Skip to main content
SpringerLink
Log in

Evidence That Petromyzontid Lampreys Employ a Common Migratory Pheromone That Is Partially Comprised of Bile Acids

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

This study examined whether the larval pheromone employed by adult sea lamprey (Petromyzon marinus) to locate spawning streams and known to be at least partially comprised of bile acids is also employed by other lamprey species. Both production and release of lamprey-specific bile acids, and sensitivity to them were examined in a wide variety of species. High pressure liquid chromatography and electrospray ionization/mass spectrometry (ESI-MS) found gallbladders from 10 species of European and North American lamprey to contain large quantities of petromyzonol sulfate (PS) together with much smaller quantities of allocholic acid (ACA) and petromyzonol (P). Evaluation of holding waters from three of these species using ESI-MS found all to contain large quantities of PS and lesser quantities of ACA in similar ratios. Electro-olfactogram recording from the olfactory systems of three parasitic lamprey species found all to detect PS and ACA with high sensitivity. Behavioral studies using migratory adult sea lamprey found them to be attracted to the odors of heterospecific larvae as well as conspecific larvae, both of which contained similar amounts of PS and ACA. Finally, adult silver lampreys (Ichthyomyzon unicuspis) were also found to be attracted to the odor of larval sea lamprey. Together, these results demonstrate that PS and ACA are commonly produced and released by larval petromyzontid lampreys and likely used as part of a common evolutionarily conserved pheromone. This scenario is reasonable because lampreys share similar larval and spawning habitat requirements, and their larvae derive no apparent benefit from producing compounds that serve as an attractant for adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Applegate, V. C. 1950. Natural history of the sea lamprey (Petromyzon marinus) in Michigan. U.S. Fish Wild. Serv. Spec. Sci. Rep. Fish. Serv. 55:237.

    Google Scholar 

  • Bergstedt, R.A. and Seelye, J. G. 1995. Evidence for lack of homing by sea lamprey. Trans. Am. Fish. Soc. 124:235–239.

    Google Scholar 

  • Bjerselius, R. K., Li, W., Teeter, J. H., Seelye, J.G., Maniak, P.J., Grant, G.C., Polkinghorne, C. N., and Sorensen, P. W. 2000. Direct behavioral evidence that unique bile acids released by larval sea lamprey function as a migratory pheromone. Can. J. Fish. Aquat. Sci. 57:557–569.

    Google Scholar 

  • Close, D.A., Fitzpatrick, M. S., and Li, H. W. 2002. The ecological and cultural importance of a species at risk of extinction, Pacific lamprey. Fisheries 27:19–25.

    Google Scholar 

  • Docker, M.F., Youson, J. H., Beamish, R.J.,and Devlin, R. H. 1999. Phylogeny of the lamprey genus Lampetra inferred from mitochondrial cytochrome b and ND3 gene sequences. Can. J. Fish. Aquat. Sci. 56:2340–2349.

    Google Scholar 

  • Elliott, W. H. 1985. Metabolism of bile acids in liver and extrahepatic tissues, pp. 303–329, in H. Danielsson and J. Sjovall (eds.). Sterols and Bile Acids, Vol. 12. Elsevier, Amsterdam.

    Google Scholar 

  • Fodale, M.F., Bergstedt, R. A., Cuddy, D.W., Adams, J.V., and Stolyarenko, D. A. 2003. Planning and executing a lampricide treatment of the St. Marys River using georeferenced data. J. Great Lakes Res. 29:706–716.

    Google Scholar 

  • Fricker, G., Wossner, R., Drewe, J., Fricker, R., and Boyer, J. L. 1997. Enterohepatic circulation of scymnol sulfate in an elasmobranch, the little skate (Raja erinacesa). Am.J.Physiol. 273:G1023–G1030.

    Google Scholar 

  • Gill, H. S., Renaud, C.B., Chapleau, F., Mayden, R.L., and Potter, I. C. 2003. Phylogeny of living parasitic lampreys (Petromyzontiformes) based on morphological data. Copeia 4:687–703.

    Google Scholar 

  • Hardisty, M.W. and Potter, I. C. 1971a. The general biology of adult lampreys, pp. 127–206, in M. W. Hardisty and I. C. Potter (eds.). The Biology of Lampreys, Vol. 1. Academic Press, London.

    Google Scholar 

  • Hardisty, M.W. and Potter, I. C. 1971b. The behavior, ecology, and growth of larval lampreys, pp. 85–127, in M. W. Hardisty and I. C. Potter (eds.). The Biology of Lampreys, Vol. 1. Academic Press, London.

    Google Scholar 

  • Hoshita, T. 1985. Bile alcohols and primitive bile acids, pp. 279–302, in H. Danielsson and J. Sjovall (eds.). Sterols and Bile Acids, Vol. 12. Elsevier, Amsterdam.

    Google Scholar 

  • Hylemon, P. B. 1985. Metabolism of bile acids in intestinal microflora, pp. 331–343, in H. Danielsson and J. Sjovall (eds.). Sterols and Bile Acids, Vol. 12. Elsevier, Amsterdam.

    Google Scholar 

  • Li, W., Scott, A. P., Siefkas, M. J., Yan, H., Liu, Q., and Yun, S.-S. 2002. Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296:138–141.

    Google Scholar 

  • Li, W., Siefkes, M. J., Scott, A. P., and Teeter, J. H. 2003. Sex pheromone communication in the sea lamprey. J. Great Lakes Res. 29:85–94.

    Google Scholar 

  • Li, W. and Sorensen, P. W. 1997. Highly independent receptor sites for naturally occurring bile acids in the sea lamprey, Petromyzon marinus. J. Comp. Physiol. A 180:429–438.

    Google Scholar 

  • Li, W., Sorensen, P. W., and Gallaher, D. D. 1995. The olfactory system of migratory adult sea lamprey is acutely and specifically sensitive to unique bile acids released by conspecific larvae. J. Gen. Physiol. 105:569–587.

    Google Scholar 

  • Locket, P.L. and Gallaher, D. D. 1989. An improved procedure for bile acid extraction and purification and tissue distribution in the rat. Lipids 24:221–223.

    Google Scholar 

  • Maitland, P. S. 1980. Review of the ecology of lampreys of Northern Europe. Can. J. Fish. Aquat. Sci. 37:1944–1952.

    Google Scholar 

  • Malmqvist, B. 1980. The spawning migration of the brook lamprey, Lampetra planeri Bloch, in a south Swedish stream. J. Fish Biol. 16:105–114.

    Google Scholar 

  • MANION, P.J.andHANSON, L. H. 1980. Spawning behavior and fecundity of lampreys from the upper three Great Lakes. Can. J. Fish. Aquat. Sci. 37:1635–1640.

    Google Scholar 

  • Moore, H. H. and Schleen, L. P. 1980. Changes in spawning runs of sea lamprey (Petromyzon marinus) in selected streams in Lake Superior after chemical control. Can. J. Fish. Aquat. Sci. 37:1851–1860.

    Google Scholar 

  • Morman, R. H. 1979. Distribution and ecology of lampreys in the lower peninsula of Michigan, 1957–75. Great Lakes Fish. Comm. Tech. Rep. 33:59.

    Google Scholar 

  • Morman, R. H., Cuddy, D. W.,and Rugen, P. C. 1980. Factors influencing the distribution of sea lamprey (Petromyzon marinus) in the Great Lakes. Can. J. Fish. Aquat. Sci. 37:1811–1826.

    Google Scholar 

  • Polkinghorne, C. N., Olson, J. M., Gallaher, D. D., and Sorensen, P. W. 2001. Larval sea lamprey release two unique bile acids to the water at a sufficient rate to produce a detectable pheromonal plume. Fish Physiol. Biochem. 24:15–30.

    Google Scholar 

  • Potter, I. C. 1980. The Petromyzoniformes with particular reference to paired species. Can. J. Fish. Aquat. Sci. 37:1595–1605.

    Google Scholar 

  • Potter, I. C. and Hilliard, R. W. 1987. A proposal for the functional and phylogenetic significance of differences in the dentition of lampreys (Agnatha: Petromyzontiformes). J. Zool. 212:713–737.

    Google Scholar 

  • Purvis, H. A. 1980. Effects of temperature on metamorphosis and the age and length at metamorphosis in sea lamprey (Petromyzon marinus) in the Great Lakes. Can. J. Fish. Aquat. Sci. 37:1824–1834.

    Google Scholar 

  • Schuldt, R. J. and Goold, R. 1980. Changes in the distribution of native lampreys in Lake Superior tributaries in response to sea lamprey (Petromyzon marinus) control, 1953–77. Can. J. Fish. Aquat. Sci. 37:1872–1885.

    Google Scholar 

  • Sorensen, P. W. and Caprio, J. 1998. Chemoreception, pp. 375–405, in D. H. Evans (ed.). The Physiology of Fishes, 2nd edn. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Sorensen, P. W., Li, W., Bjerselius, R., Zielinski, B., and Bowdin, L. 1995. Peripheral olfactory sensitivity of sea lamprey is greatest just prior to their spawning migration and then rapidly deteriorates. Chem. Senses 20:782.

    Google Scholar 

  • Sorensen, P.W. and Stacey, N. E. 1999. Evolution and specialization of fish hormonal pheromones, pp. 15–48, in R. E. Johnson, D. Muller-Schwarze, and P. W. Sorensen (eds.). Advances of Chemical Signals in Vertebrates. Kluwer Academic/Plenum Publishers, New York.

    Google Scholar 

  • Sorensen, P.W. and Vrieze, L. A. 2003. Recent progress understanding the chemical ecology and potential application of the sea lamprey migratory pheromone. J. Great Lakes Res. 29(Suppl. 1):66–84.

    Google Scholar 

  • Sorensen, P. W., Vrieze, L. A., and Fine, J. M. 2003. A multi-component migratory pheromone in the sea lamprey. Fish Biochem. Physiol. 28:253–257.

    Google Scholar 

  • Stacey, N. E. and Sorensen, P. W. 2002. Fish hormonal pheromones, pp. 375–435, in D. W. Pfaff, D. Arnold, A. Etgen, S. Fahrbach, and R. Rubin (eds.). Hormones, Brain, and Behavior, Vol. 2. Academic Press, New York.

    Google Scholar 

  • Tuunainen, P., Ikonen, E., and Auvinen, H. 1980. Lampreys and lamprey fisheries in Finland. Can. J. Fish. Aquat. Sci. 37:1953–1959.

    Google Scholar 

  • Twohey, M. B., Sorensen, P. W., and Li, W. 2003. Possible applications of pheromones in an integrated sea lamprey management program. J. Great Lakes Res. 29(Suppl. 1):794–800.

    Google Scholar 

  • Vladykov, V. D. and Kott, E. 1980. Description and key to metamorphosed specimens and ammocoetes of Petromyzonidae found in the Great Lakes region. Can. J. Fish. Aquat. Sci. 37:1616–1625.

    Google Scholar 

  • Vrieze, L. A. and Sorensen, P. W. 2001. Laboratory assessment of the role of a larval pheromone and natural stream odor in spawning stream localization by migratory sea lamprey (Petromyzon marinus). Can. J. Fish. Aquat. Sci. 58:2374–2385.

    Google Scholar 

  • Yamazaki, Y. and Goto, A. 2000. Breeding season and nesting assemblages in two forms of Lethen-teron reissneri, with reference to reproductive isolating mechanisms. Ichthyol. Res. 47(3):271–276.

    Google Scholar 

  • Yun, S.-S., Scott, A.P., Bayer, J. M., Seelye, J. G., Close, D. A., and Li, W. 2003. HPLC and ELISA analyses of larval bile acids from Pacific and western brook lampreys. Steroids 68:5151–5523.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Fisheries, Wildlife and Conservation Biology, University of Minnesota, St. Paul, Minnesota, 55108, USA

    Jared M. Fine, Lance A. Vrieze & Peter W. Sorensen

Authors
  1. Jared M. Fine
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lance A. Vrieze
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter W. Sorensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fine, J.M., Vrieze, L.A. & Sorensen, P.W. Evidence That Petromyzontid Lampreys Employ a Common Migratory Pheromone That Is Partially Comprised of Bile Acids. J Chem Ecol 30, 2091–2110 (2004). https://doi.org/10.1023/B:JOEC.0000048776.16091.b1

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:JOEC.0000048776.16091.b1

Search

Navigation