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Fitness landscape of Atlantic cod shaped by harvest selection and natural selection

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Abstract

Harvesting may lead to evolutionary changes in life histories on a contemporary time scale, changes that could be maladaptive in natural contexts. However, our understanding of the strength and direction of harvest-induced selection versus natural selection is still limited, partly due to the difficulty of tracking the fate of individuals in the wild. Here, we present direct estimates of harvest mortality, natural mortality and site fidelity of coastal Atlantic cod (Gadus morhua) from the Norwegian Skagerrak coast. Furthermore, we present standardised selection differentials for fish body size. Estimates are obtained from acoustic telemetry, where we continuously monitored fish (n = 60) within a semi-sheltered area using a network of 25 listening stations. To obtain additional information about harvested cod, all fish (body size: 30–66 cm) were also tagged with traditional T-bar tags with a printed reward of 500 NOK (60 E). We estimate that 75% of the fish died within the study area during 1 year. Fishing mortality was markedly higher than natural mortality. Together, recreational fishers and commercial fishers caught at least 50% of the tagged fish during 1 year. Standardised selection differentials showed that fisheries targeted larger fish (i.e. favoured the survival of smaller fish), while natural selection favoured the survival of larger fish. Albeit on a small scale, we provide empirical evidence that harvesting can have a dominant influence on the fitness landscape experienced by a marine fish such as the Atlantic cod. We suggest that no-take marine reserves may help to counter evolutionary impacts of harvesting in the ocean.

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References

  • Andersen KH, Brander K (2009) Expected rate of fisheries-induced evolution is slow. Proc Natl Acad Sci USA 106:11657–11660. doi:10.1073/pnas.0901690106

    Article  PubMed  CAS  Google Scholar 

  • Baskett ML, Levin SA, Gaines SD, Dushoff J (2005) Marine reserve design and the evolution of size at maturation in harvested fish. Ecol Appl 15:882–901

    Article  Google Scholar 

  • Beamish RJ, McFarlane GA, Benson A (2006) Longevity overfishing. Prog Oceanogr 68:289–302

    Google Scholar 

  • Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. Fish Bull 53:182–196. doi:10.1016/j.pocean.2006.02.225

    Google Scholar 

  • Biro PA, Abrahams MV, Post JR, Parkinson EA (2004) Predators select against high growth rates and risk-taking behaviour in domestic trout populations. Proc R Soc B 271:2233–2237. doi:10.1098/rspb.2004.2861

    Article  PubMed  Google Scholar 

  • Brander KM (1995) The effect of temperature on growth of Atlantic cod (Gadus morhua). ICES J Mar Sci 52:1–10

    Article  Google Scholar 

  • Carlson SM, Edeline E, Vøllestad LA, Haugen TO, Winfield IJ, Fletcher JM, James JB, Stenseth NC (2007) Four decades of opposing natural and human-induced artificial selection acting on Windermere pike (Esox lucius). Ecol Lett 10:512–521. doi:10.1111/j.1461-0248.2007.01046.x

    Article  PubMed  Google Scholar 

  • Ciannelli L, Knutsen H, Olsen EM, Espeland SH, Asplin L, Jelmert A, Knutsen JA, Stenseth NC (2010) Maintenance of small-scale genetic structure in a marine population in relation to water circulation and egg characteristics. Ecology (in press)

  • Conover DO (2007) Nets versus nature. Nature 450:179–180

    Article  PubMed  CAS  Google Scholar 

  • Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297:94–96

    Article  PubMed  CAS  Google Scholar 

  • Cook RM, Sinclair A, Stefánsson G (1997) Potential collapse of North Sea cod stocks. Nature 385:521–522

    Article  CAS  Google Scholar 

  • Dahl K, Dannevig GM (1906) Studies on the effectiveness of releasing cod larvae for stock improvement in fjords in eastern Norway. Aarsberetn Norg Fisk 1:1–121 (in Norwegian)

    Google Scholar 

  • Dannevig A (1930) The death of fish in very cold winters. J Cons Int Explor Mer 5:194–196

    Google Scholar 

  • Dannevig A (1954) The littoral cod of the Norwegian Skagerrak coast. Rapp P-V Reun Cons Perm Int Explor Mer 136:7–14

    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. doi:10.1073/pnas.0809235106

    Article  PubMed  CAS  Google Scholar 

  • Development Core Team R (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • DiBattista JD, Feldheim KA, Gruber SH, Hendry AP (2007) When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks. J Evol Biol 20:201–212. doi:10.1111/j.1420-9101.2006.01210.x

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Edeline E, Carlson SM, Stige LC, Winfield IJ, Fletcher JM, James JB, Haugen TO, Vøllestad LA, Stenseth NC (2007) Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. Proc Natl Acad Sci USA 104:15799–15804. doi:10.1073/pnas.0705908104

    Article  PubMed  CAS  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. doi:10.1098/rspb.2003.2519

    Article  PubMed  Google Scholar 

  • Espeland SH, Gundersen AF, Olsen EM, Knutsen H, Gjøsæter J, Stenseth NC (2007) Home range and elevated egg densities within an inshore spawning ground of coastal cod. ICES J Mar Sci 64:920–928. doi:10.1093/icesjms/fsm028

    Article  Google Scholar 

  • Espeland SH, Olsen EM, Knutsen H, Gjøsæter J, Danielssen D, Stenseth NC (2008) New perspectives on fish movement: kernel and GAM smoothers applied to a century of tagging data on coastal Atlantic cod. Mar Ecol Prog Ser 372:231–241. doi:10.3354/meps07721

    Article  Google Scholar 

  • Espeland SH, Thoresen AG, Olsen EM, Stige LC, Knutsen H, Gjøsæter J, Stenseth NC (2010) Diel vertical migration patterns in young Skagerrak coastal cod. Mar Ecol Prog Ser 405:29–37. doi:10.3354/meps08524

    Article  Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman, Essex

    Google Scholar 

  • Gagliano M, McCormick MI, Meekan MG (2007) Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish. Proc R Soc B 274:1575–1582. doi:10.1098/rspb.2007.0242

    Article  PubMed  Google Scholar 

  • Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296:707–711

    Article  PubMed  CAS  Google Scholar 

  • Handford P, Bell G, Reimchen T (1977) A gillnet fishery considered as an experiment in artificial selection. J Fish Res Board Can 34:954–961

    Google Scholar 

  • Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman and Hall, London

    Google Scholar 

  • Heino M, Godø OR (2002) Fisheries-induced selection pressures in the context of sustainable fisheries. Bull Mar Sci 70:639–656

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Mol Ecol 17:20–29. doi:10.1111/j.1365-294X.2007.03428.x

    Article  PubMed  Google Scholar 

  • Heupel MR, Simpfendorfer CA (2002) Estimation of mortality in juvenile blacktip sharks, Carcharhinus limbatus, within a nursery area using telemetry data. Can J Fish Aquat Sci 59:624–632. doi:10.1139/F02-036

    Article  Google Scholar 

  • Hightower JE, Jackson JR, Pollock KH (2001) Use of telemetry methods to estimate natural mortality and fishing mortality of striped bass in Lake Gaston, North Carolina. Trans Am Fish Soc 130:557–567

    Article  Google Scholar 

  • Hilborn R (2010) Pretty good yield and exploited fishes. Mar Pol 34:193–196

    Article  Google Scholar 

  • Holmes TH, McCormick MI (2010) Size-selectivity of predatory reef fish on juvenile prey. Mar Ecol Prog Ser 399:273–283. doi:10.3354/meps98337

    Article  Google Scholar 

  • Hsieh C, Yamauchi A, Nakazawa T, Wang W-F (2010) Fishing effects on age and spatial structures undermine population stability of fishes. Aquat Sci 72:165–178. doi:10.1007/s00027-009-0122-2

    Article  Google Scholar 

  • Hutchings JA (1999) Influence of growth and survival costs of reproduction on Atlantic cod, Gadus morhua, population growth rate. Can J Fish Aquat Sci 56:1612–1623

    Article  Google Scholar 

  • Hutchings JA, Myers RA (1994) What can be learned from the collapse of a renewable resource? Atlantic cod, Gadus morhua, of Newfoundland and Labrador. Can J Fish Aquat Sci 51:2126–2146

    Article  Google Scholar 

  • Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571

    Article  Google Scholar 

  • Johnson DW, Hixon MA (2010) Ontogenetic and spatial variation in size-selective mortality of a marine fish. J Evol Biol 23:724–737. doi:10.1111/j.1420-9101.2010.01938.x

    Article  PubMed  CAS  Google Scholar 

  • Jorde PE, Knutsen H, Espeland SH, Stenseth NC (2007) Spatial scale of genetic structuring in coastal cod Gadus morhua and geographic extent of local populations. Mar Ecol Prog Ser 343:229–237

    Article  Google Scholar 

  • Julliard R, Stenseth NC, Gjøsæter J, Lekve K, Fromentin J-M, Danielssen DS (2001) Natural mortality and fishing mortality in a coastal cod population: a release-recapture experiment. Ecol Appl 11:540–558

    Google Scholar 

  • Kinnison MT, Hairston NG Jr (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct Ecol 21:444–454

    Article  Google Scholar 

  • Kjesbu OS (1989) The spawning activity of cod, Gadus morhua L. J Fish Biol 34:195–206

    Article  Google Scholar 

  • Knutsen H, Jorde PE, André C, Stenseth NC (2003) Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394

    Article  PubMed  CAS  Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Law R (2000) Fishing, selection and phenotypic evolution. ICES J Mar Sci 57:659–669. doi:10.1006/jmsc.2000.0731

    Article  Google Scholar 

  • Law R (2007) Fisheries-induced evolution: present status and future directions. Mar Ecol Prog Ser 335:271–277

    Article  Google Scholar 

  • Law R, Grey DR (1989) Evolution of yields from populations with age-specific cropping. Evol Ecol 3:343–359

    Article  Google Scholar 

  • Law W, Salick J (2005) Human-induced dwarfing of Himalayan snow lotus, Saussurea laniceps (Asteraceae). Proc Natl Acad Sci USA 102:10218–10220. doi:10.1073/pnas.0502931102

    Article  PubMed  CAS  Google Scholar 

  • Marshall CT, McAdam BJ (2007) Integrated perspectives on genetic and environmental effects on maturation can reduce potential for errors of inference. Mar Ecol Prog Ser 335:301–310

    Article  Google Scholar 

  • Miethe T, Dytham C, Dieckmann U, Pitchford JW (2010) Marine reserves and the evolutionary effects of fishing on size at maturation. ICES J Mar Sci 67:412–425. doi:10.1093/icesjms/fsp248

    Article  Google Scholar 

  • Munday PL, Wilson SK (1997) Comparative efficacy of clove oil and other chemicals in anaesthetization of Pomacentrus amboinensis, a coral reef fish. J Fish Biol 51:931–938

    CAS  Google Scholar 

  • Myers RA, Hoenig JM (1997) Direct estimates of gear selectivity from multiple tagging experiments. Can J Fish Aquat Sci 54:1–9

    Article  Google Scholar 

  • Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of Northern cod. Nature 428:932–935. doi:10.1038/nature.02430

    Article  PubMed  CAS  Google Scholar 

  • Olsen EM, Knutsen H, Gjøsæter J, Jorde PE, Knutsen JA, Stenseth NC (2008) Small-scale biocomplexity in coastal Atlantic cod supporting a Darwinian perspective on fisheries management. Evol Appl 1:524–533. doi:10.1111/j.1752-4571.2008.00024.x

    Article  Google Scholar 

  • Olsen EM, Carlson SM, Gjøsæter J, Stenseth NC (2009) Nine decades of decreasing phenotypic variability in Atlantic cod. Ecol Lett 12:622–631. doi:10.1111/j.1461-0248.2009.01311.x

    Article  PubMed  Google Scholar 

  • Palumbi S (2001) Humans as the world’s greatest evolutionary force. Science 293:1786–1790

    Article  PubMed  CAS  Google Scholar 

  • Pelletier F, Garant D, Hendry AP (2009) Eco-evolutionary dynamics. Phil Trans R Soc B 364:1483–1489. doi:10.1098/rstb.2009.0027

    Article  PubMed  CAS  Google Scholar 

  • Pine WE, Pollock KH, Hightower JE, Kwak TJ, Rice JA (2003) A review of tagging methods for estimating fish population size and components of mortality. Fisheries 28:10–23

    Article  Google Scholar 

  • Pollock KH, Hoenig JM, Hearn WS, Calingaert B (2001) Tag reporting rate estimation: 1. An evaluation of the high-reward tagging method. N Am J Fish Manage 21:521–532

    Article  Google Scholar 

  • Reznick DA, Bryga H, Endler JA (1990) Experimentally induced life-history evolution in a natural population. Nature 346:357–359

    Article  Google Scholar 

  • Rijnsdorp AD (1993) Fisheries as a large-scale experiment on life-history evolution: disentangling phenotypic and genetic effects in changes in maturation and reproduction of North Sea plaice, Pleuronectes platessa, L. Oecologia 96:391–401

    Article  Google Scholar 

  • Russ GR, Cheal AJ, Dolman AM, Emslie MJ, Evans RD, Miller I, Sweatman H, Williamson DH (2008) Rapid increase in fish numbers follows creation of world’s largest marine reserve network. Curr Biol 18:514–515

    Article  Google Scholar 

  • Sars GO (1865) On the reproduction of the winter cod (Gadus morrhua). Nor Acad Sci Lett 1:237–249 (in Norwegian)

    Google Scholar 

  • Schluter D (1988) Estimating the form of natural selection on a quantitative trait. Evolution 42:849–861

    Article  Google Scholar 

  • Siepielski AM, DiBattista JD, Carlson SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276. doi:10.1111/j.1461-0248.2009.01381.x

    Article  PubMed  Google Scholar 

  • Svedäng H, Bardon G (2003) Spatial and temporal aspects of the decline in cod (Gadus morhua L.) abundance in the Kattegat and eastern Skagerrak. ICES J Mar Sci 60:32–37. doi:10.1006/jmsc.2002.1330

    Article  Google Scholar 

  • Swain DP (2010) Life-history evolution and elevated natural mortality in a population of Atlantic cod (Gadus morhua). Evol Appl (in press). doi:10.1111/j.1752-4571.2010.00128.x

  • Swain DP, Sinclair AF, Hanson JM (2007) Evolutionary response to size-selective mortality in an exploited fish population. Proc R Soc B 274:1015–1022. doi:10.1098/rspb.2006.0275

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Venturelli PA, Shuter BJ, Murphy CA (2009) Evidence for harvest-induced maternal influences on the reproductive rates of fish populations. Proc R Soc B 276:919–924. doi:10.1098/rspb.2008.1507

    Article  PubMed  Google Scholar 

  • Vetter EF (1988) Estimation of natural mortality in fish stocks: a review. Fish Bull 86:25–43

    Google Scholar 

  • Walsh MR, Munch SB, Chiba S, Conover DO (2006) Maladaptive changes in multiple traits caused by fishing: impediments to population recovery. Ecol Lett 9:142–148. doi:10.1111/j.1461-0248.2005.00858.x

    Article  PubMed  Google Scholar 

  • Zeller DC (1999) Ultrasonic telemetry: its application to coral reef fisheries research. Fish Bull 97:1058–1065

    Google Scholar 

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Acknowledgments

We thank Jan Atle Knutsen for skilled surgical implantation of the acoustic transmitters and a number of people at the Flødevigen marine research station for help with the telemetry monitoring. Suggestions from three anonymous referees improved the quality of this article. This study was presented at the International Conference on Evolutionary Ecology of Fishes Diversification, Adaptation and Speciation, November 2009, Erkner, Berlin. Our work was funded by the Norwegian Research Council through the Oceans and the Coastal Areas programme, project 178376.

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Correspondence to Esben Moland Olsen.

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Olsen, E.M., Moland, E. Fitness landscape of Atlantic cod shaped by harvest selection and natural selection. Evol Ecol 25, 695–710 (2011). https://doi.org/10.1007/s10682-010-9427-9

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