Skip to main content

Advertisement

SpringerLink
Log in

Variation in plasma levels of insulin-like growth factor-I (IGF-I) in lingcod: relationships among season, size, and gonadal steroids

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The physiological response of a fish to its environment is mediated through the endocrine axis controlling growth. Therefore, growth-regulating hormone levels can serve as ecologically relevant indicators of fish growth rate. We quantified variation in plasma insulin-like growth factor-I (IGF-I) to evaluate its potential as an indicator of growth in lingcod, an economically and ecologically important bottomfish species in the northeast Pacific. An information-theoretic model selection approach was used to test the hypothesis that variation in lingcod IGF-I is related to season, body size, and gonadal steroid concentration. Season and a length × season interaction were the most important predictors of plasma IGF-I among the variables we evaluated, suggesting that season and body size should be explicitly accounted for when interpreting endocrine patterns in wild fish populations. This is among the few studies that have measured and interpreted patterns of IGF-I in wild fish and the first to describe seasonal endocrine profiles in lingcod.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Andrews KS, Beckman BR, Beaudreau AH, Larsen DA, Williams GD, Levin PS (in review) Developing a physiological tool to measure spatial variation in the growth of fishes. J Mar Coast Fish (submitted)

  • Beamish RJ, Chilton D (1977) Age determination of lingcod (Ophiodon elongatus) using dorsal fin rays and scales. J Fish Res Board Can 34:1305–1313

    Google Scholar 

  • Beaudreau AH, Essington TE (2007) Spatial, temporal, and ontogenetic patterns of predation on rockfishes by lingcod. Trans Am Fish Soc 136:1438–1452

    Article  Google Scholar 

  • Beaudreau AH, Essington TE (2009) Development of a new field-based approach for estimating consumption rates of fishes and comparison with a bioenergetics model for lingcod (Ophiodon elongatus). Can J Fish Aquat Sci 66:565–578

    Article  Google Scholar 

  • Beckman BR (2010) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol. doi:10.1016/j.ygcen.2010.08.009

  • 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 109:325–335

    Article  CAS  Google Scholar 

  • Beckman BR, Larsen DA, Sharpe C, Lee-Pawlak B, Schreck CB, Dickhoff WW (2000) Physiological status of naturally reared juvenile spring Chinook salmon in the Yakima River: seasonal dynamics and changes associated with smolting. Trans Am Fish Soc 129:727–753

    Article  Google Scholar 

  • 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 133:1057–1067

    Article  CAS  Google Scholar 

  • 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 135:334–344

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science + Business Media Inc, New York, NY

    Google Scholar 

  • Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032

    Article  Google Scholar 

  • Campbell B, Dickey JT, Swanson P (2003) Endocrine changes during onset of puberty in male spring Chinook salmon, Oncorhynchus tshawytscha. Biol Repro 69:2109–2117

    Article  CAS  Google Scholar 

  • Cass AJ, Beamish RJ, McFarlane GA (1990) Lingcod (Ophiodon elongatus). Canada Department of Fisheries and Oceans, Ottawa

    Google Scholar 

  • Chatwin BM (1954) Growth of young lingcod. Fisheries Research Board of Canada Progress Reports of the Pacific Coastal Station 99: 14–17

  • Coates J, Gunderson DR, LaFrance L, Miller BS, Goetz B, Palsson WA (2007) Changes in growth and recruitment of Puget Sound rockfish (Sebastes emphaeus) in northern Puget Sound. University of Alaska College Sea Grant Program Report, AK-SG-07-01

  • Cuisset B, Pradelles P, Kime DE, Kuhn ER, Babin P, Le Menn F (1994) Enzyme immunoassay for 11-ketotestosterone using acetylcholineesterase as label: application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon. Comp Biochem Physiol 108:229–241

    Article  Google Scholar 

  • Dahle R, Taranger GL, Karlsen O, Kjesbu OS, Norberg B (2003) Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). Comp Biochem Physiol A 136:641–653

    Article  Google Scholar 

  • Daughaday WH, Mariz IK, Blethen SL (1980) Inhibition of access of bound somatomedin to membrane receptor and immunobinding sites: a comparison of radioreceptor and radioimmunoassay of somatomedin in native and acid-ethanol-extracted serum. J Clin Endocrinol Metab 51:781–788

    Article  CAS  Google Scholar 

  • Davis LK, Pierce AL, Hiramatsu N, Sullivan CV, Hirano T, Grau EG (2008) Gender-specific expression of multiple estrogen receptors, growth hormone receptors, insulin-like growth factors and vitellogenins, and effects of 17 beta-estradiol in the male tilapia (Oreochromis mossambicus) Gen Comp Endocrinol 156:544–551

    Google Scholar 

  • Goetz FW, Rise ML, Rise M, Goetz GW, Binkowski F, Shepherd BS (2009) Stimulation of growth and changes in the hepatic transcriptome by 17 beta-estradiol in the yellow perch (Perca flavescens). Phys Genom 38:261–280

    Article  CAS  Google Scholar 

  • Gregg JL (2003) Diel otolith increment validation and other early life history observations of lingcod (Ophiodon elongatus). Master of Science thesis. School of aquatic and fishery sciences, Seattle

  • Guy CS, Blankenship HL, Nielsen LA (1996) Tagging and marking. In: Murphy BR, Willis DW (eds) Fisheries techniques. American Fisheries Society, Bethesda, MD, pp 353–383

    Google Scholar 

  • Haukenes AH, Plante S, Buck CL (2008) Pattern of sex steroid concentrations in relation to the annual reproductive cycle of wild and captive black rockfish. N Am J Aquacult 70:212–218

    Article  Google Scholar 

  • Hinch SG, Collins NC (1991) Importance of diurnal and nocturnal nest defense in the energy budget of male smallmouth bass: insights from direct video observations. Trans Am Fish Soc 120:657–663

    Article  Google Scholar 

  • Hobbs NT, Hilborn R (2006) Alternatives to statistical hypothesis testing in ecology: a guide to self teaching. Ecol Appl 16:5–19

    Article  Google Scholar 

  • Jagielo TH, Wallace FR (2005) Assessment of lingcod (Ophiodon elongatus) for the Pacific Fishery Management Council. Washington Department of Fish and Wildlife, Montesano, Washington

    Google Scholar 

  • Jagielo TH, LeClair LL, Vorderstrasse BA (1996) Genetic variation and population structure of lingcod. Trans Am Fish Soc 125:372–386

    Article  CAS  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  Google Scholar 

  • Kajimura S, Uchida K, Yada T, Riley LG, Byatt JC, Collier RJ, Aida K, Hirano T, Grau EG (2001) Stimulation of insulin-like growth factor-I production by recombinant bovine growth hormone in Mozambique tilapia, Oreochromis mossambicus. Fish Physiol Biochem 25:221–230

    Article  CAS  Google Scholar 

  • Knapp R, Wingfield JC, Bass AH (1999) Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Horm Behav 35:81–89

    Article  CAS  Google Scholar 

  • LaRiviere MG, Jessup DD, Mathews SB (1981) Lingcod, Ophiodon elongatus, spawning and nesting in San Juan channel, Washington. Calif Fish Game 67:231–239

    Google Scholar 

  • Larsen DA, Beckman BR, Dickhoff WW (2001) The effect of low temperature and fasting during the winter on metabolic stores and endocrine physiology (insulin, insulin-like growth factor-I, and thyroxine) of coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol 123:308–323

    Article  CAS  Google Scholar 

  • Larsen DA, Shimizu M, Cooper KA, Swanson P, Dickhoff WW (2004) Androgen effects on plasma GH, IGF-I, and 41-kDa IGFBP in coho salmon (Oncorhynchus kisutch). Gen Comp Endocrinol 139:29–37

    Article  CAS  Google Scholar 

  • Lynn SG, Powell KA, Westneat DF, Shepherd BS (2009) Seasonal and sex-specific mRNA levels of key endocrine genes in adult yellow perch (Perca flavescens) from Lake Erie. J Mar Biotechnol 11:210–222

    Article  CAS  Google Scholar 

  • Magee SE, Neff BD, Knapp R (2006) Plasma levels of androgens and cortisol in relation to breeding behavior in parental male bluegill sunfish, Lepomis macrochirus. Horm Behav 49:598–609

    Article  CAS  Google Scholar 

  • Marko PB, Rogers-Bennett L, Dennis AB (2007) MtDNA population structure and gene flow in lingcod (Ophiodon elongatus): limited connectivity despite long-lived pelagic larvae. Mar Biol 150:1301–1311

    Article  CAS  Google Scholar 

  • McFarlane GA, King JR (2001) The validity of the fin-ray method of age determination for lingcod (Ophiodon elongatus). Fish Bull 99:459–464

    Google Scholar 

  • Miller DJ, Geibel JJ (1973) Summary of blue rockfish and lingcod life histories: a reef ecology study; and giant kelp, Macrocystis pyrifera, experiments in Monterey Bay, California. Calif Dept Fish Game Fish Bull 158. 135 pp

  • Mingarro M, Vega-Rubin de Celis S, Astola A, Pendon C, Valdivia MM, Perez-Sanchez J (2002) Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and somatolactin paradigm. Gen Comp Endocrinol 128:102–111

    Article  CAS  Google Scholar 

  • Nicieza AG, Metcalfe NB (1997) Growth compensation in juvenile Atlantic salmon: responses to depressed temperature and food availability. Ecology 78:2385–2400

    Article  Google Scholar 

  • Ohlsson C, Mohan S, Sjogren K, Tivesten A, Isgaard J, Isaksson O, Jansson JO, Svensson J (2009) The role of liver-derived insulin-like growth factor-I. Endo Rev 30:494–535

    Article  CAS  Google Scholar 

  • Onuma TA, Makino K, Katsumata H, Beckman BR, Ban M, Ando H, Fukuwaka M, Azumaya T, Swanson P, Urano A (2010) Changes in the plasma levels of insulin-like growth factor-I from the onset of spawning migration through upstream migration in chum salmon. Gen Comp Endocrinol 165:237–243

    Article  CAS  Google Scholar 

  • Pall MK, Mayer I, Borg B (2002) Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus I.—Changes in 11-ketotestosterone levels during the nesting cycle. Horm Behav 41:377–383

    Article  CAS  Google Scholar 

  • Pérez-Sánchez J, Marti-Palanca H, LeBail PY (1994) Seasonal-changes in circulating growth- hormone (GH), hepatic GH-binding and plasma insulin-like growth-factor-I immunoreactivity in a marine fish, gilthead sea bream, Sparus aurata. Fish Physiol Biochem 13:199–208

    Article  Google Scholar 

  • Pérez-Sánchez J, Marti-Palanca H, Kaushik SJ (1995) Ration size and protein-intake affect circulating growth-hormone concentration, hepatic growth-hormone binding and plasma insulin-like growth-factor-I immunoreactivity in a marine teleost, the gilthead sea bream (Sparus aurata). J Nutrition 125:546–552

    Google Scholar 

  • Picha ME, Turano MJ, Beckman BR, Borski RJ (2008) 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 Aquacult 70:196–211

    Article  Google Scholar 

  • Pierce AL, Beckman BR, Shearer KD, Larsen DA, Dickhoff WW (2001) Effects of ration on somatotropic hormones and growth in coho salmon. Comp Biochem Phys B 128:255–264

    Article  CAS  Google Scholar 

  • Ratz H-J, Lloret J (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity, and management implications. Fish Res 60:369–380

    Article  Google Scholar 

  • Riley LG, Hirano T, Grau EG (2002) Disparate effects of gonadal steroid hormones on plasma and liver mRNA levels of insulin-like growth factor-I and vitellogenin in the tilapia, Oreochromis mossambicus. Fish Physiol Biochem 26:223–230

    Article  CAS  Google Scholar 

  • Roberts SB, Jackson LF, King VW, Taylor RG, Grier HJ, Sullivan CV (1999) Annual reproductive cycle of the common snook: endocrine correlates of maturation. Trans Am Fish Soc 128:436–445

    Article  CAS  Google Scholar 

  • Rodgers EW, Earley RL, Grober MS (2006) Elevated 11-ketotestosterone during parental behavior in the bluebanded goby (Lythrypnus dalli). Horm Behav 49:610–614

    Article  CAS  Google Scholar 

  • Shimizu M, Swanson P, Fukada H, Hara A, Dickhoff WW (2000) Comparison of extraction methods and assay validation for salmon insulin-like growth factor-I using commercially available components. Gen Comp Endocrinol 119:26–36

    Article  CAS  Google Scholar 

  • 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—Reg I 297: R352–R361

  • Silberberg KR, Laidig TE, Adams PB (2001) Analysis of maturity in lingcod (Ophiodon elongatus). Calif Fish Game 87(4):139–152

    Google Scholar 

  • Simenstad C, Miller B, Nyblade C, Thornburgh K, Bledsoe L (1979) Food web relationships of northern Puget Sound and the Strait of Juan de Fuca; a synthesis of available knowledge, NOAA-EPA-600/7-79-259

  • Sogard SM (1997) Size-selective mortality in the juvenile stage of teleost fishes: a review. Bull Mar Sci 60:1129–1157

    Google Scholar 

  • Sower SA, Schreck CB (1982) Steroid and thyroid hormones during sexual maturation of coho salmon. Gen Comp Endocrinol 47:43–57

    Google Scholar 

  • Taylor JF, Porter MJR, Bromage NR, Migaud H (2008) Relationships between environmental changes, maturity, growth rate and plasma insulin-like growth factor-I (IGF-I) in female rainbow trout. Gen Comp Endocrinol 155:257–270

    Article  CAS  Google Scholar 

  • Uchida K, Kajimura S, Riley LG, Hirano T, Aida K, Grau EG (2003) Effects of fasting on growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Phys A 134:429–439

    Article  CAS  Google Scholar 

  • Weatherley AH (1990) Approaches to understanding fish growth. Trans Am Fish Soc 119:662–672

    Article  Google Scholar 

  • Weisberg S (1985) Applied linear regression. John Wiley, New York

    Google Scholar 

  • Wespestad VG, Bargmann GG, Hay DE (1994) Opportunities for the enhancement of the lingcod, Ophiodon elongatus Girard, in Puget Sound and Georgia Straits. Aquacult Fish Manage 25:189–197

    Google Scholar 

  • Whittingham MJ, Stephens PA, Bradbury RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behaviour? J Anim Ecol 75:1182–1189

    Article  Google Scholar 

  • Wilby GV (1937) The lingcod, Ophiodon elongatus Girard. Fish Res Board Can Bull 54. 24 pp

  • Withler RE, King JR, Marliave JB, Beaith B, Li S, Supernault KJ, Miller KM (2004) Polygamous mating and high levels of genetic variation in lingcod, Ophiodon elongatus, of the Strait of Georgia, British Columbia. Environ Biol Fishes 69:345–357

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, vol 4. Prentice Hall, Upper Saddle River, New Jersey

    Google Scholar 

Download references

Acknowledgments

This research was funded in part by the Internal Grant Program at the Northwest Fisheries Science Center. The University of Washington School of Aquatic and Fishery Sciences (UW-SAFS) and Friday Harbor Laboratories provided funding and facilities for field work. A.H.B. was supported by the National Science Foundation, ARCS Foundation, and UW-SAFS. We thank the many volunteers involved in the collection of lingcod, especially A. Dufault and C. Sergeant. We thank K. Cooper and J. Dickey (UW-SAFS) for conducting the hormone assays. Thanks to three anonymous reviewers for providing valuable comments on a draft of the manuscript. The research complies with all applicable United States laws, and the authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

  1. School of Aquatic and Fishery Sciences, University of Washington, Box 355020, Seattle, WA, 98195, USA

    Anne H. Beaudreau & Graham Young

  2. NOAA Fisheries, Northwest Fisheries Science Center, 2725 Montlake Blvd E., Seattle, WA, 98112, USA

    Kelly S. Andrews, Donald A. Larsen & Brian R. Beckman

  3. Center for Reproductive Biology, Washington State University, Pullman, WA, 99164, USA

    Graham Young

Authors
  1. Anne H. Beaudreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelly S. Andrews
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donald A. Larsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Graham Young
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Brian R. Beckman
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne H. Beaudreau.

Additional information

Communicated by C. Harrod.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beaudreau, A.H., Andrews, K.S., Larsen, D.A. et al. Variation in plasma levels of insulin-like growth factor-I (IGF-I) in lingcod: relationships among season, size, and gonadal steroids. Mar Biol 158, 439–450 (2011). https://doi.org/10.1007/s00227-010-1571-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1571-9

Keywords

Search

Navigation