Utilization of an endocrine growth index, insulin-like growth factor binding protein (IGFBP)-1b, for postsmolt coho salmon in the Strait of Georgia, British Columbia, Canada

  • Nobuto Kaneko
  • Meredith L. Journey
  • Chrys M. Neville
  • Marc Trudel
  • Brian R. Beckman
  • Munetaka ShimizuEmail author


Monitoring the growth of salmon during their early marine phase provides insights into prey availability, and growth rates may be linked to risks of size-dependent mortality. However, the measurement of growth rate is challenging for free-living salmon in the ocean. Insulin-like growth factor (IGF)-I is a growth-promoting hormone that is emerging as a useful index of growth in salmon. In addition, laboratory-based studies using coho salmon have shown that one of circulating IGF-binding proteins (IGFBPs), IGFBP-1b, is induced by fasting and thus could be used as an inverse index of growth and/or catabolic state in salmon. However, few studies have measured plasma levels of IGFBP-1b in salmon in the wild. We measured plasma IGFBP-1b levels for postsmolt coho salmon collected in the Strait of Georgia and surrounding waters, British Columbia, Canada, and compared regional differences in IGFBP-1b to ecological information such as seawater temperature and stomach fullness. Plasma IGFBP-1b levels were the highest in fish from Eastern Johnstone Strait and relatively high in Queen Charlotte Strait and Western Johnstone Strait, which was in good agreement with the poor ocean conditions for salmon hypothesized to occur in that region. The molar ratio of plasma IGF-I to IGFBP-1b, a theoretical parameter of IGF-I availability to the receptor, discriminated differences among regions better than IGF-I or IGFBP-1b alone. Our data suggest that plasma IGFBP-1b reflects catabolic status in postsmolt coho salmon, as highlighted in fish in Eastern Johnston Strait, and is a useful tool to monitor negative aspects of salmon growth in the ocean.


Insulin-like growth factor binding protein-1b Inverse index of growth Insulin-like growth factor I Endocrine growth indices Coho salmon Strait of Georgia 



The authors wish to thank Mary Thiess, John Morris, Tyler Zubkowski, Yeongha (Johan) Jung, and Carol Cooper for their assistance with the organization of survey and sampling and the crews of the C.C.G.S. W.E. Ricker, and the F/V Viking Storm, Larissa Rohrbach, Dina Spangenberg and Shelly Nance for the laboratory support.


This work was financially supported by the Japan Society for the Promotion Science (JSPS), KAKENHI Grant Numbers 16H0496606 (Munetaka Shimizu), JSPS Research Fellow (16J0343706; Nobuto Kaneko), Fisheries and Oceans Canada, the Pacific Salmon Commission (Brian R. Beckman and Marc Trudel), and the National Marine Fisheries Service International Science grant (Brian R. Beckman).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was carried out in accordance with all applicable international, national, and/or institutional guidelines for the care and use of animals.

Supplementary material

10695_2019_681_MOESM1_ESM.pdf (18 kb)
ESM 1 (PDF 18 kb)


  1. Allard JB, Duan C (2018) IGF-binding proteins: why do they exist and why are there so many? Front Endocrinol 9:117CrossRefGoogle Scholar
  2. Andrews KS, Beckman BR, Beaudreau AH, Larsen DA, Williams GD, Levin PS (2011) Suitability of insulin-like growth factor 1 (IGF1) as a measure of relative growth rates in lingcod. Mar Coast Fish 3:250–260CrossRefGoogle Scholar
  3. Balic D, Latifagic A, Hudic I (2008) Insulin-like growth factor-binding protein-1 (IGFBP-1) in cervical secretions as a predictor of preterm delivery. J Matern Fetal Neonatal Med 21:297–300CrossRefGoogle Scholar
  4. Beacham TD, Beamish RJ, Neville CM, Candy JR, Wallace C, Tucker S, Trudel M (2016) Stock-specific size and migration of juvenile coho salmon in British Columbia and southeastern Alaskan waters. Mar Coast Fish 8:292–314CrossRefGoogle Scholar
  5. Beamish RJ, Sweeting RM, Lange KL, Neville CM (2008) Changes in the population ecology of hatchery and wild coho salmon in the Strait of Georgia. Trans Am Fish Soc 137:503–520CrossRefGoogle Scholar
  6. Beamish RJ, Neville C, Sweeting R, Lange K (2012) The synchronous failure of juvenile Pacific salmon and herring production in the Strait of Georgia in 2007 and the poor return of sockeye salmon to the Fraser River in 2009. Mar Coast Fish 4:403–414CrossRefGoogle Scholar
  7. Beaudreau AH, Andrews KS, Larsen DA, Young G, Beckman BR (2011) Assessing the potential of plasma insulin-like growth factor-I (IGF-I) as a growth index in wild lingcod: relationships among season, size, and gonadal steroids. Mar Biol 158:439–450CrossRefGoogle Scholar
  8. Beckman BR (2011) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol 170:233–252CrossRefGoogle Scholar
  9. Beckman BR, Larsen DA, Moriyama S, Lee-Pawlak B, Dickhoff WW (1998) Insulin-like growth factor-I and environmental modulation of growth during smoltification of spring Chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 109:325–335CrossRefGoogle Scholar
  10. Beckman BR, Fairgrieve W, Cooper KA, Mahnken CVW, Beamish RJ (2004a) Evaluation of endocrine indices of growth in individual postsmolt coho salmon. Trans Am Fish Soc 133:1057–1067CrossRefGoogle Scholar
  11. Beckman BR, Shimizu M, Gadberry BA, Cooper KA (2004b) Response of the somatotropic axis of juvenile coho salmon to alterations in plane of nutrition with an analysis of the relationships among growth rate and circulating IGF-I and 41 kDa IGFBP. Gen Comp Endocrinol 135:334–344CrossRefGoogle Scholar
  12. Beckman BR, Shimizu M, Gadberry BA, Parkins PJ, Cooper KA (2004c) The effect of temperature change on the relations among plasma IGF-I, 41-kDa IGFBP, and growth rate in postsmolt coho salmon. Aquaculture 241:601–619CrossRefGoogle Scholar
  13. Bernard B, Sobandi KC, Darras V, Rollin X, Mandiki SNM, Kestemont P (2018) Influence of strain origin on osmoregulatory and endocrine parameters of two non-native strains of Atlantic salmon (Salmo salar L.). Gen Comp Endocrinol 258:205–212Google Scholar
  14. Bond MH, Beckman BR, Rohrbach L, Quinn TP (2014) Differential growth in estuarine and freshwater habitats indicated by plasma IGF1 concentrations and otolith chemistry in Dolly Varden Salvelinus malma. J Fish Biol 85:1429–1445CrossRefGoogle Scholar
  15. Buckley LJ (1984) RNA-DNA ratio: an index of larval fish growth in the sea. Mar Biol 80:291–298CrossRefGoogle Scholar
  16. Campana SE, Thorrold SR (2001) Otolith, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38Google Scholar
  17. Carter S, Li Z, Lemieux I, Alméras N, Tremblay A, Bergeron J, Poirier P, Deshaies Y, Després JP, Picard F (2014) Circulating IGFBP-2 levels are incrementally linked to correlates of the metabolic syndrome and independently associated with VLDL triglycerides. Atherosclerosis 237:645–651CrossRefGoogle Scholar
  18. Chamberlin JW, Beckman BR, Greene CM, Rice CA, Hall JE (2017) How relative size and abundance structures the relationship between size and individual growth in an ontogenetically piscivorous fish. Ecol Evol 7:6981–6995CrossRefGoogle Scholar
  19. Davis KB, Peterson BC (2006) The effect of temperature, stress, and cortisol on plasma IGF-I and IGFBPs in sunshine bass. Gen Comp Endocrinol 149:219–225CrossRefGoogle Scholar
  20. du Dot TJ, Rosen D, Richmond J, Kitaysky A, Zinn S, Trites A (2009) Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus). Comp Biochem Physiol A 152:524–534CrossRefGoogle Scholar
  21. Dyer AR, Barlow CG, Bransden MP, Carter CG, Glencross BD, Richardson N, Thomas PM, Williams KC, Carragher JF (2004) Correlation of plasma IGF-I concentrations and growth rate in aquacultured finfish: a tool for assessing the potential of new diets. Aquaculture 236:583–592CrossRefGoogle Scholar
  22. Ferriss BE, Trudel M, Beckman BR (2014) Regional and inter-annual trends in marine growth of juvenile salmon in coastal pelagic ecosystems of British Columbia, Canada. Mar Ecol Prog Ser 503:247–261CrossRefGoogle Scholar
  23. Fukuda M, Kaneko N, Kawaguchi K, Hevrøy EM, Hara A, Shimizu M (2015) Development of a time-resolved fluroimmunoassay for salmon insulin-like growth factor binding protein-1b. Comp Biochem Physiol A 187:66–73CrossRefGoogle Scholar
  24. Gabillard JC, Weil C, Rescan PY, Navarro I, Gutierrez J, Le Beil PY (2005) Does the GH/IGF system mediate the effect of water temperature on fish growth? A review. Cybium 29(2):107–117Google Scholar
  25. Healey MC (1982) Timing and relative intensity of size-selective mortality of juvenile chum salmon (Oncorhynchus keta) during early sea life. Can J Fish Aquat Sci 39:952–957CrossRefGoogle Scholar
  26. Hourston AS, Haegele CW (1980) Herring on Canada’s Pacific coast. Can Spec Publ Fish Aquat Sci 48:23p. BC, Canada: Department of Fisheries and OceansGoogle Scholar
  27. Johnson MW, Rooker JR, Gatlin DM III, Holt GJ (2002) Effects of variable ration levels on direct and indirect measures of growth in juvenile red drum (Sciaenops ocellatus). J Exp Mar Biol Ecol 274:141–157CrossRefGoogle Scholar
  28. Journey ML (2015) Intra and inter-annual patterns of juvenile Pacific salmon (Oncorhynchus) growth in the Strait of Georgia. Master thesis, School of Aquatic and Fisheries Sciences, University of Washington, Seattle, WashingtonGoogle Scholar
  29. Journey ML, Trudel M, Young G, Beckman BR (2017) Evidence for depressed growth of juvenile pacific salmon (Oncorhynchus) in Johnstone and Queen Charlotte Straits, British Columbia. Fish Oceanogr 00:1–10Google Scholar
  30. Kajimura S, Duan C (2007) Insulin-like growth factor-binding protein-1: an evolutionarily conserved fine tuner of insulin-like growth factor action under catabolic and stressful conditions. J Fish Biol 71:309–325CrossRefGoogle Scholar
  31. Kaneko N, Taniyama N, Inatani Y, Nagano Y, Fujiwara M, Torao M, Miyakoshi Y, Shimizu M (2015) Circulating insulin-like growth factor I in juvenile chum salmon: relationship with growth rate and changes during downstream and coastal migration in northeastern Hokkaido, Japan. Fish Physiol Biochem 41:991–1003CrossRefGoogle Scholar
  32. Kaneko N, Torao M, Koshino Y, Fujiwara M, Miyakoshi Y, Shimizu M (2019) Evaluation of growth status using endocrine growth indices, insulin-like growth factor (IGF)-I and IGF-binding protein-1b, in out-migrating juvenile chum salmon. Gen Comp Endocrinol 274:50–59CrossRefGoogle Scholar
  33. Kawaguchi K, Kaneko N, Fukuda M, Nakano Y, Kimura S, Hara A, Shimizu M (2013) Responses of insulin-like growth factor (IGF)-I and two IGF-binding protein-1 subtypes to fasting and re-feeding, and their relationships with individual growth rates in yearling masu salmon (Oncorhynchus masou). Comp Biochem Physiol A 165:191–198CrossRefGoogle Scholar
  34. Kelley KM, Price TD, Galima MM, Sak K, Reyes JA, Zepeda O, Hagstrom R, Truong TA, Lowe CG (2006) Insulin-like growth factor-binding proteins (IGFBPs) in fish: beacons for (disrupted) growth endocrine physiology. In: Reinecke M, Zaccone G, Kapoor BG (Eds) Fish endocrinology. Science Publishers, Enfield, New Hampshire, pp 167–195Google Scholar
  35. Klauwer D, Blum WF, Hanitsch S, Rascher W, Lee PDK, Kiess W (1997) IGF-I, IGF-II, free IGF-I and IGFBP-1, IGFBP-2 and IGFBP-3 levels in venous cord blood: relationship to birthweight, length and gestational age in healthy newborns. Acta Paediatr 86:826–833CrossRefGoogle Scholar
  36. Knacke H, Pietzner M, Do KT, Römisch-Margl W, Kastenmüller G, Völker U, Völzke H, Krumsiek J, Artati A, Wallaschofski H, Nauck M, Suhre K, Adamski J, Friedrich N (2016) Metabolic fingerprints of circulating IGF-1 and the IGF-1/IGFBP-3 ratio: a multifluid metabolomics study. J Clin Endocrinol Metab 101:4730–4742CrossRefGoogle Scholar
  37. Kostyo JL (1999) The endocrine system. In: Goodman HM (ed) Hormonal control of growth. Oxford University Press, New York, pp 849–906Google Scholar
  38. McKinnell S, Ser EC, Groot K, Ama MK, Trudel M (2014) Oceanic and atmospheric extremes motivate a new hypothesis for variable marine survival of Fraser River sockeye salmon. Fish Oceanogr 23(4):322–341CrossRefGoogle Scholar
  39. MacLean SA, Caldarone EM, St Onge-burns JM (2008) Estimating recent growth rates of Atlantic salmon smolts using RNA–DNA ratios from nonlethally sampled tissues. Trans Am Fish Soc 137:1279–1284Google Scholar
  40. Pérez-Sánchez J, Le Bail PY (1999) Growth hormone axis as marker of nutritional status and growth performance in fish. Aquaculture 177:117–128CrossRefGoogle Scholar
  41. Picha ME, Turano MJ, Beckman BR, Borski RJ (2008a) Endocrine biomarkers of growth and applications to aquaculture: a minireview of growth hormone, insulin-like growth factor (IGF)-I , and IGF-binding proteins as potential growth indicators in fish. N Am J Aquac 70:196–211CrossRefGoogle Scholar
  42. Picha M, Turano M, Tipsmark C, Borski J (2008b) Regulation of endocrine and paracrine sources of Igfs and Gh receptor during compensatory growth in hybrid striped bass (Morone chrysops × Morone saxatilis). J Endocrinol 199:81–94CrossRefGoogle Scholar
  43. Pierce AL, Shimizu M, Beckman BR, Baker DM, Dickhoff WW (2005) Time course of the GH/IGF axis response to fasting and increased ration in Chinook salmon (Oncorhynchus tshawyscha). Gen Comp Endocrinol 140:192–202CrossRefGoogle Scholar
  44. Rajaram S, Baylink DJ, Mohan S (1997) Insulin-like growth factor-binding proteins in serum and other biological fluids: regulation and functions. Endocr Rev 18:801–831Google Scholar
  45. Reinecke M (2010) Insulin-like growth factor and fish reproduction. Biol Reprod 82:656–661CrossRefGoogle Scholar
  46. Richmond JP, Zinn SA (2009) Validation of heterologous radioimmunoassays (RIA) for growth hormone (GH) and insulin-like growth factor (IGF)-I in phocid, otariid, and cetacean species. Aquat Mamm 35:19–31CrossRefGoogle Scholar
  47. Sandhu MS, Gibson JM, Heald AH, Dunger DB, Wareham NJ (2004) Association between insulin-like growth factor-I: insulin-like growth factor-binding protein-1 ratio and metabolic and anthropometric factors in men and women. Cancer Epidemiol Biomark Prev 13:166–170CrossRefGoogle Scholar
  48. Shepherd BS, Aluru N, Vijayan MM (2011) Acute handling disturbance modulates plasma insulin-like growth factor binding proteins in rainbow trout (Oncorhynchus mykiss). Domest Anim Endocrinol 40:129–138CrossRefGoogle Scholar
  49. Shimizu M, Dickhoff WW (2017) Circulating insulin-like growth factor binding proteins in fish: their identities and physiological regulation. Gen Comp Endocrinol 252:150–161CrossRefGoogle Scholar
  50. Shimizu M, Hara A, Dickhoff WW (2003) Development of an RIA for salmon 41 kDa IGF-binding protein. J Endocrinol 178:275–283CrossRefGoogle Scholar
  51. Shimizu M, Beckman BR, Hara A, Dickhoff WW (2006) Measurement of circulating salmon IGF binding protein-1: assay development, response to feeding ration and temperature, and relation to growth parameters. J Endocrinol 188:101–110CrossRefGoogle Scholar
  52. Shimizu M, Cooper KA, Dickhoff WW, Beckman BR (2009) Postprandial changes in plasma growth hormone, insulin, insulin-like growth factor (IGF)-I, and IGF-binding proteins in coho salmon fasted for varying periods. Am J Physiol Regul Integr Comp Physiol 297:R352–R361CrossRefGoogle Scholar
  53. Shimizu M, Kishimoto K, Yamaguchi T, Nakano Y, Hara A, Dickhoff WW (2011a) Circulating salmon 28- and 22-kDa insulin-like growth factor binding proteins (IGFBPs) are co-orthologs of IGFBP-1. Gen Comp Endocrinol 174:97–106CrossRefGoogle Scholar
  54. Shimizu M, Suzuki S, Horikoshi M, Hara A, Dickhoff WW (2011b) Circulating salmon 41-kDa insulin-like growth factor binding protein (IGFBP) is not IGFBP-3 but an IGFBP-2 subtype. Gen Comp Endocrinol 171:326–331CrossRefGoogle Scholar
  55. Sparkman AM, Byars D, Ford NB, Bronkowski AM (2010) The role of insulin-like growth factor-1 (IGF-1) in growth and reproduction in female brown house snakes (Lamprophis fuliginosus). Gen Comp Endocrinol 168:408–414CrossRefGoogle Scholar
  56. Terova G, Rimoldi S, Chini V, Gornati R, Bernardini G, Saroglia M (2007) Cloning and expression analysis of insulin-like growth factor I and II in liver and muscle of sea bass (Dicentrarchus labrax, L.) during long-term fasting and refeeding. J Fish Biol 70:219–233CrossRefGoogle Scholar
  57. Tomaro LM, Teel DJ, Peterson WP, Miller JA (2012) When is bigger better? Early marine residence of middle and upper Columbia River spring Chinook salmon. Mar Ecol Prog Ser 452:237–252CrossRefGoogle Scholar
  58. Tucker S, Trudel M, Welch DW, Candy JR, Morris JFT, Thiess ME, Thiess ME, Wallace C, Teel DJ, Crawford W, Farley EV Jr, Beacham TD (2009) Seasonal stock-specific migrations of juvenile sockeye salmon along the west coast of North America: implications for growth. Trans Am Fish Soc 138:1458–1480CrossRefGoogle Scholar
  59. Wechter ME, Beckman BR, Andrews AG III, Beaudreau AH, McPhee MV (2017) Growth and condition of juvenile chum and pink salmon in the northeastern Bering Sea. Deep Sea Research II 135:145–155CrossRefGoogle Scholar
  60. Wells BK, Friedland KD, Clarke LM (2003) Increment patterns in otoliths and scales from mature Atlantic salmon Salmo salar. Mar Ecol Prog Ser 262:293–298CrossRefGoogle Scholar
  61. Wheatcroft SB, Kearney MT (2009) IGF-dependent and IGF-independent actions of IGF-binding protein-1 and -2: implications for metabolic homeostasis. Trends Endocrinol Meab 20:153–162CrossRefGoogle Scholar
  62. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Faculty of Fisheries SciencesHokkaido UniversityHakodateJapan
  2. 2.Environmental and Fisheries Sciences DivisionNorthwest Fisheries Science Center, National Marine Fisheries ServiceSeattleUSA
  3. 3.Fisheries and Oceans Canada, St Andrews Biological StationSt AndrewsCanada

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