal
  4. 4.ICBAS-Instituto de Ciências Biomédicas de Abel SalazarUniversidade do PortoPortoPortugal

Personalised recommendations