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If and when: intrinsic differences and environmental stressors influence migration in brown trout (Salmo trutta)

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Abstract

Partial migration is a common phenomenon, yet the causes of individual differences in migratory propensity are not well understood. We examined factors that potentially influence timing of migration and migratory propensity in a wild population of juvenile brown trout (Salmo trutta) by combining experimental manipulations with passive integrated transponder telemetry. Individuals were subjected to one of six manipulations: three designed to mimic natural stressors (temperature increase, food deprivation, and chase by a simulated predator), an injection of exogenous cortisol designed to mimic an extreme physiological challenge, a sham injection, and a control group. By measuring length and mass of 923 individuals prior to manipulation and by monitoring tagged individuals as they left the stream months later, we assessed whether pre-existing differences influenced migratory tendency and timing of migration, and whether our manipulations affected growth, condition, and timing of migration. We found that pre-existing differences predicted migration, with smaller individuals and individuals in poor condition having a higher propensity to migrate. Exogenous cortisol manipulation had the largest negative effect on growth and condition, and resulted in an earlier migration date. Additionally, low-growth individuals within the temperature and food deprivation treatments migrated earlier. By demonstrating that both pre-existing differences in organism state and additional stressors can affect whether and when individuals migrate, we highlight the importance of understanding individual differences in partial migration. These effects may carry over to influence migration success and affect the evolutionary dynamics of sub-populations experiencing different levels of stress, which is particularly relevant in a changing world.

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References

  • Aarestrup K, Nielsen C, Koed A (2002) Net ground speed of downstream migrating radio-tagged Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.) smolts in relation to environmental factors. Hydrobiol 48:95–102

    Article  Google Scholar 

  • Aarestrup K, Birnie-Gauvin K, Larsen MH (2017) Another paradigm lost? Autumn downstream migration of juvenile brown trout: evidence for a presmolt migration. Ecol Fresh Fish. doi:10.1111/eff.12335

    Google Scholar 

  • Acolas ML, Labonne J, Bagliniere JL (2012) The role of body size versus growth on the decision to migrate: a case study with Salmo trutta. Naturwissenchaften 99:11–21

    Article  CAS  Google Scholar 

  • Armbruster WS, Pelabon C, Bolstad GH, Hansen TF (2014) Integrated phenotypes: understanding trait covariation in plants and animals. Philos Trans Roy Soc B Biol Sci 369:20130245

    Article  Google Scholar 

  • Avgar T, Street G, Fryxell JM (2013) On the adaptive benefits of mammal migration. Can J Zool 92:481–490

    Article  Google Scholar 

  • Baker MR, Gobush KS, Vynne CH (2013) Review of factors influencing stress hormones in fish and wildlife. J Nat Conserv 21:309–318

    Article  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integ Comp Biol 42:517–525

    Article  CAS  Google Scholar 

  • Benjamin JR, Connolly PJ, Romine JG, Perry RW (2013) Potential effects of changes in temperature and food resources on life history trajectories of juvenile Oncorhynchus mykiss. Trans Am Fish Soc 142:208–220

    Article  Google Scholar 

  • Boel M, Aarestrup K, Baktoft H, Larsen T, Madsen SS, Malte H, Skov C, Svendsen JC, Koed A (2014) The physiological basis of the migration continuum in brown trout (Salmo trutta). Physiol Biochem Zool 87:334–345

    Article  PubMed  Google Scholar 

  • Bohlin T, Dellefors C, Faremo U (1994) Probability of first sexual maturation of male parr in wild sea-run brown trout (Salmo trutta) depends on condition factor 1 yr in advance. Can J Fish Aquat Sci 51:1920–1926

    Article  Google Scholar 

  • Bohlin T, Dellefors C, Faremo U (1996) Date of smolt migration depends on body-size but not age in wild sea-run brown trout. J Fish Biol 49:157–164

    Article  Google Scholar 

  • Boyle WA (2008) Partial migration in birds: tests of three hypotheses in a tropical lekking frugivore. J Anim Ecol 77:1122–1128

    Article  PubMed  Google Scholar 

  • Brodersen J, Nilsson PA, Hansson L-A, Skov C, Bronmark C (2008) Condition-dependent individual decision-making determines cyprinid partial migration. Ecology 89:1195–1200

    Article  PubMed  Google Scholar 

  • Brodersen J, Chapman BB, Nilsson PA, Skov C, Hansson L-A, Bronmark C (2014) Fixed and flexible: coexistence of obligate and facultative migratory strategies in a freshwater fish. PLoS One 9:390294

    Article  Google Scholar 

  • Chapman BB, Bronmark C, Nilsson J-A, Hansson L-A (2011a) The ecology and evolution of partial migration. Oikos 120:1764–1775

    Article  Google Scholar 

  • Chapman BB, Hulthen K, Blomqvist DR, Hansson L-A, Nilsson J-A, Brodersen J, Nilsson PA, Skov C, Bronmark C (2011b) To boldly go: individual differences in boldness influence migratory tendency. Eco Lett 14:871–876

    Article  Google Scholar 

  • Chapman BB, Skov C, Hulthen K, Brodersen J, Nilsson PA, Hansson L-A, Bronmark C (2012a) Partial migration in fishes: definitions, methodologies and taxonomic distribution. J Fish Biol 81:479–499

    Article  CAS  PubMed  Google Scholar 

  • Chapman BB, Hulthen K, Brodersen J, Nilsson PA, Skov C, Hansson L-A, Bronmark C (2012b) Partial migration in fishes: causes and consequences. J Fish Biol 81:456–478

    Article  CAS  PubMed  Google Scholar 

  • Crespi EJ, Williams TD, Jessop TS, Delehanty B (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals? Funct Ecol 27:93–106

    Article  Google Scholar 

  • Crossin GT, Love OP, Cooke SJ, Williams TD (2016) Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context, and reproductive state. Funct Ecol 30:116–125

    Article  Google Scholar 

  • Cucherousset J, Ombredane D, Charles K, Marchand F, Bagliniere J-L (2005) A continuum of life history tactics in a brown trout (Salmo trutta) population. Can J Fish Aquat Sci 62:1600–1610

    Article  Google Scholar 

  • del Villar-Guerra D, Arrestrup K, Skov C, Koed A (2014) Marine migrations in anadromous brown trout (Salmo trutta). Fjord residency as a possible alternative in the continuum of migration to the open sea. Ecol Fresh Fish 23:594–603

    Article  Google Scholar 

  • Donaldson MR, Clark TD, Hinch SG, Cooke SJ, Patterson DA, Gale MK, Frappell PB, Farrell AP (2010) Physiological responses of free-swimming adult coho salmon to simulated predator and fisheries encounters. Physiol Biochem Zool Ecol Evol Approaches 8:973–983

    Article  Google Scholar 

  • Eros SK, Milligan CL (1996) The effect of cortisol on recovery from exhaustive exercise in rainbow trout (Oncorhynchus mykiss): potential mechanisms of action. Physiol Zool 69:1196–1214

    Article  CAS  Google Scholar 

  • Folkedal O, Stien LH, Torgersen T, Oppedal F, Oslen RE, Fosseidengen JE, Braithwaite VA, Kristiansen TS (2012) Food anticipatory behavior as an indicator of stress response and recovery in Atlantic salmon post-smolt after exposure to acute temperature fluctuation. Physiol Behav 105:350–356

    Article  CAS  PubMed  Google Scholar 

  • Forseth T, Naesje TF, Jonsson B, Harsaker K (1999) Juvenile migration in brown trout: a consequence of energetic state. J Anim Ecol 8:783–793

    Article  Google Scholar 

  • Fullerton AH, Garvey JE, Wright RA, Stein RA (2000) Overwinter growth and survival of largemouth bass: interactions among size, food, origin, and winter severity. Trans Am Fish Soc 129:1–12

    Article  Google Scholar 

  • Gamperl AK, Vijayan MM, Boutilier RG (1994) Experimental control of stress hormone levels in fishes: techniques and applications. Rev Fish Biol Fish 4:215–255

    Article  Google Scholar 

  • Gibbons WJ, Andrews KM (2004) PIT tagging: simple technology at its best. Bioscience 54:447–454

    Article  Google Scholar 

  • Grayson KL, Wilbur HM (2009) Sex- and context-dependent migration in a pond-breeding amphibian. Ecology 90:306–311

    Article  PubMed  Google Scholar 

  • Gross MR (1987) Evolutionary of diadromy in fishes. Am Fish Soc Symp 1:14–25

    Google Scholar 

  • Handeland SO, Wilkinson E, Sveinsbo B, McCormick SD, Stefansson SO (2004) Temperature influence on the development and loss of seawater tolerance in two fast-growing strain of Atlantic salmon. Aquaculture 233:513–529

    Article  Google Scholar 

  • Harrison XA, Blount JD, Inger R, Norris DR, Bearhop S (2011) Carry-over effects as drivers of fitness differences in animals. J Anim Ecol 80:4–18

    Article  PubMed  Google Scholar 

  • Heugens EHW, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainly factors for use in risk assessment. Critical Rev Toxicol 31:247–284

    Article  CAS  Google Scholar 

  • Holmstrup M, Bindesbol A-M, Oostingh GJ, Duschl A, Scheil V, Kohler H-R, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Dramarz PE, Bayley M, Svendsen C, Spurgeon SJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762

    Article  CAS  PubMed  Google Scholar 

  • Iwama GK (1998) Stress in fish. Ann New York Acad Sci 851:304–310

    Article  Google Scholar 

  • Jahn AE, Levey DJ, Hostetler JA, Mamani AM (2010) Determinants of partial bird migration in the Amazon Basin. J Anim Ecol 79:983–992

    Article  PubMed  Google Scholar 

  • Jonsson B (1985) Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Trans Am Fish Soc 114:182–194

    Article  Google Scholar 

  • Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365

    Article  Google Scholar 

  • Jonsson B, Jonsson N (2009) A review of the likely effects of climate change on anadromous Atlantic salmon Salmo salar and brown trout Salmo trutta, with particular reference to water temperature and flow. J Fish Biol 75:2381–2447

    Article  CAS  PubMed  Google Scholar 

  • Kerr LA, Secor DH (2009) Bioenergetic trajectories underlying partial migration in Patuxent River (Chesapeake Bay) white perch (Morone americana). Can J Fish Aquat Sci 66:602–612

    Article  Google Scholar 

  • Ketterson ED, Nolan V Jr (1976) Geographic variation and its climatic correlates in the sex ratio of eastern-wintering dark-eyed juncos (Junco hyemalis hyemalis). Ecology 57:679–693

    Article  Google Scholar 

  • Lans L, Greenberg LA, Karlsson J, Calles O, Schmitz M, Bergman E (2011) The effects of ration size on migration by hatchery-raised Atlantic salmon (Salmo salar) and brown trout (Salmo trutta). Ecol Freshw Fish 20:548–557

    Article  Google Scholar 

  • Lendvai AZ, Ouyang JQ, Schoenle LA, Fasanello V, Haussmann MF, Bonier F, Moore IT (2014) Experimental food restriction reveals individual differences in corticosterone reaction norms with no oxidative costs. PLoS One 9:e110564

    Article  PubMed  PubMed Central  Google Scholar 

  • Lundberg P (1988) The evolution of partial migration in birds. Trends Ecol Evol 3:172–175

    Article  CAS  PubMed  Google Scholar 

  • Madaro A, Olsen RE, Kristiansen TS, Ebbesson LOE, Flik G, Gorissen M (2016) A comparative study of the response to repeated chasing stress in Atlantic salmon (Salmo salar L.) parr and post-smolts. Comp Biochem Physiol Part A 192:7–16

    Article  CAS  Google Scholar 

  • Metcalfe NB (1998) The interaction between behavior and physiology in determining life history patterns in Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 55:93–103

    Article  Google Scholar 

  • Metcalfe NB, Thorpe JE (1992) Early predictors of life-history events: the link between first feeding date, dominance and seaward migration in Atlantic salmon, Salmo salar L. J Fish Biol 41:93–99

    Article  Google Scholar 

  • Metcalfe NB, Huntingford FA, Thorpe JE, Adams CE (1990) The effects of social status on life-history variation in juvenile salmon. Can J Zool 68:2630–2636

    Article  Google Scholar 

  • Midwood JD, Larsen MH, Boel M, Jepsen N, Aarestrup K, Cooke SJ (2014) Does cortisol manipulation influence outmigration behaviour, survival and growth of sea trout? A field test of carryover effects in wild fish. Marine Ecol Prog Series 496:135–144

    Article  CAS  Google Scholar 

  • Midwood JD, Larsen MH, Boel M, Aarestrup K, Cooke SJ (2015) An experimental field evaluation of winter carryover effects in semi-anadromous brown trout (Salmo trutta). J Exp Zool 323A:645–654

    Article  Google Scholar 

  • Midwood JD, Larsen MH, Aarestrup K, Cooke SJ (2016) Stress and food deprivation: linking physiological state to migration success in a teleost fish. J Exp Biol. doi:10.1242/jeb.140665

    PubMed  Google Scholar 

  • Morinville GR, Rasmussen JB (2003) Early juvenile bioenergetics differences between anadromous and resident brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 60:401–410

    Article  Google Scholar 

  • Nordeng H (1983) Solution to the ‘char problem’ based on Artic char (Salvelinus alpinus) in Norway. Can J Fish Aquat Sci 40:1372–1387

    Article  Google Scholar 

  • O'Connor CM, Gilmour KM, Arlinghaus R, Van Der Kraak G, Cooke SJ (2009) Stress and parental care in a wild teleost fish: insights from exogenous supraphysiological cortisol implants. Physiol Biochem Zool 82(6):709–719

    Article  PubMed  Google Scholar 

  • O’Connor CM, Norris DR, Crossin GT, Cooke SJ (2014) Biological carryover effects: linking common concepts and mechanisms in ecology and evolution. Ecosphere 5:1–11

    Article  Google Scholar 

  • Olsson IC, Greenberg LA, Bergman E, Wysujack K (2006) Environmentally induced migration: the importance of food. Ecol Lett 9:645–651

    Article  PubMed  Google Scholar 

  • Otero J, L’Abee-Lund JH, Castro-Santos T, Leonardsson K, Storvik GO, Jonsson B, Dempson B, Russell IC, Jensen AJ, Bagliniere J-L, Dionne M, Armstrong JD, Romakkaniemi A, Letcher BH, Kocik JF, Erkinaro J, Poole R, Rogan G, Lundqvist H, Maclean JC, Jokikokko E, Arnekleiv JV, Kennedy RJ, Niemela E, Caballero P, Music PA, Antonsson T, Gudjonsson S, Veselov AE, Lamberg A, Groom S, Taylor BH, Taberner M, Dillane M, Arnason F, Horton G, Hvidsten NA, Jonsson IR, Jonsson N, McKelvey S, Naesje TF, Skaala O, Smith GW, Saegrov H, Stenseth NC, Vollestad LA (2014) Basin-scale phenology and effects of climate variability on global timing of initial seaward migration of Atlantic salmon (Salmo salar). Glob Change Biol 20:61–75

    Article  Google Scholar 

  • Paez DJ, Brisson-Bonenfant C, Rossignol O, Guderley HE, Bernatchez L, Dodson JJ (2011) Alternative developmental pathways and the propensity to migrate: a case study in the Atlantic salmon. J Evol Biol 24:245–255

    Article  CAS  PubMed  Google Scholar 

  • Pankhurst NW, Van Der Kraak G (1997) Effects of stress on reproduction and growth of fish. In: Iwama GK, Pickering AD, Sumpter JP, Schreck CB (eds) Fish stress and health in aquaculture. Cambridge University Press, New York, pp 73–93

    Google Scholar 

  • Pickering AD (1989) Environmental stress and the survival of brown trout, Salmo trutta. Freshw Biol 21:47–55

    Article  Google Scholar 

  • Pulido F (2011) Evolutionary genetics of partial migration—the threshold model of migration revis(it)ed. Oikos 120:1776–1783

    Article  Google Scholar 

  • Quigley JT, Hinch SG (2006) Effects of rapid experimental temperature increases on acute physiological stress and behaviour of stream dwelling juvenile chinook salmon. J Thermal Biol 31:429–441

    Article  Google Scholar 

  • Redding JM, DeLuze A, Leloup-Hatey J, Leloup J (1986) Suppression of plasma thyroid hormone concentrations by cortisol in the European eel Anguilla anguilla. Comp Biochem Physiol A 83:409–413

    Article  CAS  PubMed  Google Scholar 

  • Ricker WE (1975) Computation and interpretation of biological statistics of populations. Bull Fish Res Board Can 191:382

    Google Scholar 

  • Roff DA, Fairbairn DJ (2007) The evolution and genetics of migration in insects. Bioscience 57:155–164

    Article  Google Scholar 

  • Romero LM (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    Article  PubMed  Google Scholar 

  • Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gen Comp Endocr 165:549–556

    Article  CAS  PubMed  Google Scholar 

  • Skov C, Brodersen J, Nilsson PA, Hansson L-A, Bronmark C (2008) Inter- and size-specific patterns of fish seasonal migration between a shallow lake and its streams. Ecol Freshwater Fish 17:406–415

    Article  Google Scholar 

  • Skov C, Baktoft H, Brodersen J, Bronmark C, Chapman BB, Hansson L-A, Nilsson PA (2010) Sizing up your enemy: individual predation vulnerability predicts migratory probability. Proc R Soc B 278:1414–1418

    Article  PubMed  PubMed Central  Google Scholar 

  • Sopinka NM, Patterson LD, Redfern JC, Pleizier NK, Belanger CB, Midwood JD, Crossin GT, Cooke SJ (2015) Manipulating glucocorticoids in wild animals: basic and applied perspectives. Conserv Physiol 3:cov031

    Article  PubMed  PubMed Central  Google Scholar 

  • Strange RJ, Schreck CB, Golden JT (1977) Corticoid stress responses to handling and temperature in salmonids. Trans Am Fish Soc 106:213–218

    Article  CAS  Google Scholar 

  • Sumpter JP, Le Bail PY, Pickering AD, Pottinger TG, Carragher JF (1991) The effect of starvation on growth and plasma growth hormone concentrations of rainbow trout, Oncorhynchus mykiss. Gen Comp Endocr 83:94–102

    Article  CAS  PubMed  Google Scholar 

  • Terrill SB, Able KP (1988) Bird migration terminology. Auk 105:205–206

    Google Scholar 

  • Theriault V, Dodson JJ (2003) Body size and the adoption of a migratory tactic in brook charr. J Fish Biol 63:1144–1159

    Article  Google Scholar 

  • Theriault V, Dunlop ES, Dieckmann U, Bernatchez L, Dodson JJ (2008) The impact of fishing-induced mortality on the evolution of alternative life-history tactics in brook charr. Evol Appl 1:409–423

    Article  PubMed  PubMed Central  Google Scholar 

  • Thorstad EB, Whoriskey F, Uglem I, Moore A, Rikardsen AH, Finstad B (2012) A critical life stage of the Atlantic salmon Salmo salar: behaviour and survival during the smolt and initial post-smolt migration. J Fish Biol 81:500–542

    Article  CAS  PubMed  Google Scholar 

  • Tipping JM, Byrne JB (1996) Reducing feed levels during the last month of rearing enhances emigration rates of hatchery-reared steelhead smolts. Progress Fish-Culturist 58:128–130

    Article  Google Scholar 

  • Van Leeuwen TE, Killen SS, Metcalfe NB, Adams CE (2016) Differences in early developmental rates and yolk conversion efficiency in offspring of trout with alternative life histories. Ecol Freshw Fish. doi:10.1111/eff.12281

    Google Scholar 

  • Wingfield JC (2008) Comparative endocrinology, environment and global change. Gen Comp Endocr 157:207–216

    Article  CAS  PubMed  Google Scholar 

  • Wingfield JC, Romero LM (2001) Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen BS (ed) Handbook of physiology, the endocrine system, coping with the environment: neural and endocrine mechanisms. Oxford University Press, Oxford, pp 211–236

    Google Scholar 

  • Winter ER, Tummers JS, Aarestrup K, Baktoft H, Lucas MC (2016) Investigating the phenology of seaward migration of juvenile brown trout (Salmo trutta) in two European populations. Hydrobiologia 775:139

    Article  CAS  Google Scholar 

  • Wysujack K, Greenberg LA, Bergman E, Olsson IC (2009) The role of the environment in partial migration: food availability affects the adoption of a migratory tactic in brown trout Salmo trutta. Ecol Freshw Fish 18:52–59

    Article  Google Scholar 

  • Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32:95–126

    Article  Google Scholar 

  • Zydlewski GB, Horton G, Dubreuil T, Letcher B, Casey S, Zydlewski J (2006) Remote monitoring of fish in small streams: a unified approach using PIT tags. Fisheries 31:492–502

    Article  Google Scholar 

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Acknowledgements

Funding for this project was made possible through a Natural Sciences and Engineering Research Council (NSERC) of Canada Discovery Grant and NSERC E. W. R. Steacie Fellowship awarded to S.J.C., the Canada Research Chairs program, grants from the Danish National Fishing License Funds to the Technical University of Denmark, and the Swedish Research Council Formas. The authors thank Ana Silva, Michael Holm, Hans-Jørn Christensen, Henrik Baktoft, Jørgen Skole Mikkelsen, Jes Dolby, and Morten Carøe for assistance in the field and technical support.

Author contribution statement

JDM, ADMW, KA, and SJC conceived and designed the experiments. JDM, MHL and ADMW performed the experiments. KSP and KB-G analyzed the data. KSP and KB-G wrote the manuscript; other authors provided editorial advice.

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Correspondence to Kathryn S. Peiman.

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All applicable institutional and/or national guidelines for the care and use of animals were followed. Methods were approved by Carleton University (Protocol Number 315774) and the Danish Technical University (protocol number: 2013-15-2934-00808).

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Communicated by Aaron J. Wirsing.

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Peiman, K.S., Birnie-Gauvin, K., Midwood, J.D. et al. If and when: intrinsic differences and environmental stressors influence migration in brown trout (Salmo trutta). Oecologia 184, 375–384 (2017). https://doi.org/10.1007/s00442-017-3873-9

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