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Thermal reaction norms for growth vary among cohorts of Pacific cod (Gadus macrocephalus)

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Abstract

While much effort has been directed at determining the spatial scales of adaptation in thermal reaction norms for growth, it is widely assumed that these reaction norms have high temporal stability. Water temperatures in the Gulf of Alaska in 2007 were the coldest on record since the mid-1970s and we present evidence that the thermal reaction norm for growth of age-0 Pacific cod (Gadus macrocephalus) in this cohort differed significantly from two adjacent cohorts. In addition to exhibiting higher growth potential at low temperatures, the 2007 cohort had a higher mean vertebral count, consistent with the widespread thermal effect known as “Jordan’s Rule.” Variation among cohorts in these physiological and morphological traits suggests a persistent response to environmental history (epigenetic effect). Temperature-induced phenotypic plasticity in the reaction norm for growth has significant implications for using growth rates to evaluate habitat quality and illustrates the complex responses of fishes to climate variability.

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References

  • Alderdice DF, Forrester CR (1971) Effects of salinity, temperature, and dissolved oxygen on early development of the Pacific cod (Gadus macrocephalus). J Fish Res Bd Can 28:883–902

    Article  Google Scholar 

  • Ali M, Nicieza A, Wootton RJ (2003) Compensatory growth in fishes: a response to growth depression. Fish Fish 4:147–190. doi:10.1046/j.1467-2979.2003.00120.x

    Article  Google Scholar 

  • Angilletta MJ, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268. doi:10.1016/S0169-5347(03)00087-9

    Article  Google Scholar 

  • Bashey F (2006) Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata. Evolution 60:348–361. doi:10.1554/05-087.1

    Google Scholar 

  • Brander K (1979) The relationship between vertebral number and water temperature in cod. J Cons Int Explor Mer 38:286–292

    Google Scholar 

  • Buckley LJ, Caldarone EM, Lough RG, St. Onge-Burns JM (2006) Ontogenetic and seasonal trends in recent growth rates of Atlantic cod and haddock larvae on Georges Bank: effects of photoperiod and temperature. Mar Ecol Prog Ser 325:205–226. doi:10.3354/meps325205

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Burt JM, Hinch SG, Patterson DA (2011) The importance of parentage in assessing temperature effects on fish early life history: a review of the experimental literature. Rev Fish Biol Fish 21:377–406. doi:10.1007/s11160-010-9179-1

    Article  Google Scholar 

  • Clemmesen C, Buhler V, Carvalho G, Case R, Evans G, Hauser L, Hutchinson WF, Kjesbu OS, Mempel H, Moksness E, Otterå H, Paulsen H, Thorsen A, Svaasand T (2003) Variability in condition and growth of Atlantic cod larvae and juveniles reared in mesocosms: environmental and maternal effects. J Fish Biol 62:706–723. doi:10.1046/j.1095-8649.2003.00060.x

    Article  Google Scholar 

  • Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Amer Nat 123:297–313

    Article  Google Scholar 

  • Conover DO, Clarke LM, Munch SB, Wagner GN (2006) Spatial and temporal scales of adaptive divergence in marine fishes and the implications for conservation. J Fish Biol 69(Suppl. C):21–47. doi:10.1111/j.1095-8649.2006.01274.x

    Article  Google Scholar 

  • Conover DO, Duffy TA, Hice LA (2010) The covariance between genetics and environmental influences across ecological gradients: Reassessing the evolutionary significance of countergradient and cogradient variation. In: Schlichting CD, Mousseau TA (eds) The year in evolutionary biology 2009. Wiley, New York, pp 100–129

    Google Scholar 

  • Cunningham KM, Canino MF, Spies IB, Hauser L (2009) Genetic isolation by distance and localized fjord population structure in Pacific cod (Gadus macrocephalus): limited effective dispersal in the northeastern Pacific Ocean. Can J Fish Aquat Sci 66:153–166. doi:10.1139/F08-199

    Article  CAS  Google Scholar 

  • Davis MW, Ottmar ML (2009) Vertical distribution of juvenile Pacific cod Gadus macrocephalus: potential role of light, temperature, food, and age. Aquat Biol 8:29–37. doi:10.3354/ab00209

    Article  Google Scholar 

  • Dentry W, Lindsey CC (1978) Vertebral variation in zebrafish (Brachydanio-rerio) related to pre-fertilization temperature history of their parents. Can J Zool 56:280–283. doi:10.1139/z78-037

    Article  Google Scholar 

  • Dunn JR, Matarese AC (1987) A review of the early life history of northeast Pacific gadoid fishes. Fish Res 5:163–184

    Article  Google Scholar 

  • Dutil JD, Jabouin C, Larocque R, Desrosiers G, Blier PU (2008) Atlantic cod (Gadus morhua) from cold and warm environments differ in their maximum growth capacity at low temperatures. Can J Fish Aquat Sci 65:2579–2591. doi:10.1139/f08-159

    Article  Google Scholar 

  • Folkvord A (2005) Comparison of size-at-age of larval Atlantic cod (Gadus morhua) from different populations based on size- and temperature-dependent growth models. Can J Fish Aquat Sci 62:1037–1052. doi:10.1139/F05-008

    Article  Google Scholar 

  • Folkvord A, Otterå H (1993) Effects of initial size distribution, day length, and feeding frequency on growth, survival, and cannibalism in juvenile Atlantic cod (Gadus morhua L). Aquaculture 114:243–260. doi:10.1016/0044-8486(93)90300-n

    Article  Google Scholar 

  • Fowler AJ (1970) Control of vertebral number in teleosts—an embryological problem. Quart Rev Biol 45:148–167

    Article  Google Scholar 

  • Freitas V, Campos J, Fonds M, Van der Veer HW (2007) Potential impact of temperature change on epibenthic predator-bivalve prey interactions in temperate estuaries. J Therm Biol 32:328–340. doi:10.1016/j.jtherbio.2007.04.004

    Article  Google Scholar 

  • Green BS (2008) Maternal effects in fish populations. In: Sims DW (ed) Advances in marine biology, vol 54. Elsevier Academic Press Inc, San Diego, pp 1–105

    Google Scholar 

  • Green BS, McCormick MI (2005) Maternal and paternal effects determine size, growth and performance in larvae of a tropical reef fish. Mar Ecol Prog Ser 289:263–272

    Article  Google Scholar 

  • Gunnarsson B, Jonasson JP, McAdam BJ (2010) Variation in hatch date distributions, settlement and growth of juvenile plaice (Pleuronectes platessa L.) in Icelandic waters. J Sea Res 64:61–67. doi:10.1016/j.seares.2009.10.010

    Article  Google Scholar 

  • Harrald M, Neat FC, Wright PJ, Fryer RJ, Huntingford FA (2010) Population variation in thermal growth responses of juvenile Atlantic cod (Gadus morhua L.). Environ Biol Fish 87:187–194. doi:10.1007/s10641-010-9586-0

    Article  Google Scholar 

  • Huey RB, Kingsolver JG (1989) Evolution of thermal sensitivity of ectotherm performance. Trends Ecol Evol 4:131–135. doi:10.1016/0169-5347(89)90211-5

    Article  CAS  Google Scholar 

  • Hurst TP, Abookire AA (2006) Temporal and spatial variation in potential and realized growth rates of age-0 northern rock sole. J Fish Biol 68:905–919. doi:10.1111/j.1095-8649.2006.00985.x

    Article  Google Scholar 

  • Hurst TP, Spencer ML, Sogard SM, Stoner AW (2005) Compensatory growth, energy storage and behavior of juvenile Pacific halibut Hippoglossus stenolepis following a thermally induced growth reduction. Mar Ecol Prog Ser 293:233–340. doi:10.3354/meps293233

    Article  Google Scholar 

  • Hurst TP, Cooper DW, Scheingross JS, Seale EM, Laurel BJ, Spencer ML (2009) Effects of ontogeny, temperature, and light on vertical movements of larval Pacific cod (Gadus macrocephalus). Fish Oceanogr 18:301–311. doi:10.1111/j.1365-2419.2009.00512.x

    Article  Google Scholar 

  • Hurst TP, Abookire AA, Knoth B (2010a) Quantifying thermal effects on contemporary growth variability to predict responses to climate change in northern rock sole (Lepidopsetta polyxystra). Can J Fish Aquat Sci 67:97–107. doi:10.1139/F09-171

    Article  Google Scholar 

  • Hurst TP, Laurel BJ, Ciannelli L (2010b) Ontogenetic patterns and temperature-dependence of growth rate in early life stages of Pacific cod (Gadus macrocephalus). Fish Bull 108:382–392

    Google Scholar 

  • Hutchings JA, Swain DP, Rowe S, Eddington JD, Puvanendran V, Brown JA (2007) Genetic variation in life-history reaction norms in a marine fish. Proc Royal Soc Lond 274:1693–1699. doi:10.1098/rspb.2007.0263

    Article  Google Scholar 

  • Ihssen PE, Booke HE, Casselman JM, McGlade JM, Payne NR, Utter FM (1981) Stock identification—materials and methods. Can J Fish Aquat Sci 38:1838–1855. doi:10.1139/f81-230

    Article  Google Scholar 

  • Imsland AK, Foss A, Koedijk R, Folkvord A, Stefansson SO, Jonassen TM (2006) Short- and long-term differences in growth, feed conversion efficiency and deformities in juvenile Atlantic cod (Gadus morhua) startfed on rotifers or zooplankton. Aquac Res 37:1015–1027. doi:10.1111/j.1365-2109.2006.01523.x

    Article  Google Scholar 

  • Imsland AK, Foss A, Koedijk R, Folkvord A, Stefansson SO, Jonassen TM (2007) Persistent growth effects of temperature and photoperiod in Atlantic cod Gadus morhua. J Fish Biol 71:1371–1382. doi:10.1111/j.1095-8649.2007.01600.x

    Article  Google Scholar 

  • Janhunen M, Piironen J, Peuhkuri N (2010) Parental effects on embryonic viability and growth in Arctic charr Salvelinus alpinus at two incubation temperatures. J Fish Biol 76:2558–2570. doi:10.1111/j.1095-8649.2010.02648.x

    Article  CAS  Google Scholar 

  • Janout MA, Weingartner TJ, Royer TC, Danielson SL (2009) On the nature of winter cooling and the recent temperature shift on the northern Gulf of Alaska shelf. J Geophys Res 115:C05023. doi:10.1029/2009JC005774

    Article  Google Scholar 

  • Johnston IA, Lee HT, Macqueen DJ, Paranthaman K, Kawashima C, Anwar A, Kinghorn JR, Dalmay T (2009) Embryonic temperature affects muscle fibre recruitment in adult zebrafish: genome-wide changes in gene and microRNA expression associated with the transition from hyperplastic to hypertrophic growth phenotypes. J Exp Biol 212:1781–1793. doi:10.1242/jeb.029918

    Article  CAS  Google Scholar 

  • King JR, Shuter BJ, Zimmerman AP (1999) Empirical links between thermal habitat, fish growth, and climate change. Trans Am Fish Soc 128:656–665. doi:10.1577/1548-8659

    Article  Google Scholar 

  • Kingsolver JG, Izem R, Ragland GJ (2004) Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves. Integr Comp Biol 44:450–460. doi:10.1093/icb/44.6.450

    Article  Google Scholar 

  • Laurel BJ, Hurst TP, Ciannelli L (2011) An experimental examination of temperature interactions in the match-mismatch hypothesis for Pacific cod larvae. Can J Fish Aquat Sci 68:51–61. doi:10.1139/F10-130

    Article  Google Scholar 

  • Lindsey CC (1988) Factors controlling meristic variation. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XI. Academic Press, San Diego, pp 197–274

    Google Scholar 

  • Løken S, Pedersen T (1996) Effect of parent type and temperature on vertebrae number in juvenile cod, Gadus morhua (L.), in northern Norway. Sarsia 80:293–298

    Google Scholar 

  • Martell DJ, Kieffer JD (2007) Persistent effects of incubation temperature on muscle development in larval haddock (Melanogrammus aeglefinus L.). J Exp Biol 210:1170–1182. doi:10.1242/jeb.002188

    Article  Google Scholar 

  • McDowall RM (2008) Jordan’s rule and other ecogeographical rules, and the vertebral number in fishes. J Biogeogr 35:501–508. doi:10.1111/j.1365-2699.2007.01823.x

    Article  Google Scholar 

  • McNab BK (2002) The physiological ecology of vertebrates. Comstock, Ithaca

    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. doi:10.3354/meps07138

    Article  Google Scholar 

  • Munch SB, Conover DO (2003) Rapid growth results in increased susceptibility to predation in Menidia menidia. Evolution 57:2119–2127. doi:10.1554/02-711

    Google Scholar 

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

    Article  Google Scholar 

  • Ospina-Álvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 3:e2837. doi:10.1371/journal.pone.0002837

    Article  Google Scholar 

  • Plaistow SJ, Benton TG (2009) The influence of context-dependent maternal effects on population dynamics: an experimental test. Philos Trans R Soc B 364:1049–1058. doi:10.1098/rstb.2008.0251

    Article  CAS  Google Scholar 

  • Power M, Attrill MJ (2007) Temperature-dependent temporal variation in the size and growth of Thames estuary smelt Osmerus eperlanus. Mar Ecol Prog Ser 330:213–222. doi:10.3354/meps330213

    Article  Google Scholar 

  • Rakocinski CF, Peterson MS, Comyns BH, Zapfe GA, Fulling GL (2006) Do abiotic factors drive the early growth of juvenile spot (Leiostomus xanthurus)? Fish Res 82:186–193. doi:10.1016/j.fishres.2006.06.006

    Article  Google Scholar 

  • Rijnsdorp AD, Peck MA, Ehngelhard GH, Möllmann C, Pinnegar J (2009) Resolving the effect of climate change on fish populations. ICES J Mar Sci 66:1570–1583. doi:10.1093/icesjms/fsp056

    Article  Google Scholar 

  • Ryer CH, Hurst TP (2008) Indirect predator effects on age-0 northern rock sole Lepidopsetta polyxystra: growth suppression and temporal reallocation of feeding. Mar Ecol Prog Ser 357:207–212. doi:10.3354/meps07303

    Article  Google Scholar 

  • Salinas S, Munch SB (2012) Thermal legacies: transgenerational effects of temperature on growth in a vertebrate. Ecol Lett 15:159–163. doi:10.1111/j.1461-0248.2011.01721.x

    Article  Google Scholar 

  • Schaefer J, Ryan A (2006) Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. J Fish Biol 69:722–734. doi:10.1111/j.1095-8649.2006.01268.x

    Article  Google Scholar 

  • Schulte P (2004) Changes in gene expression as biochemical adaptations to environmental change: a tribute to Peter Hochachka. Comp Biochem Physiol 139:519–529. doi:10.1016/j.cbpc.2004.06.001

    Article  Google Scholar 

  • Searcy SP, Eggleston DB, Hare JA (2007) Is growth a reliable indicator of habitat quality and essential fish habitat for a juvenile estuarine fish? Can J Fish Aquat Sci 64:681–691. doi:10.1139/F07-038

    Article  Google Scholar 

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

    Google Scholar 

  • Sogard SM, Olla BL (1994) The potential for intracohort cannibalism in age-0 walleye pollock, Theragra chalcogramma, as determined under laboratory feeding conditions. Environ Biol Fishes 39:183–190. doi:10.1007/bf00004936

    Article  Google Scholar 

  • Stillman JH (2003) Acclimation capacity underlies susceptibility to climate change. Science 301:65

    Article  CAS  Google Scholar 

  • Swain DP, Frank KT (2000) Depth-dependent vertebral number of Atlantic cod (Gadus morhua) on the Magdalen Shallows and Scotian Shelf: stock mixing or microgeographic trends within populations? Can J Fish Aquat Sci 57:2393–2401. doi:10.1139/cjfas-57-12-2393

    Article  Google Scholar 

  • Swain DP, Lindsey CC (1984) Selective predation for vertebral number of young sticklebacks, Gasterosteus aculeatus. Can J Fish Aquat Sci 41:1231–1233. doi:10.1139/f84-146

    Article  Google Scholar 

  • Swain DP, Lindsey CC (1986) Meristic variation in a clone of the Cyprinodont fish Rivulus-marmoratus related to temperature history of the parents and of the embryos. Can J Zool 64:1444–1455. doi:10.1139/z86-216

    Article  Google Scholar 

  • Swain DP, Frank KT, Maillet G (2001) Delineating stocks of Atlantic cod (Gadus morhua) in the Gulf of St Lawrence and Cabot Strait areas using vertebral number. ICES J Mar Sci 58:253–269. doi:10.1006/jmsc.2000.1007

    Article  Google Scholar 

  • Travis J, McManus MG, Baer CF (1999) Sources of variation in physiological phenotypes and their evolutionary significance. Am Zool 39:422–433

    Google Scholar 

  • Van der Veer HW, Bies B, Witte JI (2000) Selective predation and mortality of juvenile 0-group plaice Pleuronectes platessa in the Dutch Wadden Sea: a consequence of irreversible non-genetic adaptation during early pelagic life. Mar Ecol Prog Ser 197:273–283. doi:10.3354/meps197273

    Article  Google Scholar 

  • van Doorslaer W, Stocks R (2005) Thermal reaction norms in two Coenagrion damselfly species: contrasting embryonic and larval life-history traits. Freshw Biol 50:1982–1990

    Article  Google Scholar 

  • Weingartner T, Eisner L, Eckert GL, Danielson S (2009) Southeast Alaska: oceanographic habitats and linkages. J Biogeogr 36:387–400. doi:10.1111/j.1365-2699.2008.01994.x

    Article  Google Scholar 

  • Wijekoon MP, Puvanendran V, Ings DW, Brown JA (2009) Possible countergradient variation in growth of juvenile cod Gadus morhua from the northwest Atlantic. Mar Ecol Prog Ser 375:229–238. doi:10.3354/meps07760

    Article  Google Scholar 

  • Youngson NA, Whitelaw E (2008) Transgenerational epigenetic effects. Ann Rev Genom Hum Gen 9:233–257. doi:10.1146/annurev.genom.9.081307.164445

    Article  CAS  Google Scholar 

  • Zijlstra JJ, Dapper R, Witte JI (1982) Settlement, growth and mortality of post-larval plaice (Pleuronectes platessa L.) in the western Wadden Sea. Neth J Sea Res 15:250–272

    Article  Google Scholar 

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Acknowledgments

The authors thank T. Tripp, M. Spencer, B. Knoth, and B. Laurel for assistance with fish collection and shipping. Staff in the AFSC-Fisheries Behavioral Ecology Program including S. Haines, M. Ottmar, P. Iseri assisted with growth experiments. Assistance with X-rays was provided by D. Simon and D. Markle. This manuscript benefitted from discussions with C. Schreck. B. Laurel, A. Stoner, J. Miller, and two anonymous reviewers provided valuable comments on this manuscript. K.A.L. was supported by a National Science Foundation Research Experience for Undergraduates internship under award OCE-0648515 to the Hatfield Marine Science Center of Oregon State University. This work was also supported in part by a grant from the North Pacific Research Board (#R0605 to B. Laurel et al.). This is publication #353 of the North Pacific Research Board. The findings and conclusions in this paper are those of the authors and do not necessarily represent the views of the National Marine Fisheries Service. Reference to trade names does not imply endorsement by the National Marine Fisheries Service.

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  1. Kate A. Lavelle

    Present address: Harte Research Institute 314, Unit 5869, Texas A&M University-Corpus Christi, 6300 Ocean Drive, Corpus Christi, TX, 78412, USA

Authors and Affiliations

  1. Resource Assessment and Conservation Engineering Division, Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2030 S. Marine Science Drive, Newport, OR, 97365, USA

    Thomas P. Hurst

  2. Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, NOAA, 110 Shaffer Rd., Santa Cruz, CA, 95060, USA

    Stephan B. Munch

  3. Hatfield Marine Science Center, Oregon State University, Newport, OR, 97365, USA

    Kate A. Lavelle

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Correspondence to Thomas P. Hurst.

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Hurst, T.P., Munch, S.B. & Lavelle, K.A. Thermal reaction norms for growth vary among cohorts of Pacific cod (Gadus macrocephalus). Mar Biol 159, 2173–2183 (2012). https://doi.org/10.1007/s00227-012-2003-9

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