Environmental Biology of Fishes

, Volume 93, Issue 3, pp 343–355 | Cite as

Individual condition and stream temperature influence early maturation of rainbow and steelhead trout, Oncorhynchus mykiss

  • John R. McMillan
  • Jason B. Dunham
  • Gordon H. Reeves
  • Justin S. Mills
  • Chris E. Jordan


Alternative male phenotypes in salmonine fishes arise from individuals that mature as larger and older anadromous marine-migrants or as smaller and younger freshwater residents. To better understand the processes influencing the expression of these phenotypes we examined the influences of growth in length (fork length) and whole body lipid content in rainbow trout (Oncorhynchus mykiss). Fish were sampled from the John Day River basin in northeast Oregon where both anadromous (“steelhead”) and freshwater resident rainbow trout coexist. Larger males with higher lipid levels had a greater probability of maturing as a resident at age-1+. Among males, 38% were maturing overall, and the odds ratios of the logistic model indicated that the probability of a male maturing early as a resident at age-1+ increased 49% (95% confidence interval (CI) = 23–81%) for every 5 mm increase in length and 33% (95% CI = 10–61%) for every 0.5% increase in whole body lipid content. There was an inverse association between individual condition and water temperature as growth was greater in warmer streams while whole body lipid content was higher in cooler streams. Our results support predictions from life history theory and further suggest that relationships between individual condition, maturation, and environmental variables (e.g., water temperature) are shaped by complex developmental and evolutionary influences.


Rainbow trout Steelhead trout Alternative male phenotypes Resident male maturity Anadromy Life history 



All sampling was conducted in accordance with the Oregon Department of Fish and Wildlife permit # OR2007-3680 M1 approved by NOAA and USFWS under the Endangered Species Act. Tim Unterwegner, Jim Ruzycki, Jeff Neal, Shelly Miller, and Chris James at ODFW helped identify survey locations and provided critical information on the John Day River basin. Nick Weber, Ian Tattam, Jeremiah Leslie assisted in data collection. Martin Fitzpatrick at USGS provided suggestions that improved the methods and manuscript. Funding was provided by NOAA, USGS, USFS, and the North Umpqua Foundation. Use of trade or firm names is for reader information only and does not constitute endorsement of any product or service by the U.S. Government.


  1. Adams SM, Ham KD, LeHew RF (1998) A framework for evaluating organism responses to multiple stressors: mechanisms of effect and importance of modifying ecological factors. In: Cech JJ, Wilson BW (eds) Multiple Stresses in Ecosystems. Lewis Pubs, Boca Raton, FL, pp 13–22Google Scholar
  2. Allison PD (1999) Logistic regression using the SAS system: theory and application. SAS Institute Inc., Cary, NCGoogle Scholar
  3. Anonymous (1987) Determination of total crude fat in plant materials and feeding stuffs with the Soxtec Hydrolyzing system. Tecator Appl Note AN 92: 1 – 6Google Scholar
  4. AOAC (1998) Official Methods of Analysis. 15th ed. Method 922.06. Association of Official Analytical Chemists. Arlington, VA.Google Scholar
  5. Aubin-Horth N, Borque JF, Daigle G, Hedger R, Dodson JJ (2006) Longitudinal gradients in threshold sizes for alternative male life history tactics in a population of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 63:2067–2075CrossRefGoogle Scholar
  6. Bacon PJ, Gurney WSC, Jones W, McLaren IS, Youngson AF (2005) Seasonal growth patterns of wild juvenile fish: partitioning variation among explanatory variables, based on individual growth trajectories of Atlantic salmon (Salmo salar) parr. Ecology 74:1–11Google Scholar
  7. Bagliniere JL, Maisse G (1985) Precocious maturation and smoltification in wild Atlantic salmon in the Armorican Massif, France. Aquaculture 45:249–263CrossRefGoogle Scholar
  8. Baum D, Laughton R, Armstrong JD, Metcalfe NB (2004) Altitudinal variation in the relationship between growth and maturation rate in salmon parr. J Anim Ecol 73:253–260CrossRefGoogle Scholar
  9. Baum D, Laughton R, Armstrong JD, Metcalfe NB (2005) The effect of temperature on growth and early maturation in a wild population of Atlantic salmon parr. J Fish Biol 67:1370–1380CrossRefGoogle Scholar
  10. Behnke RJ (2002) Trout and salmon of North America. The Free Press, Simon and Schuster, New York, NYGoogle Scholar
  11. Berg OK, Bremset G (1998) Seasonal changes in body composition of young riverine, Atlantic salmon and brown trout. J Fish Biol 52:1272–1288CrossRefGoogle Scholar
  12. Biro PA, Morton AE, Post JR, Parkinson EA (2004) Overwinter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 61:1513–1519CrossRefGoogle Scholar
  13. Brett JR (1952) Temperature tolerance in young Pacific Salmon, genus Oncorhynchus sp. J Fisheries Res Board Can 9:265–323CrossRefGoogle Scholar
  14. Brett JR (1979) Energetic factors and growth. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol 8, Academic Press. New York, NY, pp 575–599Google Scholar
  15. Brown LR, Moyle PB (1991) Changes in habitat and microhabitat partitioning within an assemblage of stream fishes in response to predation by Sacramento squawfish(Ptychocheilus grandis). Can J Fish Aquat Sci 48:849–856CrossRefGoogle Scholar
  16. Busby PJ, Wainwright TC, Bryant GJ, Lierheimer LJ, Waples RS, Waknitz FW, Lagomarsino IV (1996) Status review of West Coast steelhead from Washington, 46 Idaho, Oregon, and California NOAA Tech. Memo. NMFS-NWFSC-27. United States Department of Commerce.Google Scholar
  17. Chapman DG (1951) Some properties of the hypergeometric distribution applications to zoological censuses. Univ Calif Publ Stat 1(7):131–160Google Scholar
  18. Chernoff E, Curry RA (2007) First summer growth predetermined in anadromous and resident brook charr. J Fish Biol 70:334–346CrossRefGoogle Scholar
  19. Christie MR, Marine ML, Blouin MS (2011) Who are the missing parents? Grandparentage analysis identifies multiple sources of gene flow into a wild population. Mol Ecol 20:1263–1276PubMedCrossRefGoogle Scholar
  20. Clemens BJ, Crawford SS (2009) The ecology of body size and depth use by bloater (Coregonus hoyi Gill) in the Laurentian Great Lakes: patterns and hypotheses. Rev Fisheries Sci 17(2):174–186CrossRefGoogle Scholar
  21. Dunham JB, Chandler G., Rieman BE, Martin D (2005) Measuring stream temperature with digital data loggers- A user’s guide: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Center General Technical Report RMRS-GTR-150WWW.Google Scholar
  22. Einum S, Fleming IA (1999) Maternal effects of egg size in brown trout (Salmo trutta): norms of reaction to environmental quality. Proc R Soc Lond, Ser B 266:2095–2100CrossRefGoogle Scholar
  23. Emling ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223CrossRefGoogle Scholar
  24. Feldhaus JW (2006) The Physiological Ecology of Redband Rainbow Trout (Oncorhynchus mykiss gairdneri) in the South Fork John Day River, Oregon. Master’s Thesis. Oregon State University, Corvallis, OregonGoogle Scholar
  25. Flain M, Glova GJ (1988) A test of the reliability of otolith and scale readings of Chinook salmon (Oncorhynchus tshawytscha). NZ J Mar Freshw Res 22:497–500CrossRefGoogle Scholar
  26. Fleming IA, Reynolds JD (2004) Salmonid breeding systems. In: Hendry AP, Stearns SC (eds) Evolution Illuminated: Salmon and their relatives. Oxford University Press, New York, NY, pp 264–294Google Scholar
  27. Gibbons JW, Hook JT, Forney DL (1972) Winter responses of largemouth bass to heated effluent from a nuclear reactor. Progres Fish Cult 34:88–90CrossRefGoogle Scholar
  28. Graham TP (1974) Chronic malnutrition in four species of sunfish in a thermally loaded impoundment. In: Gibbons JW, Sharitz RR (eds) Thermal Ecology. AEC symposium series, CONF-730505. National Technical Information Center, Springfield, pp 151–157Google Scholar
  29. Grimes DV (1993) Vitellolipid and vitelloprotein profiles of environmentally stressed and nonstressed populations of striped bass. Trans Am Fisheries Soc 122:636–641CrossRefGoogle Scholar
  30. Gross MR (1991) Salmon breeding behavior and life history evolution in changing environments. Ecology 72(4):1180–1186CrossRefGoogle Scholar
  31. Gross MR, Repka J (1998) Stability with inheritance in the conditional strategy. J Theor Biol 192:445–453PubMedCrossRefGoogle Scholar
  32. Houston, CJG (1981) Factors affecting precocious sexual development in male rainbow trout. Master’s Thesis, University of British Columbia.Google Scholar
  33. Jones MW, Hutchings JA (2001) The influence of male parr body size and mate competition on fertilization success and effective population size in Atlantic salmon. J Heredity 86:675–684CrossRefGoogle Scholar
  34. Jones JW, Orton JH (1940) The paedogenetic male cycle in Salmo salar L. Proc R Soc Lond Ser B 128(853):485–499CrossRefGoogle Scholar
  35. Jonsson B (1985) Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Trans Am Fisheries Soc 114:182–194CrossRefGoogle Scholar
  36. Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fisheries 3:348–365CrossRefGoogle Scholar
  37. Kepshire BM Jr, Tinsley IJ, Lowry RR (1983) Effect of temperature on chemical composition of pink salmon (Oncorhynchus gorbuscha) muscle. Aquaculture 32:295–301CrossRefGoogle Scholar
  38. Madrinan F (2008) Biophysical factors driving the distribution and abundance of Redband/steelhead trout (Oncorhynchus mykiss gairdneri) in the South Fork John Day River basin, Oregon, USA. Ph.D. Dissertation. Oregon State University, Corvallis, OregonGoogle Scholar
  39. McCormick JL, Bult AM (2010) Implementation of the environmental Monitoring and assessment program (EMAP) protocol in the John Day Subbasin of the Columbia Plateau Province. Annual Technical Report. Prepared for: U.S.Department of Energy. Bonneville Power Administration Environment, Fish and Wildlife Portland, OR. Document ID #P118590.Google Scholar
  40. McCullough D (1999) A review and synthesis of effects of alterations to the water temperature regime on freshwater life stages of salmonids, with special reference to chinook salmon. Columbia Intertribal Fisheries Commission, Portland, OR. Prepared for the U.S. Environmental Protection Agency Region 10. Published as EPA 910-R-99-010.Google Scholar
  41. McMillan J (2009) Early maturing males in a partially migratory population of anadromous and resident rainbow trout Oncorhynchus mykiss: influences of individual condition and stream temperature. Master's Thesis, Oregon State University.Google Scholar
  42. McMillan JR, Katz SL, Pess GR (2007) Observational evidence of spatial and temporal structure in a sympatric anadromous (winter steelhead) and resident Oncorhynchus mykiss mating system on the Olympic Peninsula, Washington State. Trans Am Fisheries Soc 136:736–748CrossRefGoogle Scholar
  43. Mills JS, Dunham JB, Reeves GH, McMillan JR, Zimmerman CE, Jordan CJ (in press) Variability in expression of anadromy by female Oncorhynchus mykiss within a river network. Env Bio FishesGoogle Scholar
  44. Morales-Nin B, Panfili J (2002) Age estimation. In: Panfili J, de Pontual H, Troadec H, Wright PJ (eds) Manual of fish sclerochronology, Ifremer-IRD, Co-edition, pp. 91–98.Google Scholar
  45. Morgan IJ, McCarthy ID, Metcalfe NB (2002) The influence of life-history strategy on lipid metabolism in overwintering juvenile Atlantic salmon. J Fish Biol 60:674–686CrossRefGoogle Scholar
  46. Morinville GR, Rasmussen JB (2004) Early juvenile bioenergetic differences between anadromous and resident brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60(4):401–410CrossRefGoogle Scholar
  47. Neuheimer AB, Taggart CT (2007) Growing degree-day and fish size-at-age: the overlooked metric. Can J Fish Aquat Sci 64:375–385CrossRefGoogle Scholar
  48. Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University Press, Seattle, WAGoogle Scholar
  49. Quinn TP, Myers KW (2005) Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. Rev Fish Biol Fisheries 14:421–442CrossRefGoogle Scholar
  50. Railsback SE, Rose KA (1999) Bioenergetics modeling of stream trout growth: temperature and food consumption effects. Trans Am Fisheries Soc 128:241–256CrossRefGoogle Scholar
  51. Ramsey F, Schafer D (2002) The statistical sleuth: A course in methods of data analysis, 2nd edn. Duxbury Press, Belmont, CAGoogle Scholar
  52. Reeves GH, Everest FH, Hall JD (1987) Interactions between the redside shiner (Richardsonius balteatus) and the steelhead trout (Salmo gairdneri) in western Oregon: The influence of water temperature. Can J Fish Aquat Sci 44:1603–1613CrossRefGoogle Scholar
  53. Reshetnikov YS, Paranyushkina LP, Kiyashko VI (1970) Seasonal changes of blood serum protein composition and fat content in whitefishes. J Ichthyol 10:804–813Google Scholar
  54. Rikardsen AH, Elliot JM (2000) Variations in juvenile growth, energy allocation and life-history strategies of two populations of Arctic charr in north Norway. J Fish Biol 56:328–346CrossRefGoogle Scholar
  55. Rosenberger AE, Dunham JB (2005) Validation of abundance estimates from mark-recapture and removal techniques for rainbow trout captured by electrofishing in small streams. N Am J Fisheries Manag 25:251–262CrossRefGoogle Scholar
  56. Rowe DK, Thorpe JE (1990) Differences in growth between maturing and non-maturing male Atlantic salmon, Salmo salar L., parr. J Fish Biol 36:643–658CrossRefGoogle Scholar
  57. Rowe DK, Thorpe JE, Shanks AM (1991) Role of fat stores in the maturation of male Atlantic salmon (Salmo salar) parr. Can J Fish Aquat Sci 48:405–413CrossRefGoogle Scholar
  58. Schmidt SP, House EW (1979) Precocious sexual development in hatchery-reared and laboratory maintained male steelhead trout (Salmo gairdneri). J Fisheries Res Board Can 36:90–93CrossRefGoogle Scholar
  59. Schultz T, Wilson W, Ruzycki J, Carmichael R, Schricker J, Bondurant D (2004) Escapement and productivity of spring Chinook and summer steelhead in the John Day River basin, 2003–2004 Annual Report, Project No. 199801600, BPA Report DOE/BP-00005840-4.Google Scholar
  60. Seamons TR, Bentzen P, Quinn TP (2004) The mating system of steelhead (Oncorhynchus mykiss) inferred by molecular analysis of parents and progeny. Environ Biol Fish 69:333–344CrossRefGoogle Scholar
  61. Silverstein JT, Shimma H, Ogata H (1997) Early maturity in amago salmon (Oncorhynchus masu ishikawai): an association with energy storage. Can J Fish Aquat Sci 54(2):444–451CrossRefGoogle Scholar
  62. Simpkins DG, Hubert WA, Martinez del Rio C, Rule DC (2003) Interacting effects of water temperature and swimming activity on body composition and mortality of fasted juvenile rainbow trout. Can J Zoo 81:1641–1649CrossRefGoogle Scholar
  63. Simpson A (1992) Differences in body size and lipid reserves between maturing and nonmaturing Atlantic salmon parr, Salmo salar L. Can J Zool 70:1737–1742CrossRefGoogle Scholar
  64. Stevens DL, Olsen AR (2004) Spatially balanced sampling of natural resources. J Am Stat Assoc 99:262–278CrossRefGoogle Scholar
  65. Sutton SG, Bult TP, Haedrich RL (2000) Relationships among fat weight, body weight, water weight, and condition factors in wild Atlantic salmon parr. Trans Am Fish Soc 129:527–538CrossRefGoogle Scholar
  66. Tattam I (2006) Seasonal life history of Oncorhynchus mykiss in the South Fork John Day River Basin, Oregon. Master’s Thesis. Oregon State University, Corvallis, OregonGoogle Scholar
  67. Temple GM, Pearsons TN (2006) Evaluation of the recovery period in mark-recapture population estimates of rainbow trout in small streams. N Am J Fisheries Manag 26:941–948CrossRefGoogle Scholar
  68. Thériault V, Dodson JJ (2003) Body size and the adoption of a migratory tactic in brook charr. J Fish Biol 63(5):1144–1159CrossRefGoogle Scholar
  69. Thériault V, Garant D, Bernatchez L, Dodson JJ (2007) Heritability of life-history tactics and genetic correlation with body size in a natural population of brook charr (Salvelinus fontinalis). J Evol Biol 20(6):2266–2277PubMedCrossRefGoogle Scholar
  70. Thomaz D, Beall E, Burke T (1997) Alternative reproductive tactics in Atlantic salmon: factors affecting mature parr success. Proc R Soc Lond, Ser B 264:219–226CrossRefGoogle Scholar
  71. Thorpe JE, Mangel M, Metcalfe NB, Huntingford FA (1998) Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. Evol Ecol 12:581–599CrossRefGoogle Scholar
  72. Tipping JM, Gannam AL, Hillson TD, Poole JB (2003) Use of size for early detection of juvenile hatchery steelhead destined to become precocious males. N Am J Aquac 65:318–323CrossRefGoogle Scholar
  73. Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fisheries Sci 11:107–184CrossRefGoogle Scholar
  74. Ward BR, Slaney PA, Faccin AR, Land RW (1989) Size-biased survival in steelhead trout (Oncorhynchus mykiss): back-calculated lengths from adults’ scales compared to migrating smolts at the Keogh River, British Columbia. Can J Fish Aquat Sci 46:1853–1859CrossRefGoogle Scholar
  75. Wassermann GJ, Afonso LOB (2002) Validation of the aceto-carmine technique for evaluating phenotypic sex in Nile tilapia (Oreochromis niloticus) fry. Cienc Rural 32(1):133–139CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • John R. McMillan
    • 1
  • Jason B. Dunham
    • 2
  • Gordon H. Reeves
    • 3
  • Justin S. Mills
    • 1
  • Chris E. Jordan
    • 4
  1. 1.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  2. 2.U.S. Geological SurveyForest and Rangeland Ecosystem Science CenterCorvallisUSA
  3. 3.United States Forest Service/PNW Research StationCorvallisUSA
  4. 4.National Oceanic and Atmospheric AdministrationCorvallisUSA

Personalised recommendations