Environmental Biology of Fishes

, Volume 101, Issue 2, pp 341–353 | Cite as

Vertical self-sorting behavior in juvenile Chinook salmon (Oncorhynchus tshawytscha): evidence for family differences and variation in growth and morphology

  • Julia R. Unrein
  • Eric J. Billman
  • Karen M. Cogliati
  • Rob Chitwood
  • David L. G. Noakes
  • Carl B. Schreck


Life history variation is fundamental to the evolution of Pacific salmon and their persistence under variable conditions. We discovered that Chinook salmon sort themselves into surface- and bottom-oriented groups in tanks within days after exogenous feeding. We hypothesised that this behaviour is correlated with subsequent differences in body morphology and growth (as measured by final length and mass) observed later in life. We found consistent morphological differences between surface and bottom phenotypes. Furthermore, we found that surface and bottom orientation within each group is maintained for at least one year after the phenotypes were separated. These surface and bottom phenotypes are expressed across genetic stocks, brood years, and laboratories and we show that the proportion of surface- and bottom-oriented offspring also differed among families. Importantly, feed delivery location did not affect morphology or growth, and the surface fish were longer than bottom fish at the end of the rearing experiment. The body shape of the former correlates with wild individuals that rear in mainstem habitats and migrate in the fall as subyearlings and the latter resemble those that remain in the upper tributaries and migrate as yearling spring migrants. Our findings suggest that early self-sorting behaviour may have a genetic basis and be correlated with other phenotypic traits that are important indicators for juvenile migration timing.


Life history variation Geometric morphometrics Phenotype Genetics 



We thank R. Couture and J. O’Neil for rearing fish for these experiments and construction of behavioural observation facilities. O. Hakanson, C. Danley, K. Self and H. Stewart assisted with sampling and data collection. L. Ciannelli and others provided constructive comments on earlier drafts of this manuscript. The US Army Corps of Engineers, Portland District provided funding for this research (Project TD-13-02). Additional support was provided by the USGS, the Oregon Department of Fish and Wildlife and the Oregon Hatchery Research Center. Animal rearing, behaviour experiments and morphometric procedures were approved by the Institutional Animal Care and Use Committee at Oregon State University (ACUP #4289).

Compliance with ethical standards


Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

This draft manuscript is distributed solely for purposes of scientific peer review. Its content is deliberative and predecisional, so it must not be disclosed or released by reviewers. Because the manuscript has not yet been approved for publication by the U.S. Geological Survey (USGS), it does not represent any official USGS finding or policy.

Supplementary material

10641_2017_702_MOESM1_ESM.docx (737 kb)
ESM 1 (DOCX 737 kb)


  1. Beckman BR, Larsen DA, Dickhoff WW (2003) Life history plasticity in Chinook salmon: relation of size and growth rate to autumnal smolting. Aquaculture 222(1-4):149–165. CrossRefGoogle Scholar
  2. Beeman JW, Rondorf DW, Tilson ME (1994) Assessing smoltification of juvenile spring Chinook salmon (Oncorhynchus tshawytscha) using changes in body morphology. Can J Fish Aquat Sci 51(4):836–844. CrossRefGoogle Scholar
  3. Billman EJ, Whitman LD, Schroeder RK, Sharpe CS, Noakes DLG, Schreck CB (2014) Body morphology differs in wild juvenile Chinook salmon (Oncorhynchus tshawytscha) that express different migratory phenotypes in the Willamette River, Oregon, U.S. A. J Fish Biol 85(4):1097–1110. CrossRefPubMedGoogle Scholar
  4. Biro PA, Ridgeway MS (2008) Repeatability of foraging tactics in young brook trout, Salvelinus fontinalis. Can Field-Nat 122(1):40–44.  10.22621/cfn.v122i1.541 CrossRefGoogle Scholar
  5. Bodaly RA (1979) Morphological and ecological divergence within the lake whitefish (Coregonus clupeaformis) species complex in Yukon territory. Can J Fish Aquat Sci 36:1214–1222Google Scholar
  6. Bottom DL, Jones KK, Cornwell TJ, Gray A, Simenstad CA (2005) Patterns of Chinook salmon migration and residency in the Salmon River estuary (Oregon). Estuar Coast Shelf Sci 64(1):79–93. CrossRefGoogle Scholar
  7. Bourke P, Magnan P, Rodríguez MA (1997) Individual variations in habitat use and morphology in brook charr. J Fish Biol 51(4):783–794. CrossRefGoogle Scholar
  8. Carl LM, Healey MC (1984) Differences in enzyme frequency and body morphology among three juvenile life history types of Chinook salmon (Oncorhynchus tshawytscha) in the Nanaimo River, British Columbia. Can J Fish Aquat Sci 41(7):1070–1077. CrossRefGoogle Scholar
  9. Carlson SM, Seamons TR (2008) A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change. Evol Appl 1(2):222–238. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chavarie L, Howland K, Tonn WM (2013) Sympatric polymorphism in lake trout: the coexistence of multiple shallow-water morphotypes in great bear lake. T Am Fish Soc 142(3):814–823. CrossRefGoogle Scholar
  11. Christiansen JS, Jobling M (1990) The behaviour and the relationship between food intake and growth of juvenile Arctic charr, Salvelinus alpinus L., subjected to sustained exercise. Can J Zool 68(10):2185–2191. CrossRefGoogle Scholar
  12. Fernö A, Huse I, Juell JE, Bjordal Å (1995) Vertical distribution of Atlantic salmon (Salmo salar L.) in net pens: trade-off between surface light avoidance and food attraction. Aquaculture 132(3-4):285–296. CrossRefGoogle Scholar
  13. Gilbert CH (1912) Age at maturity of the Pacific coast salmon of the genus Oncorhynchus. Fish Bull 32:1–22Google Scholar
  14. Grant JWA, Noakes DLG (1988) Aggressiveness and foraging mode of young-of-the-year brook charr, Salvelinus fontinalis (Pisces, Salmonidae). Behav Ecol Sociobiol 22(6):435–445. CrossRefGoogle Scholar
  15. Hassell EMA, Meyers PJ, Billman EJ, Rasmussen JE, Belk MC (2012) Ontogeny and sex alter the effect of predation on body shape in a livebearing fish: sexual dimorphism, parallelism, and costs of reproduction. Ecol Evol 2(7):1738–1746. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Healey MC (1991) Life history of Chinook salmon (Oncorhynchus tshawytscha). In: Groot C, Margolis L (eds) Pacific salmon life histories. UBC Press, Vancouver, pp 313–393Google Scholar
  17. Hoar WS (1953) Control and timing of fish migration. Biol Rev Camb Philos Soc 28(4):437–452. CrossRefGoogle Scholar
  18. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363. CrossRefPubMedGoogle Scholar
  19. Huntingford FA, Adams CE (2005) Behavioural syndromes in farmed fish: implications for production and welfare. Behaviour 142(9):1207–1221. CrossRefGoogle Scholar
  20. Imre I, McLaughlin RL, Noakes DLG (2002) Phenotypic plasticity in brook charr: changes in caudal fin induced by water flow. J Fish Biol 61(5):1171–1181. CrossRefGoogle Scholar
  21. Johnson MA, Friesen TA (2014) Genetic diversity and population structure of spring Chinook Salmon from the upper Willamette River, Oregon. N Am J Fish Manag 34(4):853–862. CrossRefGoogle Scholar
  22. Jonsson B, Jonsson N (2001) Polymorphism and speciation in Arctic charr. J Fish Biol 58(3):605–638. CrossRefGoogle Scholar
  23. Keeley ER, Parkinson EA, Taylor EB (2007) The origins of ecotypic variation of rainbow trout: a test of environmental vs. genetically based differences in morphology. J Evol Biol 20(2):725–736. CrossRefPubMedGoogle Scholar
  24. Langerhans RB, Layman CA, Langerhans AK, Dewitt TJ (2003) Habitat associated morphological divergence in two Neotropical fish species. Biol J Linn Soc 80(4):689–698. CrossRefGoogle Scholar
  25. Langerhans RB, Layman CA, Mona Shokrollahi A, DeWitt TJ (2004) Predator driven phenotypic diversification in Gambusia affinis. Evolution 58(10):2305–2318. CrossRefPubMedGoogle Scholar
  26. Martin WR (1949) The mechanics of environmental control of body form in fishes. Publications of the Ontario Fisheries Research Laboratory, U Toronto Biol Ser 70:1–72Google Scholar
  27. Mclaughlin RL, Grant JWA, Kramer DL (1992) Individual variation and alternative patterns of foraging movements in recently emerged brook charr (Salvelinus fontinalis). Behaviour 120(3):286–301. CrossRefGoogle Scholar
  28. McLaughlin RL, Grant JWA, Kramer DL (1994) Foraging movements in relation to morphology, water-column use, and diet for recently emerged brook trout (Salvelinus fontinalis) in still-water pools. Can J Fish Aquat Sci 51(2):268–279. CrossRefGoogle Scholar
  29. Metcalfe NB, Thorpe JE (1992) Early predictors of life-history events: the link between first feeding date, dominance and seaward migration in Atlantic salmon, Salmo salar L. J Fish Biol 41(sb):93–99. CrossRefGoogle Scholar
  30. O’Malley KG, Camara MD, Banks MA (2007) Candidate loci reveal genetic differentiation between temporally divergent migratory runs of Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 16(23):4930–4941. CrossRefPubMedGoogle Scholar
  31. Pakkasmaa S, Piironen J (2000) Water velocity shapes juvenile salmonids. Evol Ecol 14(8):721–730. CrossRefGoogle Scholar
  32. Pavlov DS, Kostin VV, Ponomareva VY (2010) Behavioral differentiation of underyearlings of the Black Sea salmon Salmo trutta labrax: Rheoreaction in the year preceding smoltification. J Ichthyol 50(3):270–280. CrossRefGoogle Scholar
  33. Perkins TA, Jager HI (2011) Falling behind: delayed growth explains life history variation in Snake River fall Chinook salmon. T Am Fish Soc 140(4):959–972. CrossRefGoogle Scholar
  34. Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University of Washington Press, SeattleGoogle Scholar
  35. Reinhardt UG (2001) Selection for surface feeding in farmed and sea-ranched Masu salmon juveniles. T Am Fish Soc 130(1):155–158.<0155:SFSFIF>2.0.CO;2 CrossRefGoogle Scholar
  36. Rohlf FJ (2003) tpsRegr, shape regression, version 1.28. Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
  37. Rohlf FJ (2010a) tpsDig, version 2.16. Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
  38. Rohlf FJ (2010b) tpsRelw, relative warps, version 1.49. Department of Ecology and Evolution, State University of New York at Stony BrookGoogle Scholar
  39. SAS Institute (2008) SAS 9.2 help and documentation. CaryGoogle Scholar
  40. Schroeder RK, Whitman LD, Cannon B, Olmstead P (2016) Juvenile life-history diversity and population stability of spring in Chinook salmon in the Willamette River basin, Oregon. Can J Fish Aquat Sci 73(6):921–934. CrossRefGoogle Scholar
  41. Scott LE, Johnson JB (2010) Does sympatry predict life history and morphological diversifications in the Mexican livebearing fish Poeciliopsis baenschi? Biol J Linn Soc 100(3):608–618. CrossRefGoogle Scholar
  42. Skúlason S, Smith TB (1995) Resource polymorphisms in vertebrates. Trends Ecol Evol 10(9):366–370. CrossRefPubMedGoogle Scholar
  43. Tiffan KF, Connor WP (2011) Distinguishing between natural and hatchery Snake River fall Chinook salmon subyearlings in the field using body morphology. T Am Fish Soc 140:21–30Google Scholar
  44. Vincent RE (1960) Some influences of domestication upon three stocks of brook trout (Salvelinus fontinalis Mitchill). T Am Fish Soc 89(1):35–52.[35:SIODUT]2.0.CO;2 CrossRefGoogle Scholar
  45. Waples RS et al (2001) Characterizing diversity in salmon from the Pacific northwest. J Fish Biol 59:1–41Google Scholar
  46. Wesner JS, Billman EJ, Meier A, Belk MC (2011) Morphological convergence during pregnancy among predator and nonpredator populations of the livebearing fish Brachyrhaphis rhabdophora (Teleostei: Poeciliidae). Biol J Linn Soc 104(2):386–392. CrossRefGoogle Scholar
  47. Zimmerman MS, Krueger CC, Eshenroder RL (2006) Phenotypic diversity of lake trout in great slave lake: differences in morphology, buoyancy, and habitat depth. T Am Fish Soc 135(4):1056–1067. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2017

Authors and Affiliations

  • Julia R. Unrein
    • 1
    • 2
  • Eric J. Billman
    • 3
  • Karen M. Cogliati
    • 1
    • 2
  • Rob Chitwood
    • 1
    • 2
  • David L. G. Noakes
    • 2
    • 4
  • Carl B. Schreck
    • 5
  1. 1.Oregon Cooperative Fish and Wildlife Research UnitOregon State UniversityCorvallisUSA
  2. 2.Fisheries and Wildlife DepartmentOregon State UniversityCorvallisUSA
  3. 3.Department of BiologyBrigham Young University IdahoRexburgUSA
  4. 4.Oregon Hatchery Research CenterAlseaUSA
  5. 5.U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, U.S.G.SOregon State UniversityCorvallisUSA

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