Body size is the primary regulator affecting commencement of smolting in amago salmon Oncorhynchus masou ishikawae


The present study retrospectively examined relationships between growth trajectory and smolting in order to identify the key regulators in commencement of smolting using groups of all-female homozygous clonal amago salmon. We found that (1) regardless of specific growth rate, the majority of fish above the threshold size (12–13 g) by the end of the decision window (early fall) became smolt in the future; (2) even if fish smaller than the threshold size during the decision window exceeded that size afterwards, they were not recruited to smolt; (3) smolting of fish that attained sufficient size during the decision window could not be suppressed by subsequent restriction of growth rate; (4) smaller fish that had not attained the threshold size during the decision window could not smoltify, even though they showed faster growth rates than that of future smolt during/after the decision window. Taken together, these findings indicated that fish mass by the end of the decision window was responsible for the determination of whether individual amago salmon could smoltify or not and that the faster growth rates observed in future smolt after the decision window occurred as a result of commitment of smoltification.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. 1.

    Hoar WS (1976) Smolt transformation: evolution, behavior, and physiology. J Fish Res Board Can 33:1233–1252

    Article  Google Scholar 

  2. 2.

    Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS et al (eds) Fish physiology, vol 11B., Academic PressOrlando, FL, pp 275–343

    Google Scholar 

  3. 3.

    McCormick SD, Hansen LP, Quinn TP, Saunders RL (1998) Movement, migration, and smolting of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:77–92

    Article  Google Scholar 

  4. 4.

    Metcalf NB (1998) The interaction between behavior and physiology in determining life history patterns in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:93–103

    Article  Google Scholar 

  5. 5.

    Stefansson SO, Th Björnsson B, Ebbesson LOE, McCormick SD (2008) Smoltification. In: Finn RN, Kapoor BG (eds) Fish larval physiology. Science Publishers, Enfield, pp 639–681

    Google Scholar 

  6. 6.

    Thorpe JE (1977) Bimodal distribution of length of juvenile Atlantic salmon (Salmo salar L.) under artificial rearing conditions. J Fish Biol 11:175–184

    Article  Google Scholar 

  7. 7.

    Thorpe JE, Morgan RJG (1978) Parental influence on growth rate, smolting rate and survival in hatchery reared juvenile Atlantic salmon, Salmo salar. J Fish Biol 13:549–556

    Article  Google Scholar 

  8. 8.

    Bailey JK, Saunders RL, Buzeta MI (1980) Influence of parental smolt age and sea age on growth and smolting of hatchery-reared Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 37:1379–1386

    Article  Google Scholar 

  9. 9.

    Thorpe JE, Morgan RJG, Ottaway EM, Milnes MS (1980) Time of divergence of growth groups between potential 1+ and 2+ smolt among sibling Atlantic salmon. J Fish Biol 17:13–21

    Article  Google Scholar 

  10. 10.

    Thorpe JE, Talbot C, Villarreal C (1982) Bimodality of growth and smolting in Atlantic salmon, Salmo salar L. Aquaculture 28:123–132

    Article  CAS  Google Scholar 

  11. 11.

    Clarke WC, Shelbourn JE (1986) Delayed photoperiod produces more uniform growth and greater seawater adaptability in underyearling coho salmon (Oncorhynchus kisutch). Aquaculture 56:287–299

    Article  Google Scholar 

  12. 12.

    Kubo T (1980) Studies on the life history of the “Masu” salmon (Oncorhynchus masou) in Hokkaido. Sci Rep Hokkaido Salmon Hatch 34:1–95 (in Japanese with English abstract)

    Google Scholar 

  13. 13.

    Kubo T (1983) Growth-rate and smolting-rate of anadromous “Masu” salmon (Oncorhynchus masou) juveniles under artificial conditions. Sci Rep Hokkaido Salmon Hatch 37:23–39 (In Japanese with English abstract)

    Google Scholar 

  14. 14.

    Hirata T, Goto A, Hamada K (1986) Bimodal length frequency distribution in 0+ aged masu salmon, Oncorhynchus masou, in a natural stream of southern Hokkaido. Jpn J Ichthyol 33:204–207 (in Japanese with English abstract)

    Google Scholar 

  15. 15.

    Hirata T, Goto A, Yamazaki F (1988) Individual growth and smoltification of juvenile masu salmon, Oncorhynchus masou Brevoort, under rearing conditions. J Fish Biol 32:77–84

    Article  Google Scholar 

  16. 16.

    Yamamoto S, Nakano S (1996) Growth and development of bimodal length-frequency distribution during smolting in a wild population of white-spotted charr in northern Japan. J Fish Biol 48:68–79

    Google Scholar 

  17. 17.

    Kato F (1973) Ecological study on the sea-run form of Oncorhynchus rhodurus, found in Ise Bay, Japan. Jpn J Ichthyol 20:225–233 (in Japanese with English abstract)

    Google Scholar 

  18. 18.

    Elson PF (1957) The importance of size in the change from parr to smolt in Atlantic salmon. Can Fish Cult 21:1–6

    Google Scholar 

  19. 19.

    Skilbrei OT (1988) Growth pattern of pre-smolt Atlantic salmon (Salmo salar L.): the percentile increment method (PIM) as a new method to estimate length-dependent growth. Aquaculture 69:129–143

    Article  Google Scholar 

  20. 20.

    Skilbrei OT (1991) Importance of threshold length and photoperiod for the development of bimodal length-frequency distribution in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 48:2163–2172

    Article  Google Scholar 

  21. 21.

    Duston J, Saunders RL (1992) Effect of 6-, 12-, and 18-month photoperiod cycles on smolting and sexual maturation in juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 49:2273–2280

    Article  Google Scholar 

  22. 22.

    Nicieza AG, Reyes-Gavilá FG, Braña F (1994) Differentiation in juvenile growth and bimodality patterns between northern and southern populations of Atlantic salmon (Salmo salar L.). Can J Zool 72:1603–1610

    Article  Google Scholar 

  23. 23.

    Saunders RL, Duston J, Benfey TJ (1994) Environmental and biological factors affecting growth dynamics in relation to smolting of Atlantic salmon, Salmo salar L. Aquacult Fish Manag 25:9–20

    Google Scholar 

  24. 24.

    Dodson JJ, Aubin-Horth N, Thériault V, Páez DJ (2013) The evolutionary ecology of alternative migratory tactics in salmonid fishes. Biol Rev Camb Philos Soc 88:602–625

    PubMed  Article  Google Scholar 

  25. 25.

    Kristinsson JB, Saunders RL, Wiggs AJ (1985) Growth dynamics during the development of bimodal length-frequency distribution in juvenile Atlantic salmon (Salmo salar L.). Aquaculture 45:1–20

    Article  Google Scholar 

  26. 26.

    Higgins PJ (1985) Metabolic differences between Atlantic salmon (Salmo salar) parr and smolts. Aquaculture 45:33–53

    Article  Google Scholar 

  27. 27.

    Metcalfe NB, Huntingford FA, Thorpe JE, Adams CE (1990) The effects of social status on life-history variation in juvenile salmon. Can J Zool 68:2630–2636

    Article  Google Scholar 

  28. 28.

    Økland F, Jonsson B, Jensen AJ, Hansen LP (1993) Is there a threshold size regulating seaward migration of brown trout and Atlantic salmon? J Fish Biol 42:541–550

    Article  Google Scholar 

  29. 29.

    Beckman BR, Donald AL, Dickhoff WW (2003) Life history plasticity in chinook salmon: relation of size and growth rate to autumnal smolting. Aquaculture 222:149–165

    Article  Google Scholar 

  30. 30.

    Thorpe JE, Mangel M, Metcalfe NB, Huntingford FA (1998) Modeling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. Evol Ecol 12:581–599

    Article  Google Scholar 

  31. 31.

    Kato F (1975) On the distribution of a sea-run form of salmonid fish, Oncorhynchus rhodurus, found in southwestern Japan. Jpn J Ichthyol 21:191–197 (in Japanese with English abstract)

    Google Scholar 

  32. 32.

    Usuda H (1989) All female production and its characteristics in amago salmon (Oncorhynchus rhodurus). Fish Genet Breed Sci 14:11–22 (in Japanese with English abstract)

    Google Scholar 

  33. 33.

    Goto K (1994) Studies of the breeding of amago salmon, Oncorhynchus masou ishikawae—characters of strain difference on phase differentiation of the fluviatile form and sea-run form of amago salmon, Oncorhynchus masou ishikawae. Rep Gifu Prefect Fish Exp Stn 39:21–28 (in Japanese)

    Google Scholar 

  34. 34.

    Kuwada T, Tuzuku N, Muto Y, Nakayama I (1995) Studies on breeding of salmonid fishes by chromosome manipulation—I: characteristics of clonal amago salmon, Oncorhynchus masou ishikawae. Rep Gifu Prefect Fish Exp Stn 40:19–33 (in Japanese)

    Google Scholar 

  35. 35.

    Tachikawa W, Kumazaki T (1975) Studies on the reproduction of amago salmon, Oncorhynchus rhodurus-XX. The effect of the growth of the precociously mature parr on the body-weight composition in fingerling amago salmon. Rep Gifu Prefect Fish Exp Stn 21:41–49 (in Japanese)

    Google Scholar 

  36. 36.

    Honjoh T (1977) Studies on the culture and transplantation of Amago salmon, Oncorhynchus rhodurus. Bull Gifu Prefect Fish Exp Stn 22:1–103 (in Japanese with English abstract)

    Google Scholar 

  37. 37.

    Kobayashi T, Ide A, Hiasa T, Fushiki S, Ueno K (1994) Production of cloned amago salmon Oncorhynchus rhodurus. Fish Sci 60:275–281

    Google Scholar 

  38. 38.

    Skilbrei OT, Hansen T, Stefansson SO (1997) Effects of decreases in photoperiod on growth and bimodality in Atlantic salmon (Salmo salar). Aquacult Res 28:43–49

    Article  Google Scholar 

  39. 39.

    Berrill IK, Porter MJR, Smart A, Mitchell D, Bromage NR (2003) Photoperiodic effects on precocious maturation, growth and smoltification in Atlantic salmon, Salmo salar. Aquaculture 222:239–252

    Article  Google Scholar 

  40. 40.

    Nagahama Y, Adachi S, Tashiro F, Grau EG (1982) Some endocrine factors affecting the development of seawater tolerance during the parr-smolt transformation of the amago salmon, Oncorhynchus rhodurus. Aquaculture 28:81–90

    Article  CAS  Google Scholar 

  41. 41.

    Yamauchi K, Koide N, Adachi S, Nagahama Y (1984) Changes in seawater adaptability and blood thyroxine concentrations during smoltification of the masu salmon, Oncorhynchus masou, and the amago salmon, Oncorhynchus rhodurus. Aquaculture 42:247–256

    Article  CAS  Google Scholar 

  42. 42.

    Leitritz E (1969) Feeding practices. Trout and salmon culture: hatchery methods. State Calif Dep Fish Game Fish Bull 107:88–90

    Google Scholar 

  43. 43.

    Kanda Y (2013) Investigation of the freely-available easy-to-use software “EZR” (Easy R) for medical statistics. Bone Marrow Transplant 48:452–458

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  44. 44.

    Saunders RL, Henderson EB, Glebe BD (1982) Precocious sexual maturation and smoltification in male Atlantic salmon (Salmo salar). Aquaculture 28:211–229

    Article  CAS  Google Scholar 

  45. 45.

    Aida K, Kato T, Awaji M (1984) Effects of castration on the smoltification of precocious male masu Salmon Oncorhynchus masou. Nippon Suisan Gakkaishi 50:565–571

    Article  Google Scholar 

  46. 46.

    Foote CJ, Clarke WC, Blackburn J (1991) Inhibition of smolting in precocious male chinook salmon, Oncorhynchus tshawytscha. Can J Zool 69:1848–1852

    Article  Google Scholar 

  47. 47.

    Takami T, Aoyama T, Nagata M, Miyamoto M, Ohkubo S, Kawamura H (1998) Individual growth and life-history divergence of juvenile masu salmon (Oncorhynchus masou) in a northern Japan stream. Sci Rep Hokkaido Fish Hatch 52:21–29

    Google Scholar 

  48. 48.

    Tamate T, Maekawa K (2002) Individual growth and phase differentiation of lacustrine masu salmon, Oncorhynchus masou, under artificial rearing conditions. Ichthyol Res 49:397–400

    Article  Google Scholar 

  49. 49.

    Páez DJ, Brisson-Bonenfant C, Rossignol O, Guderley HE, Bernatchez L, Dodson JJ (2011) Alternative developmental pathways and the propensity to migrate: a case study in the Atlantic salmon. J Evol Biol 24:245–255

    PubMed  Article  Google Scholar 

  50. 50.

    Pedersen S, Berg PR, Culling M, Danzmann RG, Glebe B, Leadbeater S, Lien S, Moen T, Vandersteen W, Boulding EG (2013) Quantitative trait loci for precocious parr maturation, early smoltification, and adult maturation in double-backcrossed trans-Atlantic salmon (Salmo salar). Aquaculture 410–411:164–171

    Article  CAS  Google Scholar 

  51. 51.

    Rossignol O, Dodson JJ, Guderley H (2011) Relationship between metabolism, sex and reproductive tactics in young Atlantic salmon (Salmo salar L.). Comp Biochem Physiol 159:82–91

    Article  CAS  Google Scholar 

  52. 52.

    Fujioka Y, Fushiki S, Tagawa M, Ogasawara T, Hirano T (1990) Seasonal changes in plasma thyroxine levels in Biwa and amago salmon reared in the pond. Nippon Suisan Gakkaishi 56:249–254

    Article  CAS  Google Scholar 

  53. 53.

    Fujioka Y (1991) Morphological, physiological, and ecological studies on Biwa salmon. Bull Shiga Pref Samegai Trout Farm 3:1–112 (in Japanese)

    Google Scholar 

  54. 54.

    Fujioka Y (2002) Size and season of smoltification and precocious sexual maturation in amago salmon. Bull Shiga Pref Fish Exp Stn 49:51–55 (in Japanese with English abstact)

    Google Scholar 

  55. 55.

    Yada T, Takahashi K, Hirano T (1991) Seasonal changes in seawater adaptability and plasma levels of prolactin and growth hormone in landlocked sockeye salmon (Oncorhynchus nerka) and amago salmon (O. rhodurus). Gen Comp Endocrinol 82:33–44

    PubMed  Article  CAS  Google Scholar 

  56. 56.

    Fujioka Y, Fushiki S (1989) Seasonal changes in hypoosmoregulatory ability of Biwa salmon Oncorhynchus rhodurus and amago salmon O. rhodurus. Nippon Suisan Gakkaishi 55:1885–1892

    Article  Google Scholar 

  57. 57.

    Orciari RD, Leonard GH (1996) Length characteristics of smolts and timing of downstream migration among three strains of Atlantic salmon in a Southern New England stream. N Am J Fish Manag 16:851–869

    Article  Google Scholar 

  58. 58.

    McCormick SD, Shrimpton MJ, Moriyama S, Bjornsson BT (2007) Differential hormonal responses of Atlantic salmon parr and smolt to increased daylength: a possible developmental basis for smolting. Aquaculture 273:337–344

    Article  CAS  Google Scholar 

  59. 59.

    Nichols KM, Edo AF, Wheeler PA, Thorgaard GH (2008) The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics 179:1559–1575

    PubMed  PubMed Central  Article  Google Scholar 

  60. 60.

    Seear PJ, Carmichael SN, Talbot R, Taggart JB, Bron JE, Sweeney GE (2010) Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study. Mar Biotechnol 12:126–140

    PubMed  Article  CAS  Google Scholar 

Download references


We would like to express our thanks to the staff of the Gifu Prefectural Research Institute for Freshwater Fish and Aquatic Environments for assisting us during our study. This work was supported in part by a grant-in-aid from the Ministry of Agriculture, Forestry, and Fisheries of Japan.

Author information



Corresponding author

Correspondence to Goro Yoshizaki.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kuwada, T., Tokuhara, T., Shimizu, M. et al. Body size is the primary regulator affecting commencement of smolting in amago salmon Oncorhynchus masou ishikawae . Fish Sci 82, 59–71 (2016).

Download citation


  • Amago salmon
  • Growth bimodality
  • Homozygous clone
  • Smoltification
  • Threshold size