Conclusions
We are studying the anatomy and physiology of the olfactory and vomeronasal systems in axolotls with the goal of determining the behavioral functions of these two chemosensory systems in aquatic amphibians. Our anatomical studies demonstrate that the vomeronasal epithelium of axolotls is much like that of other tetrapods. Other studies indicate that the projections from the olfactory and vomeronasal epithelia into the central nervous system are separate through several synapses, suggesting that these chemosensory systems serve different functions. Our electrophysiological experiments have not revealed striking differences in odorant responsivity between the olfactory and vomeronasal epithelia, but we are just beginning to work in this area and cannot draw yet strong conclusions about the relative quality or strength of odorant responses in these sensory epithelia. We have begun to show that odorant cues play a role in both foraging and in social behavior in axolotls; we hope that by combining neurobiological and behavior studies, we will be able to fully understand the ways in which chemosensory stimuli are processed to mediate behavior in axolotls. Given that separate olfactory and vomeronasal systems are present in amphibians and in amniotes, the vomeronasal system must have been present in the last common ancestor of these two groups, and this animal is now thought to have been fully aquatic (Panchen, 1991; Lebedev and Coates, 1995). An understanding of the function of the vomeronasal system in aquatic amphibians may help shed light on the factors that led to the evolutionary origin of the vomeronasal system.
Access provided by Autonomous University of Puebla. Download to read the full chapter text
Chapter PDF
Keywords
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
References
Akopian, A., 2000, Neuromodulation of ligand-and voltage-gated channels in the amphibian retina, Microsc. Res. Tech. 50:403–410.
Anton, W., 1911, Die Nasenhtihle der Perennibranchiaten, Morphol. Jahrb. 44:179–199.
Armstrong, J. B., Duhon, S. T., and Malacinski, G. M., 1989, Raising the axolotl in captivity, in: Developmental Biology of the Axolotl, J. B. Armstrong and G. M. Malacinski, eds., Oxford University Press, New York, pp. 220–227.
Arnold, S. J., 1976, Sexual behavior, sexual interference and sexual defense in the salamanders Ambystoma maculatum, Ambystoma tigrinum and Plethodonjordani, Z. Tierpsychol. 42:247–300.
Asano-Miyoshi, M., Suda, T., Yasuoka, A., Osima, S., Yamashita, S., Abe, K., and Emori, Y., 2000, Random expression of main and vomeronasal olfactory receptor genes in immature and mature olfactory epithelia of Fugu rubripes, J. Biochem. 127:915–924.
Ashmore, J. F., Geleoc, G. S., and Harbott, L., 2000, Molecular mechanisms of sound amplification in the mammalian cochlea, Proc. Natl. Acad. Sci. U. S. A. 97:11759–11764.
Bhatnagar, K. P., 1980, The chiropteran vomeronasal organ: Its relevance to the phylogeny of bats, in: Proceedings of the Fifth International Bat Research Conference, D. E. Wilson and A. L. Gardner, eds., Texas Tech Press, Lubbock, TX, pp. 289–315.
Cao, Y., Oh, B. C., and Stryer, L., 1998, Cloning and localization of two multigene receptor families in goldfish olfactory epithelium, Proc. Natl. Acad. Sci. U. S. A. 95:11987–11992.
Cohen-Tannoudji, J., Lavenet, C., Locatelli, A., Tillet, Y., and Signoret, J., 1989, Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour, J. Reprod. Fert. 86: 135–144.
David, R. S., and Jaeger, R. G., 1981, Prey location through chemical cues by a terrestrial salamander, Copeia 1981:435–440.
Dorries, K. M., Adkins-Regan, E., and Halpern, B. P., 1997, Sensitivity and behavioral responses to the pheromone, androstenone, are not mediated by the vomeronasal organ in the pig, Brain Behav. Evol. 49: 52–63.
Eisthen, H. L., 1992, Phylogeny of the vomeronasal system and of receptor cell types in the olfactory and vomeronasal epithelia of vertebrates, Micr. Res. Tech. 23:1–21.
Eisthen, H. L., 1997, Evolution of vertebrate olfactory systems, Brain Behav. Evol. 50: 222–233.
Eisthen, H. L., 2000, Presence of the vomeronasal system in aquatic salamanders, Phil. Trans. Roy. Soc. (London) 355:1209–1213.
Eisthen, H. L., Sengelaub, D. R., Schroeder, D. M., and Alberts, J. R., 1994, Anatomy and forebrain projections of the olfactory and vomeronasal organs in axolotls (Ambystoma mexicanum), Brain Behav. Evol. 44: 108–124.
Farbman, A. I., and Gesteland, R. C., 1974, Fine structure of the olfactory epithelium in the mud puppy, Necturus maculosus, Am. J. Anat. 139:227–244.
Firestein, S., and Werblin, F., 1987, Gated currents in isolated olfactory receptor neurons of the larval tiger salamander, Proc. Natl. Acad. Sci. U. S. A. 84:6292–6296.
Firestein, S., and Werblin, F., 1989, Odor-induced membrane currents in vertebrate olfactory receptor neurons, Science 244:79–82.
Halpern, M., and Kubie, J. L., 1980, Chemical access to the vomeronasal organs of garter snakes, Physiol. Behav. 24:367–371.
Halpern, M., Kubie, J. L., 1984, The role of the ophidian vomeronasal system in species-typical behavior, Trends Neurosci. 7:472–477.
Halpern, M., and Martinez-Marcos, A., 2003, Structure and function of the vomeronasal system: An update, Prog. Neurobiol. 70:245–318.
Herrick, C. J., 1927, The amphibian forebrain IV: The cerebral hemispheres of Amblystoma, J. Comp. Neurol. Psychol. 43:231–325.
Herrick, C. J., 1933, The amphibian forebrain IV: Necturus, J. Comp. Neurol. 58:1–288.
Herrick, C. J., 1948, The Brain of the Tiger Salamander, University of Chicago Press, Chicago.
Hofmann, M. H., and Meyer, D. L., 1992, Peripheral origin of olfactory nerve fibers by-passing the olfactory bulb in Xenopus laevis, Brain Res. 589:161–163.
Houck, L. D., and Reagan, N. L., 1990, Male courtship pheromones increase female receptivity in a plethodontid salamander, Anim. Behav. 39:729–734.
Kauer, J. S., 2002, On the scents of smell in the salamander, Nature 417:336–342.
Kauer, J. S., and Moulton, D. G., 1974, Responses of olfactory bulb neurones to odour stimulation of small nasal areas in the salamander, J. Physiol. 243:717–737.
Kikuyama, S., Toyoda, F., Ohmiya, Y., Matsuda, K., Tanaka, S., and Hayashi, H., 1995, Sodefrin: A female-attracting peptide pheromone in newt cloacal glands, Science 267:1643–1645.
Kokoros, J. J., and Northcutt, R. G., 1977, Telencephalic afferents of the tiger salamander Ambystoma tigrinum tigrinum (Green), J. Comp. Neurol. 173:613–628.
Lebedev, O. A., and Coates, M. I., 1995, The postcranial skeleton of the Devonian tetrapod Tulerpeton curtum Lebedev, Zool. J. Linn. Soc. 114:307–348.
Liman, E. R., and Corey, D. P., 1996, Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ, J. Neurosci. 16:4625–4637.
Lindquist, S. B., and Bachmann, M. D., 1982, The role of visual and olfactory cues in the prey catching behavior of the tiger salamander, Ambystoma tigrinum, Copeia 1982:81–90.
Lowell, W. R., and Flanigan, W. F., Jr., 1980, Marine mammal chemoreception, Mamm. Rev. 10: 53–59.
Mackay-Sim, A., Duvall, D., and Graves, B. M., 1985, The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ, Brain Behav. Evol. 27:186–194.
Mackay-Sim, A., and Kubie, J. L., 1981, The salamander nose: A model system for the study for the study of spatial coding of olfactory quality, Chem. Senses 6:249–257.
Mackay-Sim, A., Shaman, P., and Moulton, D. G., 1982, Topographic coding of olfactory quality: Odorant-specific patterns of epithelial responsivity in the salamander, J. Neurophysiol. 48:584–596.
Münz, H., Claas, B., and Fritzsch, B., 1984, Electroreceptive and mechanoreceptive units in the lateral line of the axolotl Ambystoma mexicanum, J. Comp. Physiol. A 154:33–44.
Nevison, C. M., Armstrong, S., Beynon, R. J., Humphries, R. E., and Hurst, J. L., 2003, The ownership signature in mouse scent marks is involatile, Proc. R. Soc. Lond. B Biol. Sci. 270:1957–1963.
Oelschläger, H. A., and Buhl, E. H., 1985, Development and rudimentation of the peripheral olfactory system in the harbor porpoise Phocoena phocoena (Mammalia: Cetacea), J. Morph. 184:351–360.
Panchen, A. L., 1991, The early tetrapods: Classification and the shapes of cladograms, in: Origins of the Higher Groups of Tetrapods: Controversy and Consensus, H.-P. Schultze and L. Trueb, eds., Cornell University Press, Ithaca, NY, pp. 100–144.
Park, D., and Eisthen, H. L., 2003, Gonadotropin releasing hormone (GnRH) modulates odorant responses in the peripheral olfactory system of axolotls, J. Neurophysiol. 90:731–738.
Park, D., McGuire, J. M., Majchrzak, A. L., Ziobro, J. M., and Eisthen, H. L., 2004, Discrimination of conspecific sex and reproductive condition using chemical cues in axolotls (Ambystoma mexicanum), J. Comp. Physiol. A., in press.
Park, D., and Propper, C. R., 2002, The olfactory organ is activated by a repelling pheromone in the red-spotted newt Notophthalmus viridescens, Korean J. Biol. Sci. 6:233–237.
Park, D., Zawacki, S. R., and Eisthen, H. L., 2003, Olfactory signal modulation by molluscan cardioexcitatory tetrapeptide (FMRFamide) in axolotls (Ambystoma mexicanum), Chem. Senses 28:339–348.
Parsons, T. S., 1959, Nasal anatomy and the phylogeny of reptiles, Evolution 13:175–187.
Parsons, T. S., 1967, Evolution of the nasal structures in the lower tetrapods, Am. Zool. 7: 397–413.
Parsons, T. S., 1970, The origin of Jacobson’s organ. Forma Functio 3:105–111.
Placyk, J. S., Jr., and Graves, B. M., 2002, Prey detection by vomeronasal chemoreception in a plethodontid salamander, J. Chem. Ecol. 28:1017–1036.
Rollmann, S. M., Houck, L. D., and Feldhoff, R. C., 1999, Proteinaceous pheromone affecting female receptivity in a terrestrial salamander, Science 285:1907–1909.
Sam, M., Vora, S., Malnic, B., Ma, W., Novotny, M. V., and Buck, L.B., 2001, Odorants may arouse instinctive behaviors, Nature 412:142.
Schmidt, A., and Roth, G. 1990, Central olfactory and vomeronasal pathways in salamanders, J. Hirnforsch. 31:543–553.
Seydel, O., 1895, fiber die Nasenhflhle und das Jacobson’sche Organ der Amphibien: Eine vergleichend-anatomische Untersuchung, Morphol. Jahrb. 23:453–543.
Shaffer, H. B., 1993, Phylogenetics of model organisms: The laboratory axolotl, Ambystoma mexicanum, Syst. Biol. 42:508–522.
Shepherd, G. M., 1985, Are there labeled lines in the olfactory pathway?, in: Taste, Olfaction, and the Central Nervous System, D. W. Pfaff, Rockefeller University Press, New York, pp. 307–321.
Shoop, C. R., 1960, The breeding habits of the mole salamander, Ambystoma talpoideum (Holbrook), in Southeastern Louisiana, Tulane Stud. Zool. Bot. 8:65–82.
Singer, A. G., 1991, A chemistry of mammalian pheromones, J. Steroid Biochem. Mol. Biol. 39: 627–632.
Smith, T. D., Bhatnagar, K. P., Shimp, K. L., Kinzinger, J. H., Bonar, C. J., Burrows, A. M., Mooney, M. P., and Siegel, M. I., 2002, Histological definition of the vomeronasal organ in humans and chimpanzees, with a comparison to other primates, Anat. Rec. 267:166–176.
Smith, T. D., Siegel, M. I., and Bhatnagar, K. P., 2001, Reappraisal of the vomeronasal system of catarrhine primates: Ontogeny, morphology, functionality, and persisting questions, Anat. Rec. 265:176–192.
Szabo, T., Blähser, S., Denizot, J.-P., and Ravaille-Véron, M., 1991, Projection olfactive primaire extrabulbaire chez certaines poissons t6l6ost6ens, C. R. Acad. Sci. Paris 312:555–560.
Toyoda, F., Hayakawa, Y., Ichikawa, M., and Kikuyama, S., 1999, Olfactory responses to a female-attracting pheromone in the newt, Cynops pyrrhogaster, in: R. E. Johnston, D. Müller-Schwarze, and P. W. Sorensen, eds., Advances in Chemical Signals in Vertebrates, Kluwer Academic / Plenum, New York, pp.607–615.
Verrell, P. A., 1982, The sexual behavior of the red-spotted newt, Notophthalmus viridescens (Amphibia: Urodela: Salamandridae), Anim. Behav. 30:1224–1236.
Wabnitz, P. A., Bowie, J. H., Tyler, M. J., Wallace, J. C., and Smith, B. P., 1999, Aquatic sex pheromone from a male tree frog, Nature 401:444–445.
Wirsig-Wiechmann, C. R., Houck, L. D., Feldhoff, P. W., and Feldhoff, R. C., 2002, Pheromonal activation of vomeronasal neurons in plethodontid salamanders. Brain Res. 952:335–344.
Wysocki, C. J., Wellington, J. L., and Beauchamp, G. K., 1980, Access of urinary nonvolatiles to the mammalian vomeronasal organ, Science 207:781–783.
Yamamoto, N., and Ito, H., 2000, Afferent sources to the ganglion of the terminal nerve in teleosts, J. Comp. Neurol. 428:355–375.
Yamamoto, K., Kawai, Y., Hayashi, T., Ohe, Y., Hayashi, H., Toyoda, F., Kawahara, G., Iwata, T., and Kikuyama, S., 2000, Silefrin, a sodefrin-like pheromone in the abdominal gland of the sword-tailed newt, Cynops ensicauda, FEBS Lett. 472:267–270.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2005 Springer Science+Business Media, Inc.
About this paper
Cite this paper
Eisthen, H.L., Park, D. (2005). Chemical signals and vomeronasal system function in axolotls (Ambystoma mexicanum). In: Mason, R.T., LeMaster, M.P., Müller-Schwarze, D. (eds) Chemical Signals in Vertebrates 10. Springer, Boston, MA . https://doi.org/10.1007/0-387-25160-X_26
Download citation
DOI: https://doi.org/10.1007/0-387-25160-X_26
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-387-25159-2
Online ISBN: 978-0-387-25160-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)