Homing ability and migration success in Pacific salmon: Mechanistic insights from biotelemetry, endocrinology, and neurophysiology

Marine Ecology Progress Series

Volumn 496, Issue , 2014, Pages 219-232

  Ueda, Hiroshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Biotelemetry; Endocrinology; Homing ability; Neurophysiology; Olfaction; Pacific salmon; Reproduction

Indexed keywords

AMINO ACID; BIOTELEMETRY; BREEDING SITE; ENDOCRINOLOGY; HOMING BEHAVIOR; HORMONE; MIGRATORY BEHAVIOR; OLFACTION; SALMONID; SPAWNING;

BERING SEA; HOKKAIDO; JAPAN; PACIFIC OCEAN; PACIFIC OCEAN (NORTH);

EID: 84893412776     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps10636     Document Type: Review

References (97)

1. Alioto TS, Ngai J (2005) The odorant receptor repertoire of teleost fish. BMC Genomics 6: 173
2. Amano M, Urano A, Aida K (1997) Distribution and function of gonadotropin-releasing hormone (GnRH) in the teleost brain. Zoolog Sci 14: 1-11
3. Bandoh H, Kida I, Ueda H (2011) Olfactory responses to natal stream water in sockeye salmon by BOLD fMRI. PLoS ONE 6: e16051
4. Bertmar G (1997) Chemosensory orientation in salmonid fishes. In: Datta Munshi JS, Singh HR (eds) Advances in Fish Research, Vol 2. Narendra Publishing House, Delhi, p 63-80
5. Bodznick D (1978) Calcium ion: an odorant for natural water discriminations and the migratory behavior of sockeye salmon. J Comp Physiol 127: 157-166
6. Brantley RK, Wingfield JC, Bass AH (1993) Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Horm Behav 27: 332-347
7. Cardwell JR, Liley NR (1991) Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisome viride (Scaridae). Horm Behav 25: 1-18
8. Cardwell JR, Sorensen PW, Van Der Kraak GJ, Liley NR (1996) Effect of dominance status on sex hormone levels in laboratory and wild-spawning male trout. Gen Comp Endocrinol 101: 333-341
9. Cooke SJ, Hinch SG, Wikelski M, Andrews RD, Kuchel LJ, Wolcott TG, Butler PJ (2004) Biotelemetry: a mechanistic approach to ecology. Trends Ecol Evol 19: 334-343
10. Cooper JC, Lee GF, Dizon AE (1974) An evaluation of the use of the EEG technique to determine chemical constituents in homestream water. Trans Wis Acad Sci Arts Lett 62: 165-172
11. Cooper JC, Scholz AT, Horrall RM, Hasler AD, Madison DM (1976) Experimental confirmation of the olfactory hypothesis with artificially imprinted homing coho salmon (Oncorhynchus kisutch). J Fish Res Board Can 33: 703-710
12. Costerton JW, Lewandowski Z, DeBeer D, Caldwell D, Korber D, James G (1994) Biofilms, the customized microniche. J Bacteriol 176: 2137-2142
13. Courtenay SC, Quinn TP, Dupuis HMC, Groot C, Larkin PA (1997) Factors affecting the recognition of populationspecific odors by juvenile coho salmon. J Fish Biol 50: 1042-1060
14. Dittman AH, Quinn TP (1996) Homing in Pacific salmon: mechanisms and ecological basis. J Exp Biol 199: 83-91
15. Dittman AW, Quinn TP, Nevitt GA (1996) Timing of imprinting to natural and artificial odors by coho salmon (Oncorhynchus kisutch). Can J Fish Aquat Sci 53: 434-442
16. Døving KB (1989) Molecular cues in salmonid migration. In: Maruani J (ed) Molecules in physics, chemistry, and biology. Kluwer Academic Publishers, Amsterdam, p 299-329
17. Døving KB, Westerberg H, Johnsen PB (1985) Role of olfaction in the behavioral and neuronal responses of Atlantic salmon, Salmo salar, to hydrographic stratification. Can J Fish Aquat Sci 42: 1658-1667
18. Dukes JP, Deaville R, Bruford MW, Youngson AF, Jordan WC (2004) Odorant receptor gene expression changes during the parr-smolt transformation in Atlantic salmon. Mol Ecol 13: 2851-2857
19. Dukes JP, Deaville R, Gottelli D, Neigel JE, Bruford MW, Jordan WC (2006) Isolation and characterisation of main olfactory and vomeronasal receptor gene families from the Atlantic salmon (Salmo salar). Gene 371: 257-267
20. Fagerlund UHM, McBridge JR, Smith M, Tomlinson N (1963) Olfactory perception in migrating salmon III. Stimulants for adult sockeye salmon (Oncorhynchus nerka) in home stream waters. J Fish Res Board Can 20: 1457-1463
21. Fukaya M, Ueda H, Sato A, Kaeriyama M and others (1998) Acceleration of gonadal maturation in anadromous maturing sockeye salmon by gonadotropin- releasing hormone analog implantation. Fish Sci 64: 948-951
22. Groot C, Margolis L (1991) Pacific salmon life histories. University of British Columbia Press, Vancouver
23. Groot C, Quinn TP, Hara TJ (1986) Responses of migrating adult sockeye salmon (Oncorhynchus nerka) to population-specific odors. Can J Zool 64: 926-932
24. Hansen LP, Jonsson N, Jonsson B (1993) Oceanic migration in homing Atlantic salmon. Anim Behav 45: 927-941
25. Hara TJ (1994) The diversity of chemical stimulation in fish olfaction and gustation. Rev Fish Biol Fish 4: 1-35
26. Harden Jones FR (1968) Fish migration. Edward Arnold, London
27. Harris J, Bird DJ (2000) Modulation of the fish immune system by hormones. Vet Immunol Immunopathol 77: 163-176
28. Hasler AD, Scholz AT (1983) Olfactory imprinting and homing in salmon. Springer-Verlag, New York, NY
29. Hasler AD, Wisby WJ (1951) Discrimination of stream odors by fishes and relation to parent stream behavior. Am Nat 85: 223-238
30. 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
31. Hino H, Miles NG, Bandoh H, Ueda H (2009) Molecular biological research on olfactory chemoreception in fishes. J Fish Biol 75: 945-959
32. Ikuta K (1996) Effects of steroid hormones on migration of salmonid fishes. Bull Natl Res Inst Aquacult Suppl 2: 23-27
33. Ishizawa S, Yamamoto Y, Denboh T, Ueda H (2010) Release of dissolved free amino acids from biofilms in stream water. Fish Sci 76: 669-676
34. Johnstone KA, Lubienieck KP, Koop BF, Davidson WS (2011) Expression of olfactory receptors in different life stages and life histories of wild Atlantic salmon (Salmon salar). Mol Ecol 20: 4059-4069
35. 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. North Pac Anadromous Fish Comm Bull 1: 163-171
36. Kindler PM, Philipp DP, Gross MT, Bahr JM (1989) Serum 11-ketotestosterone and testosterone concentrations associated with reproduction in male bluegill (Lepomis macrochirus: Centrarchidae). Gen Comp Endocrinol 75: 446-453
37. Kinoshita M, Fukaya M, Tojima T, Kojima S, Ando H, Watanabe M (2005) Retinotectal transmission in the optic tectum of rainbow trout. J Comp Neurol 484: 249-259
38. Kitahashi T, Ando H, Ban M, Ueda H, Urano A (1998a) Changes in the levels of gonadotropin subunit mRNAs in the pituitary of pre-spawning chum salmon. Zoolog Sci 15: 753-760
39. Kitahashi T, Alok D, Ando H, Kaeriyama M, Zohar Y, Ueda H, Urano A (1998b) GnRH analog stimulates gonadotropin II gene expression in maturing sockeye salmon. Zoolog Sci 15: 761-765
40. Kitahashi T, Sato A, Alok D, Kaeriyama M and others (1998c) Gonadotropin-releasing hormone analog and sex steroids shorten homing duration of sockeye salmon in Lake Shikotsu. Zoolog Sci 15: 767-771
41. Kudo H, Hyodo S, Ueda H, Hiroi O, Aida K, Urano A, Yamauchi K (1996a) Cytophysiology of gonadotropinreleasing-hormone neurons in chum salmon (Onco rhynchus keta) forebrain before and after upstream migration. Cell Tissue Res 284: 261-267
42. Kudo H, Ueda H, Yamauchi K (1996b) Immunocytochemical investigation of salmonid olfactory system-specific protein in the kokanee salmon (Oncorhynchus nerka). Zoolog Sci 13: 647-653
43. Kudo H, Ueda H, Mochida K, Adachi S and others (1999) Salmonid olfactory system-specific protein (N24) exhibits glutathione S-transferase class pi-like structure. J Neurochem 72: 1344-1352
44. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23: 649-711
45. Moore A, Scott AP (1992) 17α,20β-dihydroxy-4-pregnen-3-one 20-sulphate is a potent odorant precocious male Atlantic salmon (Salmo salar L.) parr which have been pre-exposed to the urine of ovulated females. Proc Biol Sci 249: 205-209
46. Moore A, Warning CP (1996) Electrophysiological and endocrinological evidence that F-series prostaglandins function as priming pheromones in mature male Atlantic salmon (Salmo salar) parr. J Exp Biol 199: 2307-2316
47. Morinishi F, Shiga T, Suzuki N, Ueda H (2007) Cloning and characterization of an odorant receptor in five Pacific salmon. Comp Biochem Physiol B Biochem Mol Biol 148: 329-336
48. Munakata A, Amano M, Ikuta K, Kitamura S, Aida K (2001a) The involvement of sex steroid hormones in downstream and upstream migratory behavior of masu salmon. Comp Biochem Physiol B Biochem Mol Biol 129: 661-669
49. Munakata A, Amano M, Ikuta K, Kitamura S, Aida K (2001b) The effects of testosterone on upstream migratory behavior in masu salmon, Oncorhynchus masou. Gen Comp Endocrinol 122: 329-340
50. Murata S, Takasaki N, Saitoh M, Tachida H, Okada N (1996) Details of retropositional genome dynamics that provide a rationale for a generic division: the distinct branching of all the Pacific salmon and trout (Oncorhynchus) from the Atlantic salmon and trout (Salmo). Genetics 142: 915-926
51. 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. John Grieg, Bergen, p 211-222
52. Nagahama Y, Adachi S (1985) Identification of a maturationinducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Dev Biol 109: 428-435
53. Nam RH, Kim W, Lee CJ (2004) NMDA receptor-dependent long-term potentiation in the telencephalon of the zebrafish. Neurosci Lett 370: 248-251
54. Nevitt GA, Dittman AH (1998) A new model for olfactory imprinting in salmon. Integr Biol 1: 215-223
55. Nevitt GA, Dittman AH, Quinn TP, Moody WJ Jr (1994) Evidence for a peripheral olfactory memory in imprinted salmon. Proc Natl Acad Sci USA 91: 4288-4292
56. Nordeng H (1971) Is the local orientation of anadromous fishes determined by pheromones? Nature 233: 411-413
57. Nordeng HA (1977) A pheromone hypothesis for homeward migration in anadromous salmonids. Oikos 28: 155-159
58. Nosyk O, Haseborg ET, Metzger U, Frimmel FH (2008) A standardized pre-treatment method of biofilm flocs for fluorescence microscopic characterization. J Microbiol Methods 75: 449-456
59. Ogura M, Ishida Y (1995) Homing behavior and vertical movements of four species of Pacific salmon (Onco rhynchus spp.) in the central Bering Sea. Can J Fish Aquat Sci 52: 532-540
60. Pankhurst NW, Barnett CW (1993) Relationship of population density, territorial interaction and plasma levels of gonadal steroids in spawning male demoiselles Chromis dispulis (Pisces: Pomacentridae). Gen Comp Endocrinol 90: 168-176
61. Putman NF, Lohmann KJ, Putman EM, Quinn TP, Klimley AP, Noakes DLG (2013) Evidence for geomagnetic imprinting as a homing mechanism in Pacific salmon. Curr Biol 23:312-316
62. Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle, WA
63. Quinn TP, Groot C (1984) Pacific salmon (Oncorhynchus) migrations: orientation vs. random movement. Can J Fish Aquat Sci 41: 1319-1324
64. Quinn TP, Tolson GM (1986) Evidence of chemically mediated population recognition in coho salmon (Oncorhynchus kisutch). Can J Zool 64: 84-87
65. Quinn TP, Terjart BA, Groot C (1989) Migratory orientation and vertical movements of homing adult sockeye salmon, Oncorhynchus nerka, in coastal waters. Anim Behav 37: 587-599
66. Sato A, Ueda H, Fukaya M, Kaeriyama M, Zohar Y, Urano A, Yamauchi K (1997) Sexual differences in homing profiles and shortening of homing duration by gonadotropinreleasing hormone analog implantation in lacustrine sockeye salmon (Oncorhynchus nerka) in Lake Shikotsu. Zoolog Sci 14: 1009-1014
67. Satou M, Hoshikawa R, Sato Y, Okawa K (2006) An in vitro study of long-term potentiation in the carp (Cyprinus carpio L.) olfactory bulb. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192: 135-150
68. Scholz AT, Horrall RM, Hasler AD (1976) Imprinting to chemical cues: the basis for home stream selection in salmon. Science 192: 1247-1249
69. Shimizu M, Kudo H, Ueda H, Hara A, Shimazaki M, Yamauchi K (1993) Identification and immunological properties of an olfactory system-specific protein in kokanee salmon (Oncorhynchus nerka). Zoolog Sci 10: 287-294
70. Shoji T, Ueda H, Ohgami T, Sakamoto T, Katsuragi Y, Yamauchi K, Kurihara K (2000) Amino acids dissolved in stream water as possible homestream odorants for masu salmon. Chem Senses 25: 533-540
71. Stabell OB (1992) Olfactory control of homing behaviour in salmonids. In: Hara TJ (ed) Fish chemoreception. Chapman & Hall, London, p 249-270
72. Tanaka H, Naito Y, Davis ND, Urawa S, Ueda H, Fukuwaka M (2005) Behavioral thermoregulation of chum salmon during homing migration in coastal waters. Mar Ecol Prog Ser 291: 307-312
73. Thomas JD (1997) The role of dissolved organic matter, particularly free amino acids and humic substances, in freshwater ecosystems. Freshw Biol 38: 1-36
74. Ueda K (1985) An electrophysiological approach to the olfactory recognition of homestream waters in chum salmon. NOAA Tech Rep NMFS 27: 97-102
75. Ueda H (1999) Artificial control of salmon homing migration and its application to salmon propagation. Bull Tohoku Natl Fish Res Inst 62: 133-139
76. Ueda H (2004) Recent biotelemetry research on lacustrine salmon homing migration. Mem Natl Inst Polar Res 58(Spec Issue): 80-88
77. Ueda H (2011) Physiological mechanisms of homing migration in Pacific salmon from behavioral to molecular biological approaches. Gen Comp Endocrinol 170: 222-232
78. Ueda H (2012) Physiological mechanisms of imprinting and homing migration in Pacific salmon Oncorhynchus spp. J Fish Biol 81: 543-558
79. Ueda H, Yamauchi K (1995) Biochemistry of fish migration. In: Hochachka PW, Mommsen TP (eds) Environmental and ecological biochemistry, Elsevier, Amsterdam, p 265-279
80. 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
81. Ueda H, Kudo H, Shimizu M, Mochida K, Adachi S, Yamauchi K (1993) Immunological similarity between an olfactory system-specific protein and a testicular germ cell protein in kokanee salmon (Oncorhynchus nerka). Zoolog Sci 10: 685-690
82. Ueda H, Shimizu M, Kudo H, Hara A and others (1994) Species-specificity of an olfactory system-specific protein in various species of teleosts. Fish Sci 60: 239-240
83. Ueda H, Kaeriyama M, Mukasa K, Urano A and others (1998) Lacustrine sockeye salmon return straight to their natal area from open water using both visual and olfactory cues. Chem Senses 23: 207-212
84. 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. Cefas, Lowestoft, p 89-97
85. Ueda H, Yamamoto Y, Hino H (2007) Physiological mechanisms of homing ability in sockeye salmon: from behavior to molecules using a lacustrine model. Am Fish Soc Symp 54: 5-16
86. Villars TA (1983) Hormones and aggressive behavior in teleost fishes. In: Svare BB (ed) Hormones and aggressive behavior. Plenum Press, New York, NY, p 407-433
87. 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
88. Wickens A, May D, Rand-Weaver M (2001) Molecular characterisation of a putative Atlantic salmon (Salmo salar) odorant receptor. Comp Biochem Physiol B Biochem Mol Biol 129: 653-660
89. Wisby WJ, Hasler AD (1954) Effect of olfactory occlusion on migrating silver salmon (Oncorhynchus kisutch). J Fish Res Board Can 11: 472-478
90. 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
91. Yamamoto Y, Hino H, Ueda H (2010) Olfactory imprinting of amino acids in lacustrine sockeye salmon. PLoS ONE 5: e8633
92. Yamamoto Y, Shibata H, Ueda H (2013) Olfactory homing of chum salmon to stable compositions of amino acids in natal stream water. Zoolog Sci 30: 607-612
93. Yambe H, Kitamura S, Kamio M, Yamada M, Matsunaga S, Fusetani N, Yamazaki F (2006) L-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc Natl Acad Sci USA 103: 15370-15374
94. Yanagi S, Kudo H, Doi Y, Yamauchi K, Ueda H (2004) Immunohistochemical demonstration of salmon olfactory glutathione S-transferase class pi (N24) in the olfactory system of lacustrine sockeye salmon during ontogenesis and cell proliferation. Anat Embryol (Berl) 208: 231-238
95. Yano K, Nakamura A (1992) Observations of the effect of visual and olfactory ablation on the swimming behavior of migrating adult chum salmon, Oncorhynchus keta. Jpn J Ichthyol 39: 67-83
96. Yano A, Ogura M, Sato A, Sakaki Y, Ban M, Nagasawa K (1996) Development of ultrasonic telemetry technique for investigating the magnetic sense of salmonids. Fish Sci 62: 698-704
97. Zohar Y (1996) New approaches for the manipulation of ovulation and spawning in farmed fish. Bull Natl Res Inst Aquacult Suppl 2: 43-48