Skip to main content

Advertisement

SpringerLink
Log in

Maturation shifts in a temperate marine fish population cannot be explained by simulated changes in temperature-dependent growth and maturity

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

Abstract

To disentangle genetic and environmental influences on phenotypic traits that influence maturation of fish, it would be useful to predict the expected change due to environment alone to compare with observations. This requires a realistically scaled, species-specific life history model of environmentally determined variation in individual growth and maturation. In this study, inter-annual variability in the proportion of mature haddock in the west North Sea was predicted using a stochastic, individual-based simulation model incorporating a temperature-dependent maturation threshold. This species and region are particularly relevant to the debate about the relative importance of genetic and climate change because North Sea haddock have experienced both high fishing mortality and substantial warming in recent decades. Using observed temperatures in combination with temperature-dependent models for growth and maturation, the simulation model predicted year-to-year variation in length and maturity at age expected for cohorts produced from 1979 to 2006. The simulated proportions mature at age 2 were then compared to the observed proportions in an annual bottom trawl survey. Although the model explained much of the high-frequency variation in maturation, the simulated time trend under-represented the rate of increase in the observed trend in proportions mature. This inability of the temperature-dependent life history model to predict the magnitude of change appears consistent with a long-term decline in the maturation threshold. This result provides indirect support for a genetic change in a key life history trait.

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

Similar content being viewed by others

References

  • Andersen KH, Brander K (2009) Expected rate of fisheries-induced evolution is slow. Proc Nat Acad Sci 106:11657–11660

    Article  CAS  Google Scholar 

  • Aubin-Horth N, Landry CR, Letcher BH, Hofmann HA (2005) Alternative life histories shape brain gene expression profiles in males of the same population. Proc R Soc B 272:1655–1662

    Article  CAS  Google Scholar 

  • Baudron AR, Needle CL, Marshall CT (2011) Implications of a warming North Sea for the growth of haddock Melanogrammus aeglefinus. J Fish Biol 78:1874–1889. doi:10.1111/j.1095-8649.2011.02940.x

    Article  CAS  Google Scholar 

  • Belkin IM (2009) Rapid warming of large marine ecosystems. Prog Oceanogr 81:207–213

    Article  Google Scholar 

  • Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98

    Article  CAS  Google Scholar 

  • Campton DE, Gall GAE (1988) Responses to selection for body size and age at sexual maturity in the mosquito fish Gambusia affinis. Aquaculture 68:221–241. doi:10.1016/0044-8486(88)90355-9

    Article  Google Scholar 

  • Darimont CT, Carlson SM, Kinnison MT, Paquet PC, Reimchen TE, Wilmers CC (2009) Human predators outpace other agents of trait change in the wild. Proc Natl Acad Sci USA 106:952–954

    Article  CAS  Google Scholar 

  • Davie A, Mazorra de Quero C, Bromage N, Treasurer J, Migaud H (2007) Inhibition of sexual maturation in tank reared haddock (Melanogrammus aeglefinus) through the use of constant light photoperiods. Aquaculture 270:379–389

    Article  Google Scholar 

  • Day T, Rowe L (2002) Development threshold and the evolution of reaction norms for age and size at life-history transitions. Am Nat 159:338–350

    Article  Google Scholar 

  • Devine Jennifer A, Wright Peter J, Pardoe Heidi E, Heino M (2012) Comparing rates of contemporary evolution in life-history traits for exploited fish stocks. Can J Fish Aquat Sci 69:1105–1120. doi:10.1139/f2012-047

    Article  Google Scholar 

  • Dhillon RS, Fox MG (2004) Growth-independent effects of temperature on age and size at maturity in Japanese Medaka (Oryzias latipes). Copeia 2004:37–45

    Article  Google Scholar 

  • Diaz Pauli B, Heino M (2013) The importance of social dimension and maturation stage for the probabilistic maturation reaction norm in Poecilia reticulata J Evol Biol 26:2184–2196. doi:10.1111/jeb.12215

  • Dieckmann U, Heino M (2007) Probabilistic maturation reaction norms: their history, strengths, and limitations. Mar Ecol Prog Ser 335:253–269

    Article  Google Scholar 

  • Elliot AJ, Clarke T, Li Z (1991) Monthly distributions of surface and bottom temperatures in the northwest European shelf seas. Cont Shelf Res 11:453–466

    Article  Google Scholar 

  • Ernande B, Dieckmann U, Heino M (2004) Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation. Proc R Soc B 271:415–423

    Article  Google Scholar 

  • Ferro RST, Özbilginb H, Breen M (2008) The potential for optimizing yield from a haddock trawl fishery using seasonal changes in selectivity, population structure and fish condition. Fish Res 94:151–159

    Article  Google Scholar 

  • Greenstreet SPR, Spence FB, Shanks AM, McMillan JA (1999) Fishing effects in northeast Atlantic shelf seas: patterns in fishing effort, diversity and community structure. II. Trends in fishing effort in the North Sea by UK registered vessels landing in Scotland. Fish Res 40:107–124

    Article  Google Scholar 

  • Greenstreet SPR, Holland GJ, Fraser TWK, Allen VJ (2009) Modelling demersal fishing effort based on landings and days absence from port, to generate indicators of “activity”. ICES J Mar Sci 66:886–901

    Article  Google Scholar 

  • Gutierrez A, Lubieniecki K, Fukui S, Withler R, Swift B, Davidson W (2014) Detection of quantitative trait loci (QTL) related to grilsing and late sexual maturation in Atlantic Salmon (Salmo salar) Mar. Biotechnol 16:103–110. doi:10.1007/s10126-013-9530-3

    CAS  Google Scholar 

  • Heino M, Dieckmann U, Godø OR (2002) Measuring probabilistic reaction norms for age and size at maturation. Evolution 56:669–678

    Article  Google Scholar 

  • Hermelink B, Wuertz S, Trubiroha A, Rennert B, Kloas W, Schulz C (2011) Influence of temperature on puberty and maturation of pikeperch, Sander lucioperca. Gen Comp Endocrinol 172:282–292. doi:10.1016/j.ygcen.2011.03.013

  • Hjollo SS, Skogen MD, Svendsen E (2009) Exploring currents and heat within the North Sea using a numerical model. J Marine Syst 78:180–192

    Article  Google Scholar 

  • Holliday NP, Hughes SL, Beszczynska-Möller A (Eds) (2009) ICES Report on Ocean Climate 2008. ICES Cooperative Research Report No. 298

  • ICES (2009) Report of the Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak—Combined Spring and Autumn (WGNSSK), 6–12 May 2009, ICES Headquarters, Copenhagen

  • ICES (2011) Manual for the International Bottom Trawl Surveys Revision VII ICES Headquarters, Copenhagen

  • Jones R, Hislop JRG (1972) Investigations into the growth of haddock, Melanogrammus aeglefinus (L) and whiting, Merlangus merlangius (L) in aquaria. J Cons Int Explor Mer 34:174–189

    Article  Google Scholar 

  • Jorgensen C, Enberg K, Dunlop ES, Arlinghaus R, Boukal DS, Brander K, Ernande B et al (2007) Managing evolving fish stocks. Science 318:1247–1248

    Article  CAS  Google Scholar 

  • Korsgaard B, Mommsen TP, Saunders RL (1986) The effect of temperature on the vitellogenic response in Atlantic salmon post-smolts (Salmo salar). Gen Comp Endocr 62:191–201. doi:10.1016/0016-6480(86)90109-7

    Article  Google Scholar 

  • Kuparinen A, Cano J, Loehr J, Herczeg G, Gonda A, Merilä J (2011) Fish age at maturation is influenced by temperature independently of growth. Oecologia 167:435–443

  • Law R (2000) Fishing, selection, and phenotypic evolution. ICES J Mar Sci 57:659–668

    Article  Google Scholar 

  • Lester NP, Shuter BJ, Abrams PA (2004) Interpreting the von Bertalanffy model of somatic growth in fishes: the cost of reproduction. Proc R Soc B 271:1625–1631

    Article  CAS  Google Scholar 

  • Mangel M, Satterthwaite WH (2008) Combining proximate and ultimate approaches to understand life history variation in salmonids with applications to fisheries, conservation, and aquaculture. Bull Mar Sci 83:107–130

    Google Scholar 

  • McCarthy MA, Masters P (2005) Profiting from prior information in Bayesian analyses of ecological data. J Appl Ecol 42:1012–1019

    Article  Google Scholar 

  • Mollet FM, Kraak SBM, Rijnsdorp AD (2007) Fisheries-induced evolutionary changes in maturation reaction norms in North Sea sole Solea solea. Mar Ecol Prog Ser 351:189–199

    Article  Google Scholar 

  • Mollet FM, Engelhard GH, Vainikka A, Laugen AT, Rijnsdorp AD, Ernande B (2013) Spatial variation in growth, maturation schedules and reproductive investment of female sole Solea solea in the Northeast Atlantic. J Sea Res 84:109–121

    Article  Google Scholar 

  • Morita K, Tsuboi J, Nagasawa T (2009) Plasticity in probabilistic reaction norms for maturation in a salmonid fish. Biol Lett 5:628–631

    Article  Google Scholar 

  • Nævdal G (1983) Genetic factors in connection with age at maturation. Aquaculture 33:97–106. doi:10.1016/0044-8486(83)90390-3

    Article  Google Scholar 

  • Nilsson J (1992) Genetic parameters of growth and sexual maturity in Arctic char (Salvelinus alpinus). Aquaculture 106:9–19. doi:10.1016/0044-8486(92)90245-G

    Article  Google Scholar 

  • Olin T, Von der Decken A (1989) Vitellogenin synthesis in Atlantic salmon (Salmo salar) at different acclimation temperatures. Aquaculture 79:397–402. doi:10.1016/0044-8486(89)90482-1

    Article  CAS  Google Scholar 

  • Pankhurst NW, Porter MJR (2003) Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiol Biochem 28:385–389. doi:10.1023/B:FISH.0000030602.51939.50

    Article  CAS  Google Scholar 

  • Pérez-Casanova J, Lall S, Gamperl A (2009) Effect of feed composition and temperature on food consumption, growth and gastric evacuation of juvenile Atlantic cod (Gadus morhua L.) and haddock (Melanogrammus aeglefinus L.). Aquaculture 294:228–235

    Article  Google Scholar 

  • 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 54:444–451

    Article  CAS  Google Scholar 

  • Taranger GL, Carrillo M, Schulz RW, Fontaine P, Zanuy S, Felip A, Weltzien FA et al (2010) Control of puberty in farmed fish. Gen Comp Endocr 165:483–515

    Article  CAS  Google Scholar 

  • Thorpe J (1986) Age at first maturity in Atlantic salmon, Salmo salar L.: freshwater period influences and conflicts with smolting. Can J Fish Aquat Sci 89:7–14

    Google Scholar 

  • Thorpe JE, Morgan RIG, Ottaway EM, Miles MS (1980) Time of divergence of growth groups between potential 1 + and 2 + smolts among sibling Atlantic salmon. J Fish Biol 17:13–21. doi:10.1111/j.1095-8649.1980.tb02738.x

    Article  Google Scholar 

  • 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 12:581–599

    Article  Google Scholar 

  • Tobin D, Wright PJ (2011) Temperature effects on female maturation in a temperate marine fish. J Exp Mar Biol Ecol 403:9–13. doi:10.1016/j.jembe.2011.03.018

    Article  Google Scholar 

  • Tobin D, Wright PJ, O’Sullivan M (2010) Timing of the maturation transition in haddock Melanogrammus aeglefinus. J Fish Biol 77:1252–1267. doi:10.1111/j.1095-8649.2010.02739.x

    Article  CAS  Google Scholar 

  • Trippel EA (1995) Age at maturity as a stress indicator in fisheries BioScience 45:759–771

    Google Scholar 

  • Uusi-Heikkilä S, Kuparinen A, Wolter C, Meinelt T, O’Toole AC, Arlinghaus R (2011) Experimental assessment of the probabilistic maturation reaction norm: condition matters. Proc R Soc B 278:709–717

    Article  Google Scholar 

  • Vainikka A, Kallio-Nyberg I, Heino M, Koljonen ML (2010) Divergent trends in life-history traits between Atlantic salmon Salmo salar of wild and hatchery origin in the Baltic Sea. J Fish Biol 76:622–640

    Article  CAS  Google Scholar 

  • Van der Kraak G, Pankhurst NW (1997) Temperature effects on the reproductive performance of fish. Cambridge University Press, Cambridge

    Google Scholar 

  • Wright PJ (2007) Understanding the maturation process for field investigations of fisheries-induced evolution. Mar Ecol Prog Ser 335:279–283

    Article  Google Scholar 

  • Wright PJ (2013) Methodological challenges to examining the causes of variation in stock reproductive potential. Fish Res 138:14–22. doi:10.1016/j.fishres.2012.06.002

    Article  Google Scholar 

  • Wright PJ, Tobin D (2013) Maturation differences between sub-stocks of haddock, Melanogrammus aeglefinus. Mar Biol 160:231–239

    Article  Google Scholar 

  • Wright PJ, Gibb FM, Gibb IM, Millar CP (2011a) Reproductive investment in the North Sea haddock: temporal and spatial variation. Mar Ecol Prog Ser 432:149–160. doi:10.3354/meps09168

    Article  Google Scholar 

  • Wright PJ, Millar CP, Gibb FM (2011b) Intrastock differences in maturation schedules of Atlantic cod. Gadus morhua ICES J Mar Sci 68:1918–1927. doi:10.1093/icesjms/fsr111

    Article  Google Scholar 

  • Yoneda M, Wright PJ (2005) Effects of varying temperature and food availability on growth and reproduction in first-time spawning female Atlantic cod. J Fish Biol 67:1225–1241

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge advice from Justin Travis in the development of the model and funding from the Scottish Government Grant SU002. Myron Peck and two anonymous reviewers provided valuable comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

  1. Marine Scotland Science, Marine Laboratory, 375 Victoria Road, Aberdeen, AB11 9DB, Scotland, UK

    Peter J. Wright

  2. School of Biological Sciences, Zoology Building, Tillydrone Avenue, Aberdeen, AB24 2TZ, UK

    Stephen C. F. Palmer & C. Tara Marshall

Authors
  1. Peter J. Wright
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen C. F. Palmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Tara Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter J. Wright.

Additional information

Communicated by M. A. Peck.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wright, P.J., Palmer, S.C.F. & Marshall, C.T. Maturation shifts in a temperate marine fish population cannot be explained by simulated changes in temperature-dependent growth and maturity. Mar Biol 161, 2781–2790 (2014). https://doi.org/10.1007/s00227-014-2543-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2543-2

Keywords

Search

Navigation