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.
Wageningen Aquaculture is a consortium of Institute for Marine Resources and Ecosystem Studies (IMARES) and Aquaculture and Fisheries Group (AFI, Wageningen University), both part of Wageningen University and Research Centre (WUR).
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Amano M, Urano A, Aida K (1997) Distribution and function of gonadotropin-releasing hormone (GnRH) in the teleost brain. Zool Sci 14:1–11
Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trend Ecol Evol 19:334–343
Dittman AW, Quinn TP (1996) Homing in pacific salmon: mechanisms and ecological basis. J Exp Biol 199:83–91
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
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
Hino H, Iwai T, Yamashita M, Ueda H (2007) Identification of an olfactory imprinting-related gene in the lacustrine sockeye salmon, Oncorhynchus nerka. Aquaculture 273:200–208
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 1:163–171
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 15:767–771
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 166:187–190
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 284:261–267
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 72:1344–1352
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:142–150
Lundqvist H, Borg B, Berglund I (1989) Androgens impair seawater adaptability in smolting Baltic salmon (Salmo salar). Can J Zool 67:1733–1736
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 152:304–309
McCormick SD, Naiman RJ (1985) Hypoosmoregulation in an anadromous teleost: influence of sex and maturation. J Exp Zool 234:193–198
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:75–89
Morinishi F, Shiga T, Suzuki N, Ueda H (2007) Cloning and characterization of an odorant receptor in five Pacific salmon. Comp Biochem Physiol 148B:329–336
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 211–222
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 212:56–70
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 1163:497–500
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 165:237–243
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 166:537–548
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 168:356–368
Palstra AP, van den Thillart GEEJM (2010) Swimming physiology of eels: energetic costs and effects on sexual maturation and reproduction. Fish Physiol Biochem 36:297–322
Palstra AP, Schnabel D, Nieveen MC, Spaink HP, van den Thillart GEEJM (2008) Male silver eels mature by swimming. BMC Physiol 8:14
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–R499
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 8:27
Quinn TP (2005) The behaviour and ecology of pacific salmon and trout. University of Washington Press, Seattle
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 19:51–62
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 14:1009–1014
Schmitz M, Mayer I (1993) Effects of androgens on seawater adaptation in Arctic charr, Salvelinus alpinus. Fish Physiol Biochem 12:11–20
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 291:307–312
Ueda H (1999) Artificial control of salmon homing migration and its application to salmon propagation. Bull Tohoku Nat Fish Res Inst 62:39–133
Ueda H (2004) Recent biotelemetry research on lacustrine salmon homing migration. Mem Natl Inst Polar Res Spec Issue 58:80–88
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
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 265–279
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 53:203–211
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 23:207–212
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 89–97
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 46–56
Walker MM, Diebel CE, Haugh CV, Pankhurst PM, Montgomery JC, Green CR (1997) Structure and function of the vertebrate magnetic sense. Nature 390:371–376
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 126:136–143
Yamamoto Y, Hino H, Ueda H (2010) Olfactory imprinting of amino acids in lacustrine sockeye salmon. PLoS ONE. doi:10.1371/journal.pone.0008633
Zohar Y (1996) New approaches for the manipulation of ovulation and spawning in farmed fish. Bull Natl Res Inst Aquacult Suppl 2:43–48
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2013 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Hayashida, K., Fukaya, K., Palstra, A.P., Ueda, H. (2013). Salmonid Reproductive Migration and Effects on Sexual Maturation. In: Palstra, A., Planas, J. (eds) Swimming Physiology of Fish. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-31049-2_1
Download citation
DOI: https://doi.org/10.1007/978-3-642-31049-2_1
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-31048-5
Online ISBN: 978-3-642-31049-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)