Advertisement

Salmonid Reproductive Migration and Effects on Sexual Maturation

  • Kazufumi Hayashida
  • Kosuke Fukaya
  • Arjan P. Palstra
  • Hiroshi Ueda
Chapter

Abstract

Salmon has amazing abilities to migrate long distances from the ocean to their natal streams for reproduction. Reproductive homing migration was investigated by two different research approaches from behavioural biology to endocrinology using chum salmon in the north Pacific Ocean as well as two land-locked salmon species. These species are lacustrine sockeye and masu salmon in Lake Toya and Lake Shikotsu, Hokkaido, Japan where the lakes serve as a model “ocean”. Physiological biotelemetry techniques were applied to examine the homing behaviours of adult chum salmon from the Bering Sea to Hokkaido as well as lacustrine sockeye and masu salmon in Lake Toya, and revealed that salmon can navigate in open water using different sensory systems. The hormone profiles in the brain–pituitary–gonadal (BPG) axis were investigated in chum salmon and lacustrine sockeye salmon during their homing migration, and clarified that salmon gonadotropin-releasing hormone (sGnRH) plays leading roles on homing migration. The interaction between metabolism and sexual maturation under exercise, as experienced during the salmonid anorexic reproductive migration, has been studied by swimming the facultative migrant rainbow trout in a large swim flume. RNA sequencing of the red and white muscle transcriptome and microarray analysis of the ovary has been performed to identify hormonal and metabolic actors that are important in switching from the growth phase to the migration phenotype. Olfaction of spawning ground specific smell is suggested as switch from the navigating migration to the sexual maturation phenotype.

Keywords

Rainbow Trout Sexual Maturation Chum Salmon Sockeye Salmon Masu Salmon 
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.

Notes

Acknowledgments

We would like to express our sincerely gratitude those who have carried out collaborative researches: M. Kaeriyama, H. Tanaka, Y. Naito, S. Urawa, N. Davis, M. Fukuwaka, JBK Leonard, H. Nii, Y Makiguchi, A. Sato, K. Orito, Y. Konno, K. Miyoshi, National Salmon Center, Hokkaido Fish Hatchery, Hokkaido Farming Fisheries Promotion Corporation, and Chitose Salmon Aquarium for the behavioural study; A. Urano, K. Amano, M. Iwata, S. Adachi, H. Ando, H. Yamada, H. Kudo, MM. Zerihun, RK. Bhandari, M. Fukaya, N. Kozu, T. Kitani, S. Matsumoto, S. Taniyama for the endocrinological study. The present study was supported in part by Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, from the Japan Society for the promotion of Science (JSPS), from the Hokkaido Foundation for the Promotion of Scientific and Industrial Technology, from the Mitsubishi Foundation, from the Mitsui & Co. Ltd, and from the Hokkaido University to HU. AP would specifically like to thank J. Planas, Y. Zohar, G. van den Thillart and F. Sibbing. AP was supported by a Marie Curie Intra-European Fellowship from the European Commission (REPRO-SWIM) with Grant Agreement number 219971 (with J. Planas), a FY2011 JSPS Invitation Fellowship for research in Japan by the Japan Society for the Promotion of Science (No. S-11097 with H. Ueda) and by IMARES.

References

  1. Amano M, Urano A, Aida K (1997) Distribution and function of gonadotropin-releasing hormone (GnRH) in the teleost brain. Zool Sci 14:1–11PubMedCrossRefGoogle Scholar
  2. Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trend Ecol Evol 19:334–343CrossRefGoogle Scholar
  3. Dittman AW, Quinn TP (1996) Homing in pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91PubMedGoogle Scholar
  4. Evans TG, Hammill E, Kaukinen K, Schulze AD, Patterson DA, English KK, Curtis JM, Miller KM (2011) Transcriptomics of environmental acclimatization and survival in wild adult Pacific sockeye salmon (Oncorhynchus nerka) during spawning migration. Mol Ecol. doi: 10.1111/j.1365-294X.2011.05276.x Google Scholar
  5. Flores A-M, Shrimpton JM, Patterson DA, Hills JA, Cooke SJ, Yada T, Moriyama S, Hinch SG, Farrell AP (2011) Physiological and molecular endocrine changes in maturing wild sockeye salmon, Oncorhynchus nerka, during ocean and river migration. J Comp Physiol B. doi: 10.1007/s00360-011-0600-4 PubMedGoogle Scholar
  6. Hino H, Iwai T, Yamashita M, Ueda H (2007) Identification of an olfactory imprinting-related gene in the lacustrine sockeye salmon, Oncorhynchus nerka. Aquaculture 273:200–208CrossRefGoogle Scholar
  7. Kaeriyama M, Ueda H (1998) Life history strategy and migration pattern of juvenile sockeye (Oncorhynchus nerka) and chum salmon (O. keta) in Japan: a review. NPAFC Bull 1:163–171Google Scholar
  8. Kitahashi T, Sato A, Alok D, Kaeriyama M, Zohar Y, Yamauchi K, Urano A, Ueda H (1998) Gonadotropin-releasing hormone analog and sex steroids shorten homing duration of sockeye salmon in Lake Shikotsu. Zool Sci 15:767–771CrossRefGoogle Scholar
  9. Kudo H, Ueda H, Kawamura H, Aida K, Yamauchi K (1994) Ultrastructural demonstration of salmon-type gonadotropin-releasing hormone in the olfactory system of masu salmon (Oncorhynchus masou). Neurosci Lett 166:187–190PubMedCrossRefGoogle Scholar
  10. Kudo H, Hyodo S, Ueda H, Hiroi O, Aida K, Urano A, Yamauchi K (1996) Cytophysiology of gonadotropin-releasing-hormone neurons in chum salmon (Oncorhynchus keta) forebrain before and after upstream migration. Cell Tissue Res 284:261–267PubMedCrossRefGoogle Scholar
  11. Kudo H, Ueda H, Mochida K, Adachi S, Hara A, Nagasawa H, Doi Y, Fujimoto S and Yamauchi K (1999) Salmonid olfactory system-specific protein (N24) exhibits glutathione S-transferase class pi-like structure. J Neurochem 72:1344–1352Google Scholar
  12. Kudo H, Doi Y, Ueda H and Kaeriyama M (2009) Molecular characterization and histochemical demonstration of salmon olfactory marker protein in the olfactory epithelium of lacustrine sockeye salmon (Oncorhynchus nerka). Comp Biochem Physiol 154A:142–150Google Scholar
  13. Lundqvist H, Borg B, Berglund I (1989) Androgens impair seawater adaptability in smolting Baltic salmon (Salmo salar). Can J Zool 67:1733–1736CrossRefGoogle Scholar
  14. Makino K, Onuma T, Kitahashi T, Ando H, Ban M, Urano A (2007) Expression of hormone genes and osmoregulation in homing chum salmon: a minireview. Gen Comp Endocrinol 152:304–309PubMedCrossRefGoogle Scholar
  15. McCormick SD, Naiman RJ (1985) Hypoosmoregulation in an anadromous teleost: influence of sex and maturation. J Exp Zool 234:193–198PubMedCrossRefGoogle Scholar
  16. Miller KM, Schulze AD, Ginther N, Li S, Patterson DA, Farrell AP, Hinch SG (2009) Salmon spawning migration: metabolic shifts and environmental triggers. Comp Biochem Physiol 4D:75–89Google Scholar
  17. Morinishi F, Shiga T, Suzuki N, Ueda H (2007) Cloning and characterization of an odorant receptor in five Pacific salmon. Comp Biochem Physiol 148B:329–336Google Scholar
  18. Nagahama Y (1999) Gonadal steroid hormones: Major regulators of gonadal differentiation and gametogenesis in fish. In: Norberg B, Kjesbu OS Taranger GL, Andersson E, Stefansson SO (eds) Proceedings of the 6th international symposium on the reproductive physiology of fish, Bergen, pp 211–222Google Scholar
  19. Onuma TA, Sato S, Katsumata H, Makino K, Hu WW, Jodo A, Davis ND, Dickey JT, Ban M, Ando H, Fukuwaka M, Azumaya T, Swanson P, Urano A (2009a) Activity of the pituitary-gonadal axis is increased prior to the onset of spawning migration of chum salmon. J Exp Biol 212:56–70PubMedCrossRefGoogle Scholar
  20. Onuma TA, Makino K, Ban M, Ando H, Fukuwaka M, Azumaya T, Swanson P, Urano A (2009b) Elevation of the plasma level of insulin-like growth factor-I with reproductive maturation prior to initiation of spawning migration of chum salmon. Ann NY Acad Sci 1163:497–500PubMedCrossRefGoogle Scholar
  21. Onuma TA, Makino K, Katsumata H, Beckman BR, Ban M, Ando H, Fukuwaka M, Azumaya T, Swanson P, Urano A (2010a) Changes in the plasma levels of insulin-like growth factor-I from the onset of spawning migration through upstream migration in chum salmon. Gen Comp Endocrinol 165:237–243PubMedCrossRefGoogle Scholar
  22. Onuma TA, Ban M, Makino K, Katsumata H, Hu WW, Ando H, Fukuwaka M, Azumaya T, Urano A (2010b) Changes in gene expression for GH/PRL/SL family hormones in the pituitaries of homing chum salmon during ocean migration through upstream migration. Gen Comp Endocrinol 166:537–548PubMedCrossRefGoogle Scholar
  23. Onuma TA, Makino K, Ando H, Ban M, Fukuwaka M, Azumaya T, Urano A (2010c) Expression of GnRH genes is elevated in discrete brain loci of chum salmon before initiation of homing behavior and during spawning migration. Gen Comp Endocrinol 168:356–368PubMedCrossRefGoogle Scholar
  24. Palstra AP, van den Thillart GEEJM (2010) Swimming physiology of eels: energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem 36:297–322PubMedCrossRefGoogle Scholar
  25. Palstra AP, Schnabel D, Nieveen MC, Spaink HP, van den Thillart GEEJM (2008) Male silver eels mature by swimming. BMC Physiol 8:14PubMedCrossRefGoogle Scholar
  26. Palstra AP, Crespo D, van den Thillart GEEJM, Planas JV (2010a) Saving energy to fuel exercise: swimming suppresses oocyte development and down-regulates ovarian transcriptomic response of rainbow trout Oncorhynchus mykiss. Am J Physiol Reg I 299:R486–R499CrossRefGoogle Scholar
  27. Palstra AP, Schnabel D, Nieveen MC, Spaink HP, van den Thillart G (2010b) Swimming suppresses hepatic vitellogenesis in European silver eel as shown by quantitative RT-PCR of the estrogen receptor 1, vitellogenin1 and vitellogenin2 in the liver. Reprod Biol Endocrinol 8:27PubMedCrossRefGoogle Scholar
  28. Quinn TP (2005) The behaviour and ecology of pacific salmon and trout. University of Washington Press, SeattleGoogle Scholar
  29. Roscoe DW, Hinch SG, Cooke SJ, Patterson DA (2010) Behaviour and thermal experience of adult sockeye salmon migrating through stratified lakes near spawning grounds: the roles of reproductive and energetic states. Ecol Freshw Fish 19:51–62CrossRefGoogle Scholar
  30. Sato A, Ueda H, Fukaya F, Kaeriyama M, Zohar Y, Urano A, Yamauchi K (1997) Sexual differences in homing profiles and shortening of homing duration by gonadotropin-releasing hormone analog implantation in lacustrine sockeye salmon (Oncorhynchus nerka) in Lake Shikotsu. Zool Sci 14:1009–1014CrossRefGoogle Scholar
  31. Schmitz M, Mayer I (1993) Effects of androgens on seawater adaptation in Arctic charr, Salvelinus alpinus. Fish Physiol Biochem 12:11–20CrossRefGoogle Scholar
  32. Tanaka H, Naito Y, Davis ND, Urawa S, Ueda H, Fukuwaka M (2005) Behavioural thermoregulation of chum salmon during homing migration in coastal waters. Mar Ecol Prog Ser 291:307–312CrossRefGoogle Scholar
  33. Ueda H (1999) Artificial control of salmon homing migration and its application to salmon propagation. Bull Tohoku Nat Fish Res Inst 62:39–133Google Scholar
  34. Ueda H (2004) Recent biotelemetry research on lacustrine salmon homing migration. Mem Natl Inst Polar Res Spec Issue 58:80–88Google Scholar
  35. Ueda H (2011) Physiological mechanisms of homing migration in Pacific salmon from behavioral to molecular biological approaches. Gen Comp Endocrinol. doi: 10.1016/j.ygen.2010.02.003 PubMedGoogle Scholar
  36. Ueda H, Yamauchi K (1995) Biochemistry of fish migration. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes Vol 5, Elsevier, Amsterdam, pp 265–279Google Scholar
  37. Ueda H, Hiroi O, Hara A, Yamauchi K, Nagahama Y (1984) Changes in serum concentrations of steroid hormone, thyroxine, and vitellogenin during spawning migration of chum salmon, Oncorhynchus keta. Gen Comp Endocrinol 53:203–211PubMedCrossRefGoogle Scholar
  38. Ueda H, Kaeriyama M, Mukasa K, Urano A, Kudo H, Shoji T, Tokumitsu Y, Yamauchi K, Kurihara K (1998) Lacustrine sockeye salmon return straight to their natal area from open water using both visual and olfactory cues. Chem Senses 23:207–212PubMedCrossRefGoogle Scholar
  39. Ueda H, Leonard JBK, Naito Y (2000) Physiological biotelemetry research on the homing migration of salmonid fishes. In: Moore A, Russell I (eds) Advances in fish telemetry. Crown Copyright, Lowestoft, pp 89–97Google Scholar
  40. Urano A, Ando H, Ueda H (1999) Molecular neuroendocrine basis of spawning migration in salmon. In: Kwon HB, Joss JMP, Ishii S (eds) Recent progress in molecular and comparative endocrinology. Hormone Research Center, Kwangju, pp 46–56Google Scholar
  41. Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC, Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390:371–376PubMedCrossRefGoogle Scholar
  42. Yamada H, Amano M, Okuzawa K, Chiba H, Iwata M (2002) Maturational changes in brain contents of salmon GnRH in rainbow trout as measured by a newly developed time-resolved fluoroimmunoassay. Gen Comp Endocrinol 126:136–143PubMedCrossRefGoogle Scholar
  43. Yamamoto Y, Hino H, Ueda H (2010) Olfactory imprinting of amino acids in lacustrine sockeye salmon. PLoS ONE. doi: 10.1371/journal.pone.0008633 Google Scholar
  44. Zohar Y (1996) New approaches for the manipulation of ovulation and spawning in farmed fish. Bull Natl Res Inst Aquacult Suppl 2:43–48Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Kazufumi Hayashida
    • 1
    • 2
  • Kosuke Fukaya
    • 1
  • Arjan P. Palstra
    • 3
  • Hiroshi Ueda
    • 4
  1. 1.Division of Biosphere ScienceGraduate School of Environmental Science, Hokkaido UniversitySapporoJapan
  2. 2.Watershed Environmental Engineering Research TeamCivil Engineering Research Institute for Cold RegionSapporoJapan
  3. 3.Institute for Marine Resources and Ecosystem Studies (IMARES)Wageningen Aquaculture, Wageningen University and Research CenterYersekeThe Netherlands
  4. 4.Laboratory of Aquatic Bioresources and Ecosystem, Section of Ecosystem Conservation, Field Science Center for Northern BiosphereHokkaido UniversitySapporoJapan

Personalised recommendations