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A Multi-Component Species Identifying Pheromone in the Goldfish

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Abstract

Although it has been established that sexually-immature goldfish and their relatives recognize members of their own species by using chemicals that they release, the identity of this cue(s) and whether it might be produced and used by other life stages is not yet known. To address this question, this study tested the behavioral responses of sexually immature and mature goldfish to each other’s body washings, their sensitivity to this cue, the role of the olfactory sense in detecting it, and whether it is comprised of either polar and/or non-polar compounds. Tests that used two-choice mazes discovered that juvenile, immature, mature male, and mature female goldfish all release and respond to a common chemical cue(s). Dilution studies next demonstrated that this cue is active when diluted over 10 times and thus capable of functioning as a short range attractant/identifier. Olfactory occlusion demonstrated that it is detected by the olfactory sense. Finally, chemical fractionation demonstrated that it is comprised of both polar and non-polar components but likely does not include bile acids. Together, these results suggest that all life stages of goldfish use a complex multicomponent pheromonal odor to discern species identity, and that this odor has the potential to function with hormonal metabolites to identify sexual condition in behaviorally active fish of many species.

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References

  • Baker, C. F., and Montgomery, J. C. 2001. Species-specific attraction of migratory banded kokopu juveniles to adult pheromones. J. Fish Biol. 58:1221–1229.

    Article  Google Scholar 

  • Baker, C. F., Carton, A. G., Fine, J. M., and Sorensen, P. W. 2006. Can bile acids function as a migratory pheromone in banded kokopu, Galaxias fasciatus (Gray)? Ecol. Freshw. Fish 15:275–283.

    Article  Google Scholar 

  • Brown, G. E., Adrian, J. C., Smyth, E., Leet, H., and Brennan, S. 2000. Ostariophysan Alarm pheromones: Laboratory and field tests of the functional significance of nitrogen oxides J. Chem. Ecol. 26:139–154,

    Article  CAS  Google Scholar 

  • Derby, C. D., and Sorensen, P. W. 2008. Neural processing, perception and behavioral responses to natural chemical stimuli by fish and crustaceans. J. Chem. Ecol. 34:898–914.

    Article  CAS  PubMed  Google Scholar 

  • Døving, K. B., Selset, R., and Thommsen, G. 1980. Olfactory sensitivity to bile acids in salmonid fishes. Acta Phisiol. Scand. 108:123–131.

    Article  Google Scholar 

  • Fine, J. M., and Sorensen, P. W. 2008. Isolation and biological activity of the multi-component sea lamprey migratory pheromone and new information in its potency. J. Chem. Ecol. 34:1259–1267

    Article  CAS  PubMed  Google Scholar 

  • Friedrich, R. W., and Korsching, S. I. 1998. Chemotopic, combinatorial, and noncombinatorial odorants representations of the olfactory bulb revealed by voltage-sensitive axon tracer. J. Neurosci. 18:87–95.

    Google Scholar 

  • Karlson, P., and Lüscher, M. 1959. “Pheromones”, a new term for a class of biologically active substances. Nature 183:55–56.

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi, M., Sorensen, P. W., and Stacey, N. E. 2002. Hormonal and pheromonal control of spawning in goldfish. Fish Physiol. Biochem. 26:71–84.

    Article  CAS  Google Scholar 

  • Le Martret, M. A., and Saglio, P. 1982. Communication intraspécifique d’origine phéromonale chez le carassin doré immature (Carassius auratus L.). Mise en évidence olfactométrique du phéromone. Biol Behav. 7:41–47.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li, W., Scott, A. P., Siefkes, 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.

    Article  CAS  PubMed  Google Scholar 

  • Liley, N. R. 1982. Chemical communication in fish. Can. J. of Fish. Aquat. Sci. 39:22–35.

    Article  CAS  Google Scholar 

  • Maniak P. J., Lossing, R., and Sorensen, P. W. 2000. Injured Eurasian ruffe, Gymnocephalus cernuss, release an alarm pheromone which may prove useful in their control. J. Great Lakes Res. 26:183–195.

    Article  Google Scholar 

  • Mccrimmon, H. R. 1968. Carp in Canada. Bull Fish. Res, Bd. Can. 165, 93p.

  • Michel, W. C. 2006. Chemoreception, pp. 471–498, in D. H. Evans and J. B. Clairborne (eds.). The Physiology of Fishes, 3rd Ed. CRC Press, Boca Raton, Florida.

    Google Scholar 

  • Olsen, K., Swaski, J. R., and Stacey, N. E. 2006. Endocrine and milt responses of male crucian carp (Carassius carassius L.) to periovulatory females under field conditions. Gen Comp. Endocrinol. 149:249–302.

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Saglio, P., and Blanc, J. M. 1989. Intraspecific chemocommunication in immature goldfish, Carassius auratus L.: attraction in olfactometer to free amino acid fractions from skin extract. Biol. Behav. 14:132–147.

    Google Scholar 

  • Saglio, P., and Le Martinet, M. -A. 1982. Communication intraspecifique d’origine phéromonale chez le carassin doré immature, Carassius auratus L. 2. Etude en olfactomètre de l’activité comportementale d’extraits d’origine épidermique. Biol. Behav. 7:41–54.

    Google Scholar 

  • Scott, A. P., and Sorensen, P. W. 1994. Time course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen. Comp. Endocrin. 96:309–323.

    Article  CAS  Google Scholar 

  • Sisler, S. P., and Sorensen, P. W. 2008. Common carp and goldfish discern conspecific identity using chemical cues. Behaviour 145:1409–1425.

    Article  Google Scholar 

  • Smith, R. J. F. 1992. Alarm signals in fish. Rev. Fish Biol. Fish. 2:33–63.

    Article  Google Scholar 

  • Sorensen, P. W., and Hoye, T. H. 2010. Pheromones in Vertebrates. pp. 225–262, in K Mori (ed.). Volume 4 Chemical Ecology, Comprehensive Natural products Chemistry II: Chemistry and Biology (series editors L.N. Mander; H. Liu). Elsevier Press, U.K.

  • Sorensen, P. W., and Stacey, N. E. 1999. Evolution and specialization of fish hormonal pheromones, pp. 15–47, in R. E. Johnston, D. Muller-Schwarze and P. W. Sorensen (eds.). Advances in Chemical Signals in Vertebrates. Kluwer Academic Plenum Publishers, New York.

    Google Scholar 

  • Sorensen, P. W., and Stacey, N. E. 2004. Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. N.Z. J. Mar. Freshwater Res. 38:399–417.

    Article  CAS  Google Scholar 

  • Sorensen, P.W., Hara, T. J., and Stacey, N. E. 1987. Extreme olfactory sensitivity of mature and gonadally-regressed goldfish to 17α,20β-dihydroxy-4-pregnen-3-one, a potent steroidal pheromone. J. Comp. Physiol. A 160: 05–313.

    Article  CAS  Google Scholar 

  • Sorensen, P. W., Irvine, I. A. S., Scott, A. P., and Stacey, N. E. 1992. Electrophysiological measures of olfactory sensitivity suggest that goldfish and other fish use species-specific mixtures of hormones and their metabolites as sex pheromones, pp. 357–364 in R. L. Doty and D. Muller-Schwarze (eds.). Chemical Signals in Vertebrates VI, Plenum Press, New York.

    Google Scholar 

  • Sorensen, P. W., Scott, A. P., and Kihslinger, R. L. 2000. How common hormonal metabolites function as specific pheromones in the goldfish. pp. 125–129 in: B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson, and S.O. Stefansson (eds.). Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. Bergen, Norway.

    Google Scholar 

  • Sorensen, P. W., Pinollis, M., and Scott, A. P. 2005. Sexually mature male goldfish release large quantities of androstenedione to the water where it functions as a pheromone. Gen. Comp. Endocrin. 140:164–175.

    Article  CAS  Google Scholar 

  • Stacey, N. E., and Sorensen, P. W. 2005. Reproductive pheromones, pp. 359–412, in K. A. Sloman, R. W. Wilson, S. Balshine (eds.). Physiology and Behaviour of Fish, vol 24 in Fish Physiology Series, A. Farrell and C.J. Brauner (senior eds.). Academic Press, San Diego, California.

  • Stacey, N. E., and Sorensen, P. W. 2009. Hormonal pheromones in fish. Volume 2, pp.639–681, in D. W. Pfaff, A. P. Arnoldf, A. Eitgen, S, Frabach and R, Rubin (eds.). Hormones, Brain and Behavior, 2ed., Elsevier Press, San Diego.

  • Stacey, N. E., Kyle, A. L., and Liley, N. R. 1986. Fish reproductive pheromones, pp. 117–134, in D. Duvall, D. Muller-Schwarze and R. M. Silverstein (eds.). Chemical Signals in Vertebrates 4, Plenum Press, New York.

    Google Scholar 

  • Tammar, A. R. 1974. Bile salts in fishes. Chem. Zool. 8:595–611.

    CAS  Google Scholar 

  • Wyatt, T. D. 2003. Pheromones and Animal Behavior. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Wyatt, T. D. 2009. Fifty years of pheromones, Nature 457:262–3.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was funded by the Minnesota Environment and Natural Resources Trust Fund. We thank Mario Travaline for his help. Two anonymous reviewers and Drs. Bajer and Lim kindly reviewed and commented on the manuscript

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Author notes

  1. Christine N. Polkinghorne

    Present address: Natural Sciences Department, University of Wisconsin, Superior, WI, 54880, USA

Authors and Affiliations

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

    Haude M. Levesque, Donelle Scaffidi, Christine N. Polkinghorne & Peter W. Sorensen

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  1. Haude M. Levesque
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  2. Donelle Scaffidi
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  3. Christine N. Polkinghorne
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  4. Peter W. Sorensen
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Correspondence to Peter W. Sorensen.

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Levesque, H.M., Scaffidi, D., Polkinghorne, C.N. et al. A Multi-Component Species Identifying Pheromone in the Goldfish. J Chem Ecol 37, 219–227 (2011). https://doi.org/10.1007/s10886-011-9907-6

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  • DOI: https://doi.org/10.1007/s10886-011-9907-6

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