Histological assessment of organs in sexually mature and post-spawning steelhead trout and insights into iteroparity

Abstract

Steelhead trout (Oncorhynchus mykiss) are anadromous and iteroparous, but repeat-spawning rates are generally low. Like other anadromous salmonids, steelhead trout fast during freshwater spawning migrations, but little is known about the changes that occur in vital organs and tissues. We hypothesized that fish capable of repeat-spawning would not undergo the same irreversible degeneration and cellular necrosis documented in semelparous salmon. Using Snake River steelhead trout as a model we used histological analysis to assess the cellular architecture in the pyloric stomach, ovary, liver, and spleen in sexually mature and kelt steelhead trout. We observed 38 % of emigrating kelts with food or fecal material in the gastrointestinal tract. Evidence of feeding was more likely in good condition kelts, and feeding was associated with a significant renewal of villi in the pyloric stomach. No vitellogenic oocytes were observed in sections of kelt ovaries, but perinucleolar and early/late stage cortical alveolus oocytes were present suggesting iteroparity was possible. We documented a negative correlation between the quantity of perinucleolar oocytes in ovarian tissues and fork length of kelts suggesting that larger steelhead trout may invest more into a single spawning event. Liver and spleen tissues of both mature and kelt steelhead trout had minimal cellular necroses. Our findings indicate that the physiological processes causing rapid senescence and death in semelparous salmon are not evident in steelhead trout, and recovery begins in fresh water. Future management efforts to increase iteroparity in steelhead trout and Atlantic salmon must consider the physiological processes that influence post-spawning recovery.

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References

  1. Agius C, Roberts RJ (1981) Effects of starvation on the melano-macrophage centres of fish. J Fish Biol 19:161–169

    Google Scholar 

  2. Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26:499–509

    CAS  PubMed  Article  Google Scholar 

  3. Allan IRH, Ritter JA (1976) Salmonid terminology. J Conseil Int 37:293–299

    Article  Google Scholar 

  4. Arrington DA, Winemiller KO, Loftus WF, Akin S (2002) How often do fishes “run on empty”. Ecology 83:2145–2151

    Google Scholar 

  5. Barry TP, Marwag A, Nunez S (2010) Inhibition of cortisol metabolism by 17α,20β-P: mechanism mediating semelparity in salmon? Gen Comp Endocrinol 165:3–59

    Article  Google Scholar 

  6. Behnke RJ (1992) Native trout of western North America. American Fisheries Society, Bethesda

    Google Scholar 

  7. Belding DL (1934) The cause of the high mortality in the Atlantic salmon after spawning. Trans Am Fish Soc 64:219–224

    Article  Google Scholar 

  8. Blazer VS (2002) Histopathological assessment of gonadal tissue in wild fishes. Fish Physiol Biochem 26:85–101

    CAS  Article  Google Scholar 

  9. Brannon EL, Powell MS, Quinn TP, Talbot A (2004) Population structure of Columbia River basin Chinook salmon and steelhead trout. Rev Fish Sci 12:99–232

    Article  Google Scholar 

  10. Brett JR (1995) Energetics. In: Groot C, Margolis L, Clarke WC (eds) Physiological ecology of Pacific salmon. UBC Press, Vancouver, pp 3–68

    Google Scholar 

  11. Burgner RL, Light JT, Margolis L, Okazaki T, Tautz A, Ito S (1992) Distribution and origins of steelhead trout (Oncorhynchus mykiss) in offshore waters of the North Pacific. International North Pacific Fisheries Commission. Bull Number 51:1–92

    Google Scholar 

  12. Busby PJ, Wainwright TC, Bryant GJ, Lierheimer LJ, Waples RS, Waknitz FW, Lagomarsino IV (1996) Status review of west coast steelhead from Washington, Idaho, Oregon, and California. NOAA Technical Memorandum NMFS-NWFSC-27. Northwest Fisheries Science Center, Seattle. http://www.nwr.noaa.gov. (September 2004)

  13. Campbell MR, Kozfkay CC, Copeland T, Schrader WC, Ackerman MW, Narum SR (2012) Estimating abundance and life history characteristics of threatened wild Snake River steelhead stocks by using genetic stock identification. Trans Am Fish Soc 141:1310–1327

    Article  Google Scholar 

  14. 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: 14. doi:10.1111/j.1365-294X.2010.04994.x

  15. Colotelo AH, Jones BW, Harnish RA et al (2013) Passage distribution and federal Columbia River power system survival for steelhead kelts tagged above and at Lower Granite Dam. PNNL-22101 http://www.salmonrecovery.gov/Files/Comprehensive%20Evaluation/Colotelo-etal_2013_-%20Kelt-Passage-Distribution-Survival_PNWD-22101.pdf. Accessed 25 September 2013

  16. Crespi BJ, Teo R (2002) Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonids fishes. Evolution 56:1008–1020

    PubMed  Article  Google Scholar 

  17. Crim LW, Wilson CE, So YP, Idler DR, Johnston CE (1992) Feeding, reconditioning, and rematuration responses of captive Atlantic salmon (Salmo salar) kelt. Can J Fish Aquat Sci 49:1835–1842

    Article  Google Scholar 

  18. Docker MF, Heath DD (2003) Genetic comparison between sympatric anadromous steelhead and freshwater resident rainbow trout in British Columbia, Canada. Conserv Genet 4:227–231

    CAS  Article  Google Scholar 

  19. Dutil JD (1986) Energetic constraints and spawning survival in anadromous Arctic Charr (Salvelinus alpinus). Copeia 1986:954–955

  20. Eales JG, Cyr DG, Finnson K, Johnston CE (1991) Changes in plasma T4 and T3 levels during reconditioning and rematuration in male and female wild Atlantic salmon (Salmo salar) kelts held in freshwater under two photoperiod regimes. Can J Fish Aquat Sci 48:2443–2448

    CAS  Article  Google Scholar 

  21. Ehrich K, Blaxter JHS, Pemberton R (1976) Morphological and histological changes during the growth and starvation of herring and plaice larvae. Mar Biol 35:105–118

    Article  Google Scholar 

  22. Farrell AP (2002) Coronary arteriosclerosis in salmon: growing old or growing fast? Comp Biochem Physiol Part A 132:723–735

    CAS  Article  Google Scholar 

  23. Fleming IA (1998) Pattern and variability in the breeding system of Atlantic salmon (Salmo salar), with comparisons to other salmonids. Can J Fish Aquat Sci 55(Supplement 1):59–76

    Article  Google Scholar 

  24. Fleming IA, Reynolds JD (2004) Salmon breeding systems. In: Hendry AP, Stearns SC (eds) Evolution illuminated salmon and their relatives. Oxford University Press, USA, pp 264–294

    Google Scholar 

  25. Franklin CE, Davison W, Mckenzie JC (1993) The role of the spleen during exercise in the Antarctic teleost, Pagothenia Borchgrevinki. J Exp Biol 174:381–386

    Google Scholar 

  26. French CJ, Hochachka PW, Mommsen TP (1983) Metabolic organization of liver during spawning migration sockeye salmon. Am J Physiol 245:R827–R830

    CAS  PubMed  Google Scholar 

  27. Gamper AK, Pinder AW, Boutilier RG (1994) Effect of coronary ablation and adrenergic stimulation on in vivo cardiac performance in trout (Oncorhynchus mykiss). J Exp Biol 186:127–143

    Google Scholar 

  28. Garner SR, Heath JW, Neff BD (2009) Egg consumption in mature Pacific salmon (Oncorhynchus sp.). Can J Fish Aquat Sci 66:1546–1553

    Article  Google Scholar 

  29. Gauthier D, Desjardins L, Robitaille JA, Vigneault Y (1989) River spawning of artificially reconditioned Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 46:824–826

    Article  Google Scholar 

  30. Gephard S, McMenemy J (2004) An overview of the program to restore Atlantic salmon and other diadromous fishes to the Connecticut Rover with notes on the current status of these species in the river. Am Fish Soc Monogr 9:287–317

    Google Scholar 

  31. Green CW (1913) Anatomy and histology of the alimentary tract of the king salmon. Bull Bureau Fish 33:73–104

    Google Scholar 

  32. Green CW (1916) On some quantitative physiological changes in the Pacific salmon during the run to the spawning grounds. Trans Am Fish Soc 45:5–12

    Article  Google Scholar 

  33. Gross MR (1987) Evolution of diadromy in fishes. Am Fish Soc Symp 1:14–25

    Google Scholar 

  34. Hane S, Robertson OH (1959) Changes in plasma 17-hydoxycorticosteroids accompanying sexual maturation and spawning of the Pacific salmon (Oncorhynchus tschawtscha) and rainbow trout (Salmo gairdnerii). Proc Natl Acad Sci USA 45:886–893

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  35. Hatch D, Anders P, Evans A, Blodgett J, Bosch B, Fast D, Newsome T (2002) Kelt reconditioning: a research project to enhance iteroparity in Columbia basin steelhead (Oncorhynchus mykiss). 2001 Annual Report. Project No. 200001700, 89 electronic pages (BPA Report DOE/BP-00004185-2) Bonneville

  36. Hatch DR, Fast DE, Bosch WJ, Blodgett JW, Whiteaker JM, Branstetter R, Pierce AL (2013) Survival and traits of reconditioned kelt steelhead Oncorhynchus mykiss in the Yakima River, Washington. N Am J Fish Manag 33:615–625

  37. Hochachka PW (1961) Liver glycogen reserves of interacting resident and introduced trout populations. J Fish Res Board Can 18:125–135

    CAS  Article  Google Scholar 

  38. Hur JW, Jo JH, Park IS (2006) Effects of long-term starvation on hepatocyte ultrastructure of olive flounder Paralichthys olivaceus. Ichthyol Res 53:306–310

    Article  Google Scholar 

  39. Johansen MJ (2001) Evidence of freshwater feeding by adult salmon in the Tana River, northern Norway. J Fish Biol 59:1405–1407

    Article  Google Scholar 

  40. Johnston CE, Gray RW, McLennan A, Paterson A (1987) Effects of photoperiod, temperature, and diet on the reconditioning response, blood chemistry, and gonad maturation of Atlantic salmon (Salmo salar) held in freshwater. Can J Fish Aquat Sci 44:702–711

    CAS  Article  Google Scholar 

  41. Johnston CE, Farmer SR, Gray RW, Hambrook M (1990) Reconditioning and reproductive responses of Atlantic salmon kelts (Salmo salar) to photoperiod and temperature manipulation. Can J Fish Aquat Sci 47:701–710

    Article  Google Scholar 

  42. Johnston CE, Hambrook MJ, Gray RW, Davidson KG (1992) Manipulation of reproductive function in Atlantic salmon (Salmo salar) kelts with controlled photoperiod and temperature. Can J Fish Aquat Sci 49:2055–2061

    Article  Google Scholar 

  43. Jones B (2013) Migratory and physiological characteristics of steelhead kelts from the Clearwater River, Idaho, and Lower Granite Dam, Washington. Master’s thesis, University of Idaho

  44. Jonsson N, Hansen LP, Jonsson B (1991) Variation in age, size, and repeat spawning of adult Atlantic salmon in relation to river discharge. J Anim Ecol 60:937–947

    Article  Google Scholar 

  45. Keefer ML, Wertheimer RH, Evans AF, Boggs CT, Peery CA (2008) Iteroparity in Columbia River summer-run steelhead (Oncorhynchus mykiss): implications for conservation. Can J Fish Aquat Sci 65:2592–2605

    Article  Google Scholar 

  46. Kita J, Itazawa Y (1989) Release of erythrocytes from the spleen during exercise and splenic constriction by adrenaline infusion in the rainbow trout. Jpn J Ichthyol 36:48–52

    Google Scholar 

  47. Krogdahl Å, Bakke-McKellep AM (2005) Fasting and refeeding cause rapid changes in intestinal mass and digestive enzyme capacities of Atlantic salmon (Salmo salar L.). Comp Biochem Physiol Part A 141:450–460

    Article  Google Scholar 

  48. Kullgren A, Samuelsson LM, Joakim Larsson DG, Gjornsson BT, Bergman EJ (2010) A metabolic approach to elucidate effects of food deprivation in juvenile rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 299:R1440–R1448

    CAS  PubMed  Google Scholar 

  49. Luna LG (1968) Manual of histological staining methods of the Armed Forces Institute of Pathology, 3rd edn. McGraw-Hill Book Company, New York

    Google Scholar 

  50. Mader SS (2001) Biology, 7th edn. McGraw-Hill Inc., New York, pp 786–789

    Google Scholar 

  51. McDowall RM (1987) The occurrence and distribution of diadromy among fishes. Am Fish Soc Symp 1:1–13

    Google Scholar 

  52. McPhee MV, Quinn TP (1998) Factors affecting the duration of nest defense and reproductive lifespan of female sockeye salmon, Oncorhynchus nerka. Environ Biol Fishes 52:369–375

    Article  Google Scholar 

  53. Mizuno S, Misaka N, Miyakoshi Y, Takeuchi K, Kasahara N (2002) Effects of starvation on melano-macrophages in the kidney of masu salmon (Oncorhynchus masou). Aquaculture 209:247–255

    Article  Google Scholar 

  54. Mommsen TP, French CJ, Hochachka PW (1980) Sites and patterns of protein and amino acid utilization during the spawning migration of salmon. Can J Zool 58:1785–1799

    CAS  Article  Google Scholar 

  55. Morbey YE, Brassil CE, Hendry AP (2005) Rapid senescence in Pacific salmon. Am Nat 166:556–568

    PubMed  Article  Google Scholar 

  56. Mumford S, Heidel J, Smith C, Morrison J, MacConnell B, Blazer V (2007) Fish histology and histopathology. United States Fish and Wildlife Service Manual. http://training.fws.gov/EC/Resources/Fish_Histology/Fish_Histology_Manual_v4.pdf

  57. Narum SR, Hatch D, Talbot A, Moran P, Powell M (2008) Iteroparity in complex mating systems of steelhead Oncorhynchus mykiss (Walbaum). J Fish Biol 72:45–60

    Article  Google Scholar 

  58. Nielsen JL, Byrne A, Graziano SL, Kozfkay CC (2009) Steelhead genetic diversity at multiple spatial scales in a managed basin: Snake River, Idaho. N Am J Fish Manag 29:680–701

    Article  Google Scholar 

  59. Null RE, Niemela KS, Hamelberg SF (2013) Post-spawn migrations of hatchery-origin Oncorhynchus mykiss kelts in the Central Valley of California. Environ Biol Fishes 96:341–353

    Article  Google Scholar 

  60. Olsen RE, Sundell K, Mayhew TM, Myklebust R, Ringǿ E (2005) Acute stress alters intestinal function of rainbow trout Oncorhynchus mykiss (Walbaum). Aquaculture 250:480–495

    CAS  Article  Google Scholar 

  61. Olsen RE, Sundell K, Ringǿ E, Myklebust R, Hemre G, Hansen T, Karlsen Ø (2008) The acute stress response in fed and food deprived Atlantic cod, Gadus morhua L. Aquaculture 280:232–241

    Article  Google Scholar 

  62. Pascual M, Bentzen P, Rossi CR, Mackey G, Kinnison MT, Walker R (2001) First documented case of anadromy in a population of introduced rainbow trout in Patagonia, Argentina. Trans Am Fish Soc 130:53–67

    Article  Google Scholar 

  63. Passantino L, Santamaria N, Zupa R, Pousis C, Garafalo R, Cianciotta A, Jirilli E, Acone F, Corriero A (2013) Liver melanomacrophage centres as indicators of Atlantic bluefin tuna, Thunnus thynnus L. well-being. J Fish Dis. doi:10.111/jfd.12102

  64. Pearse DE, Hayes SA, Bond MH, Hanson CV, Anderson EC, MacFarlane RB, Garza JC (2009) Over the falls? Rapid evolution of ecotypic differentiation in steelhead/rainbow trout (Oncorhynchus mykiss). J Hered 100:515–525

    CAS  PubMed  Article  Google Scholar 

  65. Penney ZP, Moffitt CM (in press) Proximate composition and energy density of stream-maturing adult steelhead during upstream migration, sexual maturity, and kelt emigration. Transactions of the American Fisheries Society

  66. Phleger CF (1971) Liver triglyceride failure in postspawning salmon. Lipids 6:347–349

    CAS  PubMed  Article  Google Scholar 

  67. Quinn TP, Myers KW (2004) Anadromy and the marine migrations of Pacific salmon and trout: Rounsefell revisited. Rev Fish Biol Fish 14:421–442

    Article  Google Scholar 

  68. Rebok K, Joranova M, Tavciovska-Vasileva I (2011) Spleen histology in the female Ohrid trout, Salmo letnica (Kar.) (Teleostei, Salmonidae) during the reproductive cycle. Arch Biol Sci 63:1023–1030

    Article  Google Scholar 

  69. Rideout RM, Tomkiewicz J (2011) Skipped spawning in fishes: more common than you think. Mar Coast Fish 3(1):176–189

    Article  Google Scholar 

  70. Rideout RM, Rose GA, Burton MPM (2005) Skipped spawning in female iteroparous fishes. Fish Fish 6:50–72

    Article  Google Scholar 

  71. Rios FS, Donatti L, Fernandes MN, Kalinin AL, Rantin FT (2007) Liver histopathology and accumulation of melano-macrophage centres in Hoplias malabaricus after long-term food deprivation and re-feeding. J Fish Biol 71:1393–1406

    Article  Google Scholar 

  72. Robertson OH, Wexler BC (1959) Hyperplasia on the adrenal cortical tissue in Pacific salmon (Genus Oncorhynchus) and rainbow trout (Salmo gairdnerii) accompanying sexual maturation and spawning. Endocrinology 65:225–238

    Google Scholar 

  73. Robertson OH, Wexler BC (1960) Histological changes in the organs and tissues of migrating and spawning Pacific salmon (Genus Oncorhynchus). Endocrinology 66:222–239

    CAS  PubMed  Article  Google Scholar 

  74. Robertson OH, Wexler BC, Miller BF (1961) Degenerative changes in the cardiovascular system of spawning Pacific salmon (Oncorhynchus tshawtscha). Circ Res 9:826–834

    CAS  PubMed  Article  Google Scholar 

  75. Saunders RL, Farrell AP (1988) Coronary arteriosclerosis in Atlantic salmon: no regression of lesions after spawning. Arteriorsclerosis 8:378–394

    CAS  Article  Google Scholar 

  76. Schaffer WM, Elson PF (1975) The adaptive significance of variations in life history among local populations of Atlantic salmon in North America. Ecology 56:577–590

    Article  Google Scholar 

  77. Seamons TR, Quinn TP (2010) Sex-specific patterns of lifetime reproductive success in single and repeat breeding steelhead trout (Oncorhynchus mykiss). Behav Ecol Sociobiol 64:505–513

    Article  Google Scholar 

  78. Secor SM, Lane JS, Whang EE, Ashley SW, Diamond J (2002) Luminal nutrient signals for intestinal adaptation in pythons. Am J Gastrointest Physiol 283:G1298–G1309

    CAS  Article  Google Scholar 

  79. Talbot C, Stagg RM, Eddy FB (1992) Renal, respiratory and ionic regulation in Atlantic salmon (Salmo salar L.) kelts following transfer from freshwater to seawater. J Comp Physiol 162:358–364

    CAS  Google Scholar 

  80. Thrower FP, Hard JJ, Joyce JE (2004) Genetic architecture of growth and early life-history transitions in anadromous and derived freshwater populations of steelhead. J Fish Biol 65(Supplement A):286–307

    Article  Google Scholar 

  81. Tsiger VV, Skirin VI, Krupyanko NI, Kashlin KA, Semenchenko AY (1994) Life history form of male masu salmon (Oncorhynchus masou) in South Primore, Russia. Can J Fish Aquat Sci 51:197–208

    Article  Google Scholar 

  82. Unwin MJ, Kinnison MT, Quinn TP (1999) Exceptions to semelparity: postmaturation survival, morphology, and energetic of male Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 56:1172–1181

    Article  Google Scholar 

  83. Vijayan MM, Moon TW (1992) Acute handling stress alters hepatic glycogen metabolism in food-deprived rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 49:2260–2266

    CAS  Article  Google Scholar 

  84. Viola AE, Schuck ML (1995) A method to reduce the abundance of residual hatchery steelhead in rivers. N Am J Fish Manag 15:488–493

    Article  Google Scholar 

  85. Wang T, Hung CY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251

    PubMed  Article  Google Scholar 

  86. Wertheimer RH (2007) Evaluation of a surface flow bypass system for steelhead kelt passage at Bonneville Dam, Washington. N Am J Fish Manag 27:21–29

    Article  Google Scholar 

  87. Wertheimer RH, Evans AF (2005) Downstream passage of steelhead kelts through hydroelectric dams on the lower Snake and Columbia Rivers. Trans Am Fish Soc 134:853–865

    Article  Google Scholar 

  88. Winfree RA, Kindschi GA, Shaw HT (1998) Elevated water temperature, crowding, and food deprivation accelerate fin erosion in juvenile steelhead. Prog Fish Cult 60:192–199

    Article  Google Scholar 

  89. Wingfield B (1976) Holding summer steelhead adults over to spawn a second year. Northwest Fish Cult Conf 27:63–64

    Google Scholar 

  90. Wolf JC, Wolfe MJ (2005) A brief overview of nonneoplastic hepatic toxicity in fish. Toxicol Pathol 33:75–85

    CAS  PubMed  Article  Google Scholar 

  91. Zeng LQ, Li FJ, Li XM, Cao AD, Fu SJ, Zhang YG (2012) The effects of starvation on digestive tract function and structure in juvenile southern catfish (Siluris meridionalis Chen). Comp Biochem Physiol Part A 162:200–211

    CAS  Article  Google Scholar 

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Acknowledgments

Funding for this study was provided by the Columbia River Inter-Tribal Fish Commission through the Columbia Basin Fish Accords partnership with the Bonneville Power Administration under project 2007-401-00, Doug Hatch, project manager. We thank the staff at Dworshak National Fish hatchery for their cooperation with sampling. The US Army Corps of Engineers, and Nez Perce Tribe provided assistance with logistics of sampling at Lower Granite Dam juvenile fish bypass facility. We thank Dr. Rajan Bawa and staff at Colorado Histo-prep for processing tissues samples for microscopic analysis. Ann Norton, Boling Sun, James Nagler, Chris Williams, Andrew Pierce, and Victor Cajas of the University of Idaho provided invaluable assistance in interpretation of samples, laboratory and field assistance. We thank Amy Long, Vicki Blazer, Bill Ardren, and two anonymous reviewers for their suggestions and scientific critique of this manuscript. Additional sampling support was provided by Aaron Penney, Jessica Buelow, Kala Hamilton, Andrew Pape, William Schrader, Martin Perales, Veatasha Dorsey, and Bryan Jones. This study was performed under the auspices of University of Idaho protocol # 2009–2010. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Christine M. Moffitt.

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Penney, Z.L., Moffitt, C.M. Histological assessment of organs in sexually mature and post-spawning steelhead trout and insights into iteroparity. Rev Fish Biol Fisheries 24, 781–801 (2014). https://doi.org/10.1007/s11160-013-9338-2

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Keywords

  • Iteroparity
  • Histology
  • Steelhead trout
  • Fasting