Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male atlantic salmon (Salmo salar) parr

Journal of Experimental Biology

Volumn 199, Issue 10, 1996, Pages 2307-2316

  Moore, Andrew ^a   Waring, Colin P ^b  

^a CENTRE FOR ENVIRONMENT   (United Kingdom)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

Atlantic salmon; olfa ction; pheromone; physiology; prostaglandins; reproduction; Salmo salar; urine

Indexed keywords

SALMO SALAR; SALMONIDAE; VISCUM ALBUM;

EID: 0030443038     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (54)

1. ABDULLAH, M. A. S. AND KIME, D. E. (1994). Increased substrate concentration causes a shift from production of 11-oxygenated androgens to 17,20-dihydroxyprogestogens during the in vitro metabolism of 17-hydroxyprogesterone by goldfish testes. Gen. comp. Endocr. 96, 129-139.
2. BARRY, T. P., AIDA, K., OKUMURA, T. AND HANYU, I. (1990). The shift from C-19 to C-21 steroid synthesis in spawning male common carp, Cyprinus carpio, is regulated by the inhibition of androgen production by progestogens produced by spermatozoa. Biol. Reprod. 43, 105-112.
3. 2a. Chem. Senses 18, 427-436.
4. CAPRIO, J. AND BYRD, R. P. (1984). Electrophysiological evidence for acidic, basic and neutral amino acid olfactory receptor sites in catfish. J. gen. Physiol. 84, 403-422.
5. CARDWELL, J. R., DULKA, J. G. AND STACEY, N. E. (1991). Species-specificity of olfactory responsiveness to potential sex pheromones. In Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish (ed. A. P. Scott, J. P. Sumpter, D. E. Kime and M. S. Rolfe), p. 201. Sheffield: FishSymp 91.
6. CARDWELL, J. R., DULKA, J. G. AND STACEY, N. E. (1992). Acute olfactory sensitivity to prostaglandins but not to gonadal steroids in two sympatric species of Catastomus (Pisces: Cypriniformes). Can. J. Zool. 19, 1897-1903.
7. CARDWELL, J. R., STACEY, N. E., TAN, E. S. P., MCADAM, D. S. O. AND LANG, S. L. C. (1995). Androgen increases olfactory receptor response to a vertebrate sex pheromone. J. comp. Physiol. A 176, 55-61.
8. COLOMBO, L., MARCONATO, A., BELVEDERE, P. C. AND FRISO, C. (1980). Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Boll. Zool. 47, 355-364.
9. EDDY, F. B. AND TALBOT, C. (1985). Urine production in smoking Atlantic salmon, Salmo salar L. Aquaculture 45, 67-72.
10. EVANS, R. E. AND HARA, T. J. (1985). The characteristics of the electro-olfactogram (EOG): its loss and recovery following olfactory nerve section in the rainbow trout (Oncorhynchus mykiss). Brain Res. 330, 65-75.
11. GOETZ, F. W., DUMAN, P., RANJAN, M. AND HERMAN, C. A. (1989). Prostaglandin F and E synthesis by specific tissue compartments of the brook trout (Salvelinus fontinalis) ovary. J. exp. Zool. 250, 196-205.
12. HARA, T. J. (1994). The diversity of chemical stimulation in fish olfaction and gustation. Rev. Fish Biol Fish. 4, 1-35.
13. HONDA, H. (1980). Female sex pheromone of rainbow trout, Salmo gairdneri, involved in courtship behaviour. Bull. Jap. Soc. scient. Fish. 46, 1109-1112.
14. HONDA, H. (1982). On the female sex pheromones and courtship behaviour in the salmonids, Oncorhynchus masou and O. rhodurus. Bull. Jap. Soc. scient. Fish. 48, 47-49.
15. IRVINE, I. A. S. AND SORENSEN, P. W. (1993). Acute olfactory sensitivity of wild common carp, Cyprinus carpio, to goldfish hormonal sex pheromones is influenced by gonadal maturity. Can. J. Zool. 71, 2199-2210.
16. KARLSON, P. AND LUSCHER, M. (1959). 'Pheromones': a new term for a class of biologically active substances. Nature 183, 55-56.
17. KITAMURA, S., OGATA, H. AND TAKASHIMA, F. (1994). Olfactory responses of several species of teleost to F-prostaglandins. Comp. Biochem. Physiol. 107A, 463-467.
18. LILEY, N. R., OLSEN, K. H., FOOTE, C. J. AND VAN DER KRAAK, G. J. (1993). Endocrine changes associated with spawning behaviour in male Kokanee salmon (Oncorhynchus nerka) and the effects of anosmia. Horm. Behav. 27, 470-487.
19. MOORE, A. (1994). An electrophysiological study on the effects of pH on olfaction in mature male Atlantic salmon (Salmo salar) parr. J. Fish Biol. 45, 493-502.
20. MOORE, A., IVES, M. J. AND KELL, L. T. (1994). The role of urine in sibling recognition in Atlantic salmon (Salmo salar L.) parr. Proc. R. Soc. Lond. B 255, 173-180.
21. MOORE, A. AND SCOTT, A. P. (1991). Testosterone is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr. Phil. Trans. R. Soc. Lond. B 332, 241-244.
22. MOORE, A. AND SCOTT, A. P. (1992). 17α,20β-dihydroxy-4-pregenen-3-one 20-sulphate is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr which have been pre-exposed to the urine of ovulated females. Proc. R. Soc. Lond. B 249, 205-209.
23. MOORE, A. AND WARING, C. P. (1995). Seasonal changes in olfactory sensitivity of mature male Atlantic salmon (Salmo salar L.) parr to prostaglandins. In Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish (ed. F. W. Goetz and P. Thomas), p. 273. FishSymp 95.
24. MOORE, A. AND WARING, C. P. (1996). Sub-lethal effects of the pesticide Diazinon on olfactory function in mature male Atlantic salmon parr. J. Fish Biol. 48, 758-775.
25. NEVITT, G. A., DITTMAN, A. H., QUINN, T. P. AND MOODY, W. J., JR (1994). Evidence for a peripheral olfactory memory in imprinted salmon. Proc. natn. Acad. Sci. U.S.A. 91, 4288-4292.
26. NEVITT, G. A., GROBER, M. S., MARCHATERRE, M. A. AND BASS, A. H. (1995). GnRH-like immunoreactivity in the peripheral olfactory system and forebrain of Atlantic salmon (Salmo salar): a reassessment at multiple life history stages. Brain Behav. Evol. 45, 350-358.
27. OLSEN, K. H. AND LILEY, N. R. (1993). The significance of olfaction and social cues in milt availability, sexual hormone status and spawning behaviour of male rainbow trout (Oncorhynchus mykiss). Gen. comp. Endocr. 89, 107-118.
28. POWELL, W. S. (1982). Rapid extraction of arachidonic acid metabolites from biological samples using octadecylsilyl silica. In Methods in Enzymology, vol. 86 (ed. W. E. M. Lands and W. L. Smith), pp. 467-477. New York, London: Academic Press.
29. RESINK, J. W., VOORTHUIS, P. K., VAN DEN HURK, R., PETERS, R. C. AND VAN OORDT, W. J. (1989). Steroid glucuronides of the seminal vesicles as olfactory stimuli in African catfish, Clarias gariepinus. Aquaculture 83, 153-166.
30. SAKAI, N., UEDA, H., SUZUKI, N. AND NAGAHAMA. Y. (1989). Steroid production by Amago salmon (Oncorhynchus rhodurus) testes at different developmental stages. Gen. comp. Endocr. 75, 231-240.
31. SCOTT, A. P. AND LILEY, N. R. (1994). Dynamics of excretion of 17α,20β-dihydroxy-4-pregenen-3-one 20-sulphate and of the glucuronides of testosterone and 17β-Oestradiol, by urine of reproductively mature male and female rainbow trout (Oncorhynchus mykiss). J. Fish Biol. 44, 117-129.
32. SCOTT, A. P., LILEY, N. R. AND VERMIERRSSEN, E. L. M. (1994). Urine of reproductively mature female rainbow trout, Oncorhynchus mykiss (Walbaum), contains a priming pheromone which enhances plasma levels of sex steroids and gonadotrophin II in males. J. Fish Biol. 44, 131-147.
33. SCOTT, A. P., MACKENZIE, D. S. AND STACEY, N. E. (1984). Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. II. Steroid hormones. Gen. comp. Endocr. 56, 349-359.
34. SCOTT, A. P., SHELDRICK, E. L. AND FLINT, A. P. F. (1982). Measurement of 17α,20β-dihydroxy-4-pregnen-3-one in plasma of trout (Salmo gairdneri Richardson): seasonal changes and response to salmon pituitary extract. Gen. comp. Endocr. 46, 444-451.
35. SCOTT, A. P. AND SORENSEN, P. W. (1995). Time course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen. comp. Endocr. 96, 309-323.
36. SCOTT, A. P. AND SUMPTER, J. P. (1989). Seasonal variations in testicular germ cell stages and in plasma concentrations of sex steroids in male rainbow trout (Salmo gairdneri) maturing at 2 years old. Gen. comp. Endocr. 73, 46-58.
37. SORENSEN, P. W. (1992). Hormones, pheromones and chemoreception. In Fish Chemoreception (ed. T. J. Hara), pp. 199-228. London: Chapman & Hall.
38. SORENSEN, P. W. AND GOETZ, F. W. (1993). Pheromonal and reproductive function of F prostaglandins and their metabolites in teleost fish. J. Lipid Mediat. 6, 385-393.
39. SORENSEN, P. W., GOETZ, F. W., SCOTT, A. P. AND STAGEY, N. E. (199Ia). Recent studies indicate that goldfish use mixtures of unmodified hormones and hormonal metabolites as sex pheromones. In Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish (ed. A. P. Scott, J. P. Sumpter, D. E. Kime and M. S. Rolfe), pp. 191-193. Sheffield: FishSymp 91.
40. SORENSEN, P. W., HARA, T. J. AND STACEY, N. E. (1987). Extreme olfactory sensitivity of mature and gonadally-regressed goldfish to a potent steroidal pheromone, 17α,20β;-dihydroxy-4-pregnen-3-one. J. comp. Physiol. A 160, 305-313.
41. SORENSEN, P. W., HARA, T. J., STACEY, N. E. AND DULKA, J. G. (1990). Extreme olfactory specificity of male goldfish to the preovulatory steroidal pheromone, 17α,20β-dihydroxy-4-pregnen-3-one. J. comp. Physiol. A 166, 373-383.
42. SORENSEN, P. W., HARA, T. J., STACEY, N. E. AND GOETZ, F. W. (1988). F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39, 1039-1050.
43. SORENSEN, P. W., IRVINE, I. A., SCOTT, A. P. AND STACEY, N. E. (19916). Electrophysiological measures of olfactory sensitivity suggest that goldfish and other species use species-specific mixtures of hormones and their metabolites as sex pheromones. In Chemical in Vertebrates (ed. R. Doty and D. Muller-Schwarze), pp. 357-364. New York: Plenum Press.
44. SORENSEN, P. W., SCOTT, A. P., STACEY, N. E. AND BOWDIN, L. (1995). Sulfated 17α,20β-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulent with pheromonal actions in the goldfish. Gen. comp. Endocr. 100, 128-142.
45. SORENSEN, P. W. AND STACEY, N. E. (1990). Identified hormonal pheromones in the goldfish: a model for sex pheromone function in teleost fish. In Chemical Signals in Vertebrates, vol. V (ed. D. W. MacDonald, D. Muller-Schwarze and S. E. Natynczuk), pp. 302-314. Oxford: Oxford University Press.
46. SORENSEN, P. W., STACEY, N. E. AND CHAMBERLAIN, K. J. (1989). Differing behavioural and endocrinological effects of two female sex pheromones on male goldfish. Harm. Behav. 23, 317-332.
47. STACEY, N. E. (1987). Roles of hormones and pheromones in fish reproductive behaviour. In Psychobiology of Reproductive Behaviour (ed. D. Crews), pp. 28-69. New York: Prentice-Hall
48. STACEY, N. E., CARDWELL, J. R., LILEY, N. R., SCOTT, A. P. AND SORENSEN, P. W. (1994). Hormones as sex pheromones in fish. In Perspectives in Comparative Endocrinology (ed. K. G. Davey, R. E. Peter and S. S. Tobe), pp. 438-448. Ottawa: National Research Council of Canada.
49. STACEY, N. E., KYLE, A. L. AND LILEY, N. R. (1986). Fish reproductive pheromones. In Chemical Signals in Vertebrates, vol. IV (ed. D. Duvall, D. Muller-Schwarze and R. M. Silverstein), pp. 119-133. New York: Plenum Press.
50. STACEY, N. E. AND SORENSEN, P. W. (1991). Function and evolution of fish hormonal pheromones. In Biochemistry and Molecular Biology of Fishes, vol. I (ed. P. W. Hochachka and T. P. Mommsen), pp. 109-134. New York: Elsevier.
51. STACEY, N. E., SORENSEN, P. W., VAN DER KRAAK, G. J. AND DULKA, J. G. (1989). Direct evidence that 17α,20β-dihydroxy-4-pregenen-3-one functions as a goldfish primer pheromone: preovulatory release is closely associated with male endocrine responses. Gen. comp. Endocr. 75, 62-70.
52. SVEINSSON, T. AND HARA, T. J. (1995). Mature males of Arctic charr, Salvelinus alpinus, release F-type prostaglandins to attract con-specific females and stimulate their spawning behaviour. Env. Biol. Fish. 42, 253-266.
53. WARING, C. P. AND MOORE, A. (1995). F-series prostaglandins have a pheromonal priming effect on mature male Atlantic salmon (Salmo salar) parr. In Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish (ed. F. W. Goetz and P. Thomas), p. 255. FishSymp 95.
54. WARING, C. P., MOORE, A. AND SCOTT, A. P. (1996). Milt and endocrine responses of mature male Atlantic salmon (Salmo salar L.) parr to water-borne testosterone, 17,20β-dihydroxy-4-pregnen-3-one 20-sulfate and the urines from adult female and male salmon. Gen. comp. Endocr. (in press).