Endocrine and milt responses of male crucian carp (Carassius carassius L.) to periovulatory females under field conditions

General and Comparative Endocrinology

Volumn 149, Issue 3, 2006, Pages 294-302

  Olsen K H ^a   Sawisky, G R ^b   Stacey, N E ^b  

^a School of Life Sciences Södertörn University   (Sweden)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Carassius carassius; Crucian carp; Fish; LH; Milt; Ovaprim; Ovulation; Sperm allocation; Sperm competition

Indexed keywords

LUTEINIZING HORMONE; PHEROMONE; STEROID 4 PREGNEN 17,20BETA DIOL 3 ONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL REPRODUCTIVE PROCEDURES; ARTICLE; BLOOD SAMPLING; CARP; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOCRINE SYSTEM; ENVIRONMENTAL TEMPERATURE; FEMALE; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; MALE; MILT; NONHUMAN; OVULATION; PHOTOPERIODICITY; POND; PRIORITY JOURNAL; SEASONAL VARIATION; SEMINAL PLASMA; SEXUAL BEHAVIOR; SPAWNING; SPERM; SPERM COMPETITION; STEROID RELEASE; SWEDEN;

EID: 33750708251     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2006.06.011     Document Type: Article

References (61)

1. Aho J., and Holopainen I.J. Batch spawning of crucian carp Carassius carassius (L.) in mono- and multispecies communities. Ann. Zool. Fennici 37 (2000) 101-111
2. Bjerselius R., and Olsén K.H. A study of the olfactory sensitivity of crucian carp (Carassius carassius) and goldfish (Carassius auratus) to 17α,20β-dihydroxyprogesterone and prostaglandin F2α. Chem. Senses 18 (1993) 427-436
3. Bjerselius R., Olsén K.H., and Zheng W. Endocrine, gonadal and behavioral responses of male crucian carp (Carassius carassius) to the hormonal pheromone 17α,20β-dihydroxy-4-pregnen-3-one. Chem. Senses 20 (1995) 221-230
4. Bjerselius, R, Li, W., Sorensen, P.W., Scott, A.P., 1996. Spermiated male sea lamprey release a potent sex pheromone: In: Thomas, P., Goetz, F. (Eds.), Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish, Austin, TX, p. 271.
5. Breder C.M., and Rosen D.E. Modes of Reproduction in Fishes (1966), Natural History Press, Garden City, New York
6. Cardwell J.R., and Stacey N.E. Hormonal sex pheromones in characiform fishes: an evolutionary case study. In: Canário A.V.M., and Power D.M. (Eds). Fish Pheromones: Origins and Modes of Action (1995), University of Algarve Press, Faro, Portugal 47-55
7. Cardwell J.R., Stacey N.E., Tan E.S.P., McAdam D.S.O., and Lang S.L.C. Androgen increases olfactory receptor response to a vertebrate sex pheromone. J. Comp. Physiol. A 176 (1995) 55-61
8. Cole T.B., and Stacey N.E. Olfactory responses to steroids in an African mouth-brooding cichlid Haplochromis burtoni (Günther). J. Fish Biol. 68 (2006) 661-680
9. Colombo L., Marconato A., Belvedere P.C., and Frisco C. Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Boll. Zool. 47 (1980) 355-364
10. Døving K. Evolutionary trends in olfaction. In: Benz G. (Ed). The Structure-Activity Relationships in Olfaction (1976), IRL Press, London 149-159
11. Dulka J.G., Stacey N.E., Sorensen P.W., and Van Der Kraak G.J. A sex steroid pheromone synchronizes male-female spawning readiness in goldfish. Nature 325 (1987) 251-253
12. Hamdani E.H., and Døving K. Specific projection of the olfactory crypt cells in the olfactory system in crucian carp, Carassius carassius. Chem. Senses 31 (2006) 63-67
13. Hänfling B., Bolton P., Harley M.M., and Carvalho G.R. A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius spp. and Cyprinus carpio). Freshw. Biol. 50 (2005) 403-417
14. Irvine I.A.S., and Sorensen P.W. Acute olfactory sensitivity of wild common carp, Cyprinus carpio, to goldfish sex pheromones is influenced by gonadal maturity. Can. J. Zool. 71 (1993) 2199-2210
15. Johnson N.S., Siefkes M.J., and Li W. Capture of ovulating female sea lampreys in traps baited with spermiating male sea lampreys. N. Am. J. Fish. Manag. 25 (2005) 67-72
16. Kitamura S., Ogata H., and Takashima F. Activities of F-type prostaglandins as releaser sex pheromones in cobitide loach, Misgurnus anguillicaudatus. Comp. Biochem. Physiol. A 107 (1994) 161-169
17. Kitamura S., Ogata H., and Takashima F. Olfactory responses of several species of teleost to F-prostaglandins. Comp. Biochem. Physiol. A 107 (1994) 463-467
18. Kobayashi M., Sorensen P.W., and Stacey N.E. Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol. Biochem. 26 (2002) 71-84
19. Laberge F., and Hara T.J. Behavioral and electrophysiological responses to F-prostaglandins, putative spawning pheromones, in three salmonid fishes. J. Fish Biol. 62 (2003) 206-221
20. Lastein S., Hamdani E.L., and Døving K. Gender distinction in neural discrimination of sex pheromones in the olfactory bulb of crucian carp, Carassius carassius. Chem. Senses 31 (2006) 69-77
21. Lelek A. The Freshwater Fishes of Europe, Threatened Fishes of Europe vol. 9 (1987), AULA-Verlag, Weisbaden
22. Li W., Scott A.P., Siefkes M.J., Yan H.G., Liu Q., Yun S.S., and Gage D.A. Bile acid secreted by male sea lamprey that acts as a sex pheromone. Science 296 (2002) 138-141
23. Liley N.R. Chemical communication in fish. Can. J. Fish. Aquat. Sci. 39 (1982) 22-35
24. Liley N.R., Olsén K.H., Foote C.J., and Van Der Kraak G.J. Endocrine changes associated with spawning behavior in male kokanee salmon (Oncorhynchus nerka) and the effects of anosmia. Horm. Behav. 27 (1993) 470-487
25. Lower N., Scott A.P., and Moore A. Release of sex steroids into the water by roach. J. Fish Biol. 64 (2004) 16-33
26. McBride R.S., Stengard F.J., and Mahmoudi B. Maturation and diel reproductive periodicity of round scad (Carangidae: Decapterus punctatus). Mar. Biol. 140 (2002) 713-722
27. Moore A., and Waring C.P. Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male Atlantic salmon (Salmo salar) parr. J. Exp. Biol. 199 (1996) 2307-2316
28. Moore A., Olsén K.H., Lower N., and Kindahl H. The role of F-series prostaglandins as reproductive priming pheromones in the brown trout (Salmo trutta L.). J. Fish Biol. 60 (2002) 613-624
29. Murphy C.A., Stacey N., and Corkum L.D. Putative steroidal pheromones in the round goby, Neogobius melanostomus: olfactory and behavioral responses. J. Chem. Ecol. 27 (2001) 443-470
30. Narayanan A., and Stacey N.E. Olfactory responses to putative steroidal pheromones in allopatric and sympatric species of mochokid catfish. Fish Physiol. Biochem. 28 (2003) 275-276
31. Neat F.C. Male parasitic spawning in two species of triplefin blenny (Tripterigiidae): contrasts in demography, behaviour and gonadal characteristics. Env. Biol. Fishes 61 (2001) 57-64
32. Neff B.D., Fu P., and Gross M.R. Sperm investment and alternative mating tactics in bluegill sunfish (Lepomus macrochirus). Behav. Ecol. 14 (2003) 634-641
33. Oliveira R.F., Goncalves E.J., and Santos R.S. Gonadal investment of young males in two blenniid species with alternative mating tactics. J. Fish Biol. 59 (2001) 459-462
34. Olsén K.H., and Liley N.R. The significance of olfaction and social cues in milt availability, sexual hormone status and spawning behaviour of male rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 89 (1993) 107-118
35. Olsén K.H., Bjerselius R., Mayer I., and Kindahl H. Both ovarian fluid and female urine increase sex steroid levels in mature Atlantic salmon (Salmo salar L.) male parr. J. Chem. Ecol. 27 (2001) 2337-2349
36. Olsén K.H., Johanssen A.-K., Bjerselius R., Mayer I., and Kindahl H. Mature Atlantic salmon (Salmo salar L.) male parr are attracted to ovulated female urine but not ovarian fluid. J. Chem. Ecol. 28 (2002) 29-40
37. Pinheiro M.F.M., de Souza S.M.G., and Barcellos L.J.G. Exposure to 17α,20β-dihydroxy-4- pregnen-3-one changes seminal characteristics in Nile tilapia, Oreochromis niloticus. Aquacult. Res. 34 (2003) 1047-1052
38. Pinillos M.L., Guijarro A.I., Delgado M.J., Hubbard P.C., Canário A.V.M., and Scott A.P. Production, release, and olfactory detection of sex steroids by the tench (Tinca tinca L.). Fish Physiol. Biochem. 26 (2002) 197-210
39. Poling K.R., Fraser E.J., and Sorensen P.W. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp. Biochem. Physiol. B 129 (2001) 645-651
40. Scott J.W., and Scott-Johnson P.E. The electroolfactogram: a review of its history and uses. Mic. Res. Tech. 58 (2002) 152-160
41. Scott A.P., Liley N.R., and Vermeirssen E.L.M. 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 (1994) 131-147
42. Sorensen P.W., Hara T.J., Stacey N.E., and Goetz F.W. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39 (1988) 1039-1050
43. Sorensen P.W., Scott A.P., Stacey N.E., and Bowdin L. Sulfated 17α,20β-dihydroxy-4- pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. Endocrinol. 100 (1995) 128-142
44. Sorensen P.W., Pinillos M., and Scott A.P. Sexually mature male goldfish release large quantities of androstenedione into the water where it functions as a pheromone. Gen. Comp. Endocrinol. 140 (2005) 164-175
45. Stacey N.E., and Sorensen P.W. Fish hormonal pheromones. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain, and Behavior Vol. 2 (2002), Academic Press, New York 375-435
46. Stacey N.E., and Sorensen P.W. Reproductive pheromones. In: Sloman K.A., Wilson R.W., and Balshine S. (Eds). Behavior and Physiology of Fish (2006), Elsevier Press, Amsterdam 359-412
47. Stacey N.E., Cook A.F., and Peter R.E. Spontaneous and gonadotropin-induced ovulation in the goldfish, Carassius auratus L.: effects of external factors. J. Fish Biol. 15 (1979) 349-361
48. Stacey N.E., Cook A.F., and Peter R.E. Ovulatory surge of gonadotropin in the goldfish, Carassius auratus. Gen. Comp. Endocrinol. 37 (1979) 246-249
49. Stacey N.E., Kyle A.L., and Liley N.R. Fish reproductive pheromones. In: Duvall D., Muller-Schwarze D., and Silverstein R.M. (Eds). Chemical Signals in Vertebrates vol. 4 (1986), Plenum Press, New York 117-133
50. Stacey N.E., Sorensen P.W., Van Der Kraak G.J., and Dulka J.G. Direct evidence that 17α,20β- dihydroxy-4-pregnen-3-one functions as a goldfish primer pheromone: preovulatory release is closely associated with male endocrine responses. Gen. Comp. Endocrinol. 75 (1989) 62-70
51. Stacey N.E., Zheng W.B., and Cardwell J.R. Milt production in common carp (Cyprinus carpio): stimulation by a goldfish steroid pheromone. Aquaculture 127 (1994) 265-276
52. Stockley P., Gage M.J.G., Parker G.A., and Møller A.P. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Amer. Natural. 149 (1997) 933-954
53. Sveinsson T., and Hara T.J. Mature males of Arctic char, Salvelinus alpinus, release F-type prostaglandins to attract conspecific mature females and stimulate their spawning behaviour. Environ. Biol. Fishes 42 (1995) 253-266
54. Sveinsson T., and Hara T.J. Olfactory sensitivity and specificity of arctic char, Salvelinus alpinus, to a putative male pheromone, prostaglandin F2α. Physiol. Behav. 69 (2000) 301-307
55. Taborsky M. The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J. Hered. 92 (2001) 100-110
56. Van Den Hurk R., and Lambert J.G.D. Ovarian steroid glucuronides function as sex pheromones for male zebrafish, Brachydanio rerio. Canad. J. Zool. 61 (1983) 2381-2387
57. Van Der Kraak G.J., Suzuki K., Peter R.E., Itoh H., and Kawauchi H. Properties of common carp gonadotropin I and gonadotropin II. Gen. Comp. Endocrinol. 85 (1992) 217-229
58. Waring C.P., and Moore A. Sublethal effects of a carbamate pesticide on pheromonal mediated endocrine function in mature male Atlantic salmon (Salmo salar L.) parr. Fish. Physiol. Behav. 17 (1997) 203-211
59. Zheng W., and Stacey N.E. Two mechanisms for increasing milt volume in male goldfish. J. Exp. Zool. 276 (1996) 287-295
60. Zheng W., and Stacey N.E. A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfish (Carassius auratus). Gen. Comp. Endocrinol. 105 (1997) 228-235
61. Zheng W., Strobeck C., and Stacey N.E. The steroid pheromone 17α,20β-dihydroxy-4- pregnen-3-one increases fertility and paternity in goldfish. J. Exp. Biol. 200 (1997) 2833-2840