Ecology of Atlantic Salmon and Brown Trout: Habitat as a template for life histories [1 ed.] 9400711883, 9789400711884
Destruction of habitat is the major cause for loss of biodiversity including variation in life history and habitat ecolo
246 77 10MB
English Pages 708 [732] Year 2011
Front Matter....Pages i-xxii
Habitats as Template for Life Histories....Pages 1-21
Species Diversity....Pages 23-66
Habitat Use....Pages 67-135
Development and Growth....Pages 137-209
Smolts and Smolting....Pages 211-245
Migrations....Pages 247-325
Maturation and Spawning....Pages 327-414
Recruitment, Mortality and Longevity....Pages 415-471
Climatic Effects on Atlantic Salmon and Brown Trout....Pages 473-515
Farmed Atlantic Salmon in Nature....Pages 517-566
Population Enhancement and Population Restoration....Pages 567-632
General Conclusions and Research Tasks....Pages 633-655
Back Matter....Pages 657-708
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Ecology of Atlantic Salmon and Brown Trout
FISH & FISHERIES SERIES VOLUME 33 Series Editor: David L.G. Noakes, Fisheries & Wildlife Department, Oregon State University, Corvallis, USA
For other titles published in this series, go to www.springer.com/series/5973
BrorJonsson • NinaJonsson
Ecology of Atlantic Salmon and Brown Trout Habitat as a Template for Life Histories
Bror Jonsson NorwegianInstitute forNatureResearch Oslo,Norway [email protected]
NinaJonsson NorwegianInstitute forNatureResearch Oslo,Norway [email protected]
ISBN978-94-007-1188-4 e-ISBN978-94-007-1189-1 DOI10.1007/978-94-007-1189-1 SpringerDordrechtHeidelbergLondonNewYork LibraryofCongressControlNumber:2011928085 ©SpringerScience+BusinessMediaB.V.2011 Nopartofthisworkmaybereproduced,storedinaretrievalsystem,ortransmittedinanyformorbyany means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose ofbeingenteredandexecutedonacomputersystem,forexclusiveusebythepurchaserofthework. Photo credit:©stephankerkhofs-Fotolia.com Printedonacid-freepaper Springer is part of Springer Science+Business Media (www.springer.com)
For Marte and Marius
Female brown trout hunting a mayfly, an important food item for this fish in fresh water. PhotographbyNinaJonsson.
Foreword
Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) share much of their nativeranges,withsomeimportantexceptions.Theyholdaplacedeartothehearts ofanglers,withsomeimportantexceptions.Theyhavebeendeliberatelyintroduced around the world by well–intentioned Europeans, but with important differences in the consequences. One of them, the Atlantic salmon, has now become the focal pointforapeculiarcombinationofconservationandcommercialproduction.The other,thebrowntrout,hasalwaysbeenthemoresecretive. Thereisnobookonthesefishesmoreimportantthanthis,andnobetterauthors to write this book. Atlantic salmon and brown trout are undoubtedly two of the most charismatic and some might say problematic fish species. Consider the Atlantic salmon. There is probably no fish more eagerly sought after by recreational anglerswhileatthesametimeitteeterssoclosetothebrinkofextinctionthroughout itsnativerange.Thereisaninternationalfederationdedicatedtotheconservationand managementofAtlanticsalmon.Incontrast,onthePacificcoastofNorthAmericaone wouldbehardpressedtonameafishspeciesmorereviledanddespisedbyitscritics. Itisatthesametimethemostvaluableandthecheapestsalmonspecies.Herbert Hoovercampaignedonthesloganof“Achickenineverypot,”inthedayswhen poultry was a luxury item on the dinner menu for the common folk, or perhaps reservedonlyforthewealthyelite.Butthatwas1928,andthedespairoftheGreat Depressionsoonendedhisvisionofculinaryegalitarianism.Eventuallythevision didcomeabout,andchickenbecameoneofthemostwidelyconsumedfooditems, and certainly one of the cheapest forms of animal protein. Entire international food franchises are now based on chicken. In fact we have the common expression “Tasteslikechicken”asourwayofsayingthatchickenhasbecometheuniversal standard of food. TraditionallyAtlanticsalmonheldanevenloftierrankthanchicken,intheform ofNovaScotialox,orgravlax,orNordicstylesmokedsalmon,orScottishstyle salmon or smoked salmon, or any of the other variants in countries around the North Atlantic. Atlantic salmon still holds iconic and linguistic status in many cultures.Wemighthavedreamedofsalmon,butneverdaredhopethatwecould affordsuchaluxury.Nopoliticianhadthetemeritytocampaignonthepromiseof
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“Asalmononeveryplate!”Andyetthattoohascometopass.Atlanticsalmonhas becomewidelyavailable,attrulymodestprices,asaresultofthepeculiartwistsof technologyandfate.Atlanticsalmonisnowproducedandmarketedinlargenumbers aroundtheworld.Unlessyoulookcarefullyattheproductlabel,orspecifyyour order exactly, you can be sure that the salmon on your plate will be Atlantic salmon from aquaculture. Atlantic salmon is also the basis for what some view as a host of negative consequences of aquaculture. Salmon can escape from floating cages, wastes from the fish or excess food can create water quality concerns, and the large-scale aquacultureproductionofsalmoncanhaveconsequencesasfar–reachingasthe harvestormarketingofwildspecies,landusepolicies,andfisheriesmanagement policies. Concerns about Atlantic salmon aquaculture are visible on t-shirts and bumper stickers in the Pacific Northwest, at least. Those are even more striking whenviewedincontrasttothet-shirtsandbumperstickerspromotingconservation andconsumptionof“theother”salmonspecies. Howcanwehaveasituationwiththestrangeparadoxofafishspeciesthatis nearing extinction while it is at the same time probably the most abundant fish speciesavailableinthemarketplace?Whatcanwedotoresolvetheconflictsover thissingle,magnificentfishspecies? Thebrowntrouthasalwaysbeenviewedasmoresecretive,perhapssomemight saylessnoblethantheconspecificAtlanticsalmon.Ithasneverreachedthesame levelofaquacultureproductionasAtlanticsalmonandsoithasnotsharedeitherthe marketorthecriticisms.ThenativerangeofbrowntroutwasrestrictedtoEuropean waters,incontrasttothedistributionofAtlanticsalmoninbothEuropeanandNorth American waters of the Atlantic Ocean. The typical anadromous nature of Atlantic salmon, in contrast to the more usual freshwater nature of brown trout, certainly was viewed as correlated with the differences in their native distributions. The brown trouthasbeenseenasaspeciesbettersuitedtostockinginfreshwaters,tosupport trophy fisheries well beyond their native range. It has established self-sustaining populations in many locations, and continues to maintain a reputation as a desirable fish for anglers. In fact evidence suggests that the brown trout has been more successful at establishing populations after stocking than has the more widely distributedAtlanticsalmon.Howcanthatbe? The answers to all the questions and concerns about both these species of course, areinformation,knowledge,andcommunication.Allthreeareinabundanceinthis volume.NinaandBrorJonssonhavedevotedtheirscientificcareerstothestudyof thesespecies.Inthisvolumetheybringtogetheranincrediblerangeofinformation, from molecular genetics to landscape ecology and phylogenetics. This will be the standard reference for anyone concerned with any aspect of the biology of these species. Prospective researchers will find a wealth of information and potential projects.Fisheriesmanagers,historians,economists,andenvironmentalistswillall findsomethingofvalue. Thesefisheshavechangedourlivesassubjectsofharvestandobjectsofstudy. Wecontinuetochangetheirlives,throughexploitation,aquaculture,andlandscape alterations.Asnativespeciestheyhavebeenemblematicofthekindsofenvironments
Foreword
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theysharedwithus.Theirhistoriesandfatesareevermoreentangledwithoursand wehavetheresponsibilitytousetheinformationandknowledgefromthisvolumeto communicatewiththosewhoneedtoknowabouttheseremarkablespecies.
Dr.DavidL.G.Noakes Editor, Springer Fish and Fisheries Series Professor of Fisheries and Wildlife SeniorScientist,OregonHatcheryResearchCenter OregonStateUniversity Corvallis,Oregon,USA
Preface
TheAtlantictrouts,Atlanticsalmonandbrowntrout,areattractivefishspecieswith complex life cycles and ecologies heavily influenced by their environments. Characterssuchasageandsizeatmaturity,tendencytomigrateandlongevityare all affected by the habitats they exploit. The species gain much human interest because of their quality as sporting species, their eminence as delicacies of the table and suitability for aquaculture and farming. These attributes are chief reasons for whytheyareamongthebest-studiedfishesintheworld. Atlantic trouts are oxygen-demanding, and because of that, they typically use cold,nutrient-poorhabitats.Keepingsuchhabitatsintactgivespositivefeedbackto societybyprovidingfood,ecosystemservicesandimprovingthequalityofpeople’s life.Buthumanactivities,suchaslandscapealteration,exploitation,externalinputs andresourcecompetition,areoftendeleterioustohabitatsandstocks.Theirmigratory behaviourandspawninginrunningwatermakethesesalmonidseasilyexploited, highlyresponsivetohydropowerregulations,andhumanencroachmentsinrivers. Furthermore,theirdependenceofcoldwatermakesthemsusceptibletotheongoing global warming. Throughsalmonidresearchduringthelast40years,wehavestudiedassociations between habitat and phenotypes of the Atlantic trouts. Our studies have clearly revealedthatapartofthevariationisduetophenotypicplasticity,andapartresults fromlocaladaptation.Ourchiefideaspresentedarethat:(1)habitatisatemplate for ecological variation of the species, (2) growth has pervasive effects on most other life history variables such as smolt age and size, age and size at maturity, mortalityandlongevityandmigration,and(3)earlyexperiencesinfluenceanumber ofsubsequentchoicesaffectingthefitnessofthefish.Examplesgiventhroughout thebookillustratetheseideas. TheecologicalvariabilityexhibitedbytheAtlantictroutsmakesthemparticularly interesting. Their appearances vary among localities and life stages; they exploitfreshandsaltwaters,andadapttofeedinrivers,lakes,estuariesandocean. Populations can be resident and stay in one restricted area throughout life, or migratethousandsofkilometresforfeedingintheocean,beforereturningtotheir homestreamforspawning.Manypopulationsarealsoenvironmentallysplitbetween residentandmigratoryindividuals.Onthespawninggrounds,adultmalescanweigh only a few grams but still compete for spawning opportunities with conspecifics xiii
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Preface
weighingmorethan10kg.Thereareinterestingquestionshowsuchlargevariability can persist within the same demes. Asscientists,wehavefieldexperiencefromwatercoursesinthevariousparts of Norway. We have also investigated salmonid ecology in Iceland and Canada. MostofourexperimentalworkisperformedattheNINAResearchStation,Ims, located in Sandnes, southwestern Norway. There, the staff has provided data on migratory behaviour of Atlantic salmon and brown trout every day since 1975. They have also raised the hatchery fish used in our experiments. We have also profitedfromcollaboratingwithanumberofcolleaguesattheNorwegianInstitute forNatureResearchinOsloandTrondheim,theDirectorateforNatureManagement in Trondheim and also from students and staff at the University of Oslo and the TechnologicalUniversityofNorwayinTrondheim.Wearethankfulforthat. Our own research performed in cooperation with colleagues in Norway and other countries has been the foundation of the results presented in the book. We haveplacedthisscienceincontextwiththatofothersonthesameorsimilarissues. Thetextismademorecomprehensivebytheadditionofinformationfromrelated species.Wehavenotcataloguedthevastliteratureonlifehistoryvariationofthese species,buthavefocusedonthemorerecentadvances.Ourknowledgeaboutphysiologyisincomplete,andwherephysiologicalaspectshavebeendiscussed,suchas onsmoltingandmaturation,wehaveconcentratedonwhatweviewtobethemajor mechanisms. However, key references are given that will allow anyone, who wishes,toinvestigatedeeperintotheprimaryliteratureoftheunderlyingscience. Knowledgeexchangeisofparamountimportanceinincreasingtheunderstanding of ecological phenomena such as interrelationships between habitats and organisms, comprehension that helps in proper habitat management. It is our hope that this bookwillcontributetothat:inspireandencourageecologiststocontinuedsalmonid research.TargetreadersaremasterandPhDstudentsinfishecology,fisherymanagers, fellow researchers and interested naturalists, but also sport fishers and fish breederswhohavegainedaseriousinterestinthenaturalhistoryoftheirresource. WewishtothanktheSeriesEditor,DavidL.G.Noakes,forcriticallyreadingand commentingonthemanuscript,RichardvanFrankforimprovingthelanguage,and Bengt Finstad, Mart R. Gross, Finn R. Gravem, Tormod A. Schei, Ole Kr. Berg, Trygve Hesthagen, Jan Heggenes, Harald Sægrov, Malcolm Elliott, Tor A Mo, TrygveT.Poppeandothercopyrightholdersforallowingustoreusefigures. Oslo,July2010
BrorJonsson NinaJonsson
Contents
1
Habitats as Template for Life Histories ................................................ 1.1 Introduction ...................................................................................... 1.2 AtlanticSalmonandBrownTrout.................................................... 1.3 LifeHistoryCharacters .................................................................... 1.3.1 CharactersAssociatedwithBreeding ................................... 1.3.2 AlevinsandParr.................................................................... 1.3.3 Smolts,Post-smoltsandAdults ............................................ 1.4 AdaptiveVariation ............................................................................ 1.5 Ideas,Purpose,andRelevanceoftheBook ..................................... 1.6 OrganizationoftheBook ................................................................. 1.7 Summary .......................................................................................... References .................................................................................................
1 1 2 3 3 6 9 10 12 15 18 19
2
Species Diversity...................................................................................... 2.1 OrganizationoftheChapter ............................................................. 2.2 TaxonomicDiversity ........................................................................ 2.2.1 SalmonidEvolution .............................................................. 2.2.2 Salmonidae ........................................................................... 2.2.3 Salmoninae ........................................................................... 2.2.4 Salmo .................................................................................... 2.3 TheSpecies....................................................................................... 2.3.1 AtlanticSalmon .................................................................... 2.3.2 BrownTrout .......................................................................... 2.4 GeographicalDistributions............................................................... 2.4.1 AtlanticSalmon .................................................................... 2.4.2 BrownTrout .......................................................................... 2.4.3 HabitatConstraints ............................................................... 2.5 Summary .......................................................................................... References .................................................................................................
23 23 28 28 32 34 34 40 40 43 45 45 50 54 55 56
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3
Habitat Use .............................................................................................. 3.1 OrganizationoftheChapter ............................................................. 3.2 RiversandStreams ........................................................................... 3.2.1 SizeandAgeStructuredHabitatUse ................................... 3.2.2 TerritorialityandHabitatComplexity................................... 3.2.3 FoodandFeeding.................................................................. 3.2.4 SeasonalChanges ................................................................. 3.2.5 MoversandResidents ........................................................... 3.2.6 InterspecificCompetitioninRunningWater ........................ 3.3 LakeUse ........................................................................................... 3.3.1 SpatialDistribution ............................................................... 3.3.2 PartialHabitatSegregation ................................................... 3.3.3 LakeFeeding ........................................................................ 3.3.4 InterspecificCompetitioninLakes ....................................... 3.4 Estuaries ........................................................................................... 3.4.1 HabitatUse ........................................................................... 3.4.2 Feeding ................................................................................. 3.5 Ocean ................................................................................................ 3.5.1 HabitatUse ........................................................................... 3.5.2 Feeding ................................................................................. 3.6 Summary .......................................................................................... References .................................................................................................
67 67 70 71 79 80 84 88 91 95 96 101 105 109 111 111 112 114 114 116 118 119
4
Development and Growth....................................................................... 4.1 OrganizationoftheChapter ............................................................. 4.2 ThermalHabitat................................................................................ 4.2.1 ThermalLimits ..................................................................... 4.2.2 IntraspecificandInterspecificVariation in Thermal Tolerance ............................................................ 4.3 EmbryonicDevelopment .................................................................. 4.3.1 AbioticEffectsonEarlyDevelopment ................................. 4.3.2 RateofDevelopment ............................................................ 4.3.3 EmbryoSize.......................................................................... 4.4 GrowthandSizeofJuvenilesandAdults......................................... 4.4.1 Growth,Size,andHabitatUse.............................................. 4.4.2 PhenotypicallyPlasticorGenetically Determined Body Size .......................................................... 4.4.3 Energy,MassorLength ........................................................ 4.4.4 AgeandGrowth .................................................................... 4.5 EffectsofTemperature ..................................................................... 4.5.1 LaboratoryBasedGrowthModels ........................................ 4.5.2 MaximumGrowth................................................................. 4.5.3 AdaptiontoLocalTemperature ............................................ 4.5.4 OtherApplicationsofThermalPerformanceModels ..........
137 137 138 138 140 141 142 144 149 150 150 152 154 158 163 166 168 169 172
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4.6 OtherFactorsInluencingGrowthandSize ..................................... 4.6.1 MaximumFoodConsumption ............................................ 4.6.2 GrossGrowthEfficiency .................................................... 4.6.3 RationSize.......................................................................... 4.6.4 FoodParticleSize ............................................................... 4.6.5 SizeDependence ................................................................ 4.6.6 BodySizeandTemperature................................................ 4.6.7 BimodalityinSize .............................................................. 4.6.8 SeasonalVariationinSize .................................................. 4.6.9 CompensatoryGrowth ........................................................ 4.6.10 Density-Dependence........................................................... 4.6.11 Stunting............................................................................... 4.6.12 OntogeneticNicheShiftsandGrowth ................................ 4.6.13 InterspecificCompetitionandPredatorPresence ............... 4.7 Summary .......................................................................................... References .................................................................................................
173 173 173 175 176 176 179 179 181 182 185 190 191 191 193 194
5
Smolts and Smolting ............................................................................... 5.1 OrganizationoftheChapter ............................................................. 5.2 MorphologicalandPhysiologicalChangesDuringSmolting .......... 5.2.1 ColourandMorphology ..................................................... 5.2.2 Physiology .......................................................................... 5.2.3 ControllingFactors ............................................................. 5.3 BehaviouralChange ......................................................................... 5.3.1 GatheringinSchools .......................................................... 5.3.2 DownstreamMovement...................................................... 5.3.3 Time of Day ........................................................................ 5.3.4 SeawaterPreference ........................................................... 5.4 EcologicalCharacters ....................................................................... 5.4.1 SmoltAge ........................................................................... 5.4.2 SizeandGrowth ................................................................. 5.4.3 HabitatConstraints ............................................................. 5.4.4 SexRatio............................................................................. 5.4.5 SmoltingVersusSexualMaturation ................................... 5.5 IsSmolt-AgeInherited? ................................................................... 5.6 Summary .......................................................................................... References .................................................................................................
211 211 213 213 214 218 221 222 222 223 223 225 225 228 231 233 233 236 237 238
6
Migrations................................................................................................ 6.1 OrganizationoftheChapter ............................................................. 6.2 Migration .......................................................................................... 6.2.1 HabitatSelection ................................................................ 6.2.2 WhenMigrate? ................................................................... 6.2.3 WhichFishMigrate? .......................................................... 6.2.4 VerticalMigrations .............................................................
247 247 249 249 254 255 255
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6.3 Horizontal Migrations ...................................................................... 6.3.1 PotamodromousMigrations.................................................. 6.3.2 AnadromousMigrations ....................................................... 6.4 EffectsofWaterTemperatureandFlow ........................................... 6.4.1 DownstreamMigration ......................................................... 6.4.2 UpstreamMigration .............................................................. 6.5 Homing ............................................................................................. 6.5.1 NavigationBacktoTheirHomeStream............................... 6.5.2 HomingHypotheses.............................................................. 6.5.3 Homing Precision ................................................................. 6.6 Partial Migration............................................................................... 6.6.1 DifferencesBetweenSexes................................................... 6.6.2 EnvironmentVersusGenetics? ............................................. 6.6.3 HowIsPartialMigrationControlled?................................... 6.7 Summary .......................................................................................... References .................................................................................................
256 256 258 272 272 273 286 287 288 294 301 302 303 305 306 308
Maturation and Spawning ..................................................................... 7.1 OrganizationoftheChapter ............................................................. 7.2 Reproduction .................................................................................... 7.2.1 InitiationofMaturation......................................................... 7.2.2 AgeandSizeatMaturity ...................................................... 7.2.3 PhenotypicPlasticity ............................................................ 7.2.4 Thorpe’sMaturationModel .................................................. 7.2.5 ReactionNorms .................................................................... 7.2.6 MaximizationofFitness ....................................................... 7.2.7 SexualDifference.................................................................. 7.3 Adult Morphs ................................................................................... 7.3.1 ParrMaturity ......................................................................... 7.3.2 Post-smoltMaturity .............................................................. 7.3.3 RepeatSpawners ................................................................... 7.4 SecondarySexualCharacters ........................................................... 7.4.1 BreedingColours .................................................................. 7.4.2 Morphology .......................................................................... 7.4.3 AdiposeFin ........................................................................... 7.4.4 SexualDimorphism .............................................................. 7.4.5 MateChoices ........................................................................ 7.5 Primary Sexual Characters ............................................................... 7.5.1 Spermatozoa ......................................................................... 7.5.2 FecundityandEggSize ........................................................ 7.6 ReproductiveInvestment .................................................................. 7.6.1 ResourcePartitioning............................................................ 7.6.2 GonadalInvestment .............................................................. 7.6.3 Total Energy Costs ................................................................
327 327 329 329 334 341 342 343 346 347 349 350 353 353 357 357 358 359 360 361 364 364 365 373 374 374 379
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7.7 Spawning .......................................................................................... 7.7.1 SpawningHabitat.................................................................. 7.7.2 TheSpawningTime .............................................................. 7.7.3 SpawningBehaviour ............................................................. 7.7.4 ReproductiveSuccess ........................................................... 7.8 Summary .......................................................................................... References .................................................................................................
383 383 388 389 393 396 397
Recruitment, Mortality and Longevity ................................................. 8.1 OrganizationoftheChapter ............................................................. 8.2 DensityRegulation ........................................................................... 8.2.1 DensityDependence ............................................................. 8.2.2 CarryingCapacity ................................................................. 8.2.3 Bottlenecks ........................................................................... 8.2.4 Stock-RecruitmentModels ................................................... 8.2.5 Density-IndependentMortality ............................................. 8.3 FactorsConstrainingRecruitment .................................................... 8.3.1 ReproductiveOutput ............................................................. 8.3.2 SpawningOpportunitiesandDensityofSpawners .............. 8.3.3 NestDistribution ................................................................... 8.4 FactorsInluencingDensity.............................................................. 8.4.1 WinterConditions ................................................................. 8.4.2 HighWaterFlow ................................................................... 8.4.3 Drought ................................................................................. 8.4.4 PredationandPathogens ....................................................... 8.4.5 FishingMortality .................................................................. 8.5 CriticalPeriods ................................................................................. 8.5.1 EarlyMortality...................................................................... 8.5.2 MarineMortality ................................................................... 8.6 Density-DependentMechanisms...................................................... 8.6.1 SpatialRelationships ............................................................ 8.6.2 Self-Thinning ........................................................................ 8.6.3 MortalityandGrowth ........................................................... 8.6.4 InterspecificCompetition ..................................................... 8.7 MortalityandLongevity ................................................................... 8.7.1 Heritability ............................................................................ 8.7.2 EffectofTemperature ........................................................... 8.7.3 EffectofSize ........................................................................ 8.7.4 EffectofGrowth ................................................................... 8.7.5 Longevity,MaturationandSpawning ................................... 8.8 Summary .......................................................................................... References .................................................................................................
415 415 418 418 419 421 421 423 423 424 424 425 427 427 428 428 429 434 437 437 440 447 447 448 450 451 452 452 453 455 455 456 457 459
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Contents
9
Climatic Effects on Atlantic Salmon and Brown Trout ....................... 9.1 OrganizationoftheChapter ........................................................... 9.2 Climate ........................................................................................... 9.3 Trends in Abundance ..................................................................... 9.3.1 AtlanticSalmon................................................................ 9.3.2 BrownTrout ..................................................................... 9.4 Life-HistoryEffectofClimateChange.......................................... 9.4.1 ParrGrowth ...................................................................... 9.4.2 Post-smoltGrowth............................................................ 9.4.3 SmoltAgeandSize .......................................................... 9.4.4 PartialMigration .............................................................. 9.4.5 AgeatMaturity ................................................................ 9.4.6 SizeatMaturity ................................................................ 9.4.7 EnergyUseoftheSpawners ............................................ 9.4.8 EggandEmbryoSize ....................................................... 9.4.9 SpawningTimeandAlevinEmergence ........................... 9.4.10 Recruitment ...................................................................... 9.4.11 Production ........................................................................ 9.5 Time of Migration .......................................................................... 9.5.1 SmoltMigration ............................................................... 9.5.2 SpawningMigration ......................................................... 9.6 GeographicalDistributionsMoveNorthwards .............................. 9.7 Mortality Causes ............................................................................ 9.7.1 Diseases ............................................................................ 9.7.2 HostileWinterClimateinFreshWater ............................ 9.7.3 Drought ............................................................................ 9.7.4 MarineClimate................................................................. 9.8 Summary ........................................................................................ References .................................................................................................
473 473 474 475 476 479 480 480 483 485 486 488 488 489 490 490 491 492 493 493 497 498 500 500 502 502 503 504 505
10
Farmed Atlantic Salmon in Nature ....................................................... 10.1 OrganizationoftheChapter ........................................................... 10.2 EscapedSalmoninNature ............................................................. 10.2.1 HowMuchEscapedAtlanticSalmonIsThere? .............. 10.2.2 SeaSurvival...................................................................... 10.2.3 DispersalandHoming ...................................................... 10.2.4 SpawningCompetitionandReproductiveSuccess .......... 10.2.5 OffspringSurvival ............................................................ 10.2.6 GeneFlow ........................................................................ 10.2.7 OtherLong-TermEffects ................................................. 10.3 HatcheryInducedChanges ............................................................ 10.3.1 Morphology,AnatomyandPhysiology ........................... 10.3.2 Life-HistoryCharacters.................................................... 10.3.3 SelectionforProductionTraits ........................................ 10.3.4 GeneticallyModifiedSalmon(GMS) ..............................
517 517 518 519 521 522 525 530 533 536 537 538 542 543 545
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10.4 SpreadingofParasitesandDiseases .............................................. 10.4.1 Transportation .................................................................. 10.4.2 HorizontalTransmission .................................................. 10.4.3 VerticalTransmission ....................................................... 10.4.4 AlternationofHosts ......................................................... 10.5 MeasurestoReduceNegativeImpacts .......................................... 10.6 Summary ........................................................................................ References .................................................................................................
547 548 550 551 551 552 554 555
Population Enhancement and Population Restoration ....................... 11.1 OrganizationoftheChapter ........................................................... 11.2 PopulationRestorationandEnhancement ..................................... 11.2.1 SupportiveBreeding ......................................................... 11.2.2 WhyAreFishReleased? .................................................. 11.3 SalmonStocking ............................................................................ 11.3.1 EggPlanting ..................................................................... 11.3.2 JuvenileFishStocking ..................................................... 11.3.3 StrayingofHatcheryFish ................................................ 11.4 ChangesOccurringinHatcheries .................................................. 11.4.1 HatcheryExperiencesInfluenceBehaviour in the Wild ........................................................................ 11.4.2 DevelopmentalProcesses ................................................. 11.4.3 PhysicalDamages ............................................................ 11.4.4 GeneticChanges............................................................... 11.5 EcologicalInteractionsbetweenHatcheryandWildFish ............. 11.5.1 JuvenileCompetition ....................................................... 11.5.2 DisplacementandMortalityinFreshwater ...................... 11.5.3 Growth.............................................................................. 11.5.4 OtherLifeHistoryTraits .................................................. 11.5.5 BiomassandProduction................................................... 11.6 HabitatRestorationsandImprovements ........................................ 11.6.1 Weirs................................................................................. 11.6.2 Fishways ........................................................................... 11.6.3 SpawningHabitatImprovements ..................................... 11.6.4 JuvenileHabitatImprovements ........................................ 11.6.5 AcidityStressandLiming................................................ 11.6.6 WaterLevelandFlowRegulation .................................... 11.7 SalmonManagement ..................................................................... 11.7.1 Fishing .............................................................................. 11.7.2 PopulationorHabitatRestoration? .................................. 11.7.3 AdaptiveManagement ..................................................... 11.8 Summary ........................................................................................ References .................................................................................................
567 567 569 569 570 571 571 573 581 583 585 588 589 589 592 593 593 596 596 596 597 598 599 601 602 604 605 606 606 608 610 613 614
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General Conclusions and Research Tasks ............................................ 12.1 Introduction .................................................................................... 12.2 HabitatasEcologicalTemplate ..................................................... 12.2.1 EnvironmentalInfluence .................................................. 12.2.2 InheritedVariation............................................................ 12.3 FutureResearchTasks ................................................................... 12.3.1 SystematicsandPhylogeography ..................................... 12.3.2 HabitatUse ....................................................................... 12.3.3 Growth,Competition........................................................ 12.3.4 SmoltingandMigration ................................................... 12.3.5 SexualMaturation ............................................................ 12.3.6 PopulationRegulationandManagement ......................... 12.3.7 InteractionsBetweenWildandFarmedSalmon .............. 12.4 Summary ........................................................................................ References .................................................................................................
633 633 634 634 636 639 640 641 642 643 644 645 646 648 649
Glossary ........................................................................................................... 657 Species Index ................................................................................................... 677 Author Index.................................................................................................... 681 Subject Index ................................................................................................... 701
Chapter 1
Habitats as Template for Life Histories
1.1 Introduction Habitat is a template, which influences life histories, behaviour and physiology of organisms, and is the origin of intraspecific variation (Southwood 1977, 1988; Poff and Ward 1990). This is a useful concept for considering relationships underlying demographic patterns observed in fish populations. As habitats differ geographically and temporally, life histories of conspecific populations also vary in space and time. This is not the least due to biogeoclimatic processes that influence disturbance patterns, frequencies, magnitudes and predictability of habitats. Population responses of fish populations can be phenotypically plastic, but long-term differences also cause adaptive variation due to selection. Atlantic salmon and brown trout exhibit variable life histories (Jonsson 1989; Thorpe et al. 1998), and a growing body of literature has focused on habitat effects on their population-specific characters (Jonsson et al. 1991; Gibson 1993; Elliott et al. 1998; Jonsson and Jonsson 2006a). Such studies reveal that environmental factors are drivers of growth and demographic traits. Abiotic factors, such as water temperature, flow and depth, bottom substrate, ice cover, barriers to migration, nutrient richness, habitat coherence and consistency can all influence life history traits. But also biotic factors and processes contribute to the habitat template and thus function as population regulators in stream salmonids. For instance, there are both positive and negative relationships between population density and mortality due to intracohort, intercohort, and interspecific competition. Inadequate space influences territory size, competition intensity, growth and body size of fish (Horton et al. 2009). Nutrient richness influences primary and secondary production of aquatic systems, thereby contributing to competition keenness, growth rate, fish size and production of populations. Individual growth and size are major determinants of reproductive success and recruitment, and hence, the size of subsequent cohorts. Thus, the habitat is a template for the ecology of the species, including mode of migration and reproductive behaviour, and associations between habitat and life history variation of Atlantic salmon (Salmo salar L.) and brown trout (Salmo trutta L.).
B. Jonsson and N. Jonsson, Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories, Fish & Fisheries Series 33, DOI 10.1007/978-94-007-1189-1_1, © Springer Science+Business Media B.V. 2011
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In this chapter, we present a short introduction to the life histories of the species and how they vary among environments. Then, we give the chief purpose and the organization of the content of the book.
1.2 Atlantic Salmon and Brown Trout Atlantic salmon and brown trout are known for their strong, streamlined bodies, ability to move through steep rivers and their performance of long migrations in fresh and salt waters, with precise homing to the site where they were born. The species have complex life histories, which exhibit interesting phenotypic plasticity and genetic adaptations. Atlantic salmon and brown trout are sibling species. Their morphologies are so similar, and population and individual variability so large that specialized expertise is often needed for correct species identification. But closer investigations of the individuals reveal many phenotypic differences. Atlantic salmon have smaller head relative to body, broader pectoral fins, thinner and longer caudal peduncle and a more forked caudal fin than brown trout. These differences reveal that Atlantic salmon are better adapted to life in strong water current in rivers and to complete long migrations in the ocean. Numerous adaptations are also reflected by differences in their ecology, e.g. brown trout exhibit stronger affinity to lentic habitats, grow more slowly at sea and have a greater propensity for freshwater residency than Atlantic salmon. Their genus name, Salmo, comes from Latin and means salmon. Possibly, the word originates from salir, which means ‘to leap’. The species name of Atlantic salmon, salar, means leaper. This name was probably given because of their ability of leap up high waterfalls. Those who have witnessed these fish jump up 3 m high waterfalls, on their return migration to the spawning grounds, can easily imagine the origin of the species name. The species name of brown trout, trutta, originates from late Latin, tructa, probably developed from Greek, trōgein, which means gnaw (Andrews 1955). We do not see why this name was chosen, but have found no better explanation for the origin of the name. Most populations of Atlantic salmon are anadromous. Anadromous means that they spawn in freshwater but obtain most of their food during their feeding excursions in marine habitats. But freshwater resident populations are known from a number of localities in Europe, such as the Lake Byglandsfjord, Norway; Lake Vänern, Sweden; Lake Saimaa, Finland; Lake Ladoga, Onega and Kuito, Russia and more lakes in North America. They are popularly called Ouananiche in Lake St. John and Sebago salmon in Nova Scotia, Quebec, New Brunswick, Newfoundland and the New England States of USA. These fish spend their entire life in freshwater. When large, they typically use lakes in the watershed as feeding areas. The populations in Europe were probably formed about 10,000 years ago (Berg 1985). This was a period with very low ocean temperatures, probably diminishing the growth advantage of the sea migration. In rare cases, there are landlocked populations
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dwelling in a river with no major lakes such as the upper part of the River Namsen, Norway. In this river, there is also anadromous Atlantic salmon similar to the River Magaguadavic, New Brunswick, Canada. Brown trout exploit brooks, rivers, lakes, estuaries and coastal sea and migrate among these habitats. They are found in mountainous as well as lowland areas. The lake-feeding forms are often potamodromous, migrating into tributaries or the outlet for spawning. Like Atlantic salmon, brown trout form anadromous populations. But unlike Atlantic salmon, the anadromous brown trout feed chiefly in estuaries and along coasts. Only large individuals are sometimes observed in the open ocean (Jonsson and Jonsson 2006b). Freshwater resident brown trout can be stationary or perform migrations in freshwater between spawning, nursery and feeding areas depending on local conditions. By exploiting such diverse localities, they exhibit one of the most diverse life histories among fish in the world (Jonsson 1989). Brown trout is an invasive species and among the most adaptive fish in northern waters. They easily colonize new areas and profoundly affect the functioning of stream communities, reducing the abundance of invertebrates and altering their grazing behaviour, so that algal biomass increases. Brown trout have been responsible for evolution among invertebrates of novel antipredator behaviours with far-reaching community consequences (Townsend 1996).
1.3 Life History Characters Life histories of organisms are descriptions of their life cycle including reproductive ecology and population traits important for their breeding success. Salmonid life histories can vary temporally and spatially because they evolve, and there is co-evolution of traits such as growth pattern, age-specific survivorship probability, age at first reproduction, fecundity and egg size and reproductive frequency. For instance, in anadromous populations, there are conflicts between parr maturity and smolting. Both these life history decisions depend on previous growth and the accumulation of energy stores. Thus, factors affecting growth opportunities can also affect life history outcomes. But it is also obvious that populations have evolved different genetic threshold responses to local environmental factors, i.e. optimal choices in one river may not maximize fitness in another. In this book, we discuss direct environmental influences on life history traits, associations between traits, and intraspecific and interspecific adaptations in Atlantic salmon and brown trout.
1.3.1
Characters Associated with Breeding
Atlantic salmon and brown trout spawn in freshwater in autumn or winter, and thereby, they differ from most other freshwater fish, which are spring or summer spawners. They prefer to spawn in swift-flowing rivers and streams. Compared with
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brown trout, Atlantic salmon spawn deeper and in faster-flowing water, but the preferred depths and flows are also influenced by the channel morphology. If no preferred site is found, they can spawn along exposed lake shores or in littoral areas with upwelling ground water, and brown trout may even spawn in brackish water (Fleming 1996; Limburg et al. 2001). The incubating embryos and alevins require high water flow through the substratum to provide enough dissolved oxygen and to carry away metabolic wastes. High levels of fine sediments in the substratum reduce embryo survival and may also damage the embryos by abrasion and prevent the alevins from emerging from the nests. When living sympatrically, brown trout often spawn earlier in the autumn than Atlantic salmon. The fertilized eggs are embedded in the bottom substratum and hatch in spring. The alevins dwell for the first several weeks in the bottom substratum, feeding on yolk, which they carry in a sac below their bellies (Fig. 1.1). Therefore, they are sometimes called yolk-sac larvae. When most of the yolk is consumed, the alevins emerge from within the substratum and commence external feeding on small invertebrates, which they find in the water and upon the substrate. Atlantic salmon and brown trout exhibit strong homing behaviour to natal areas for spawning (Harden Jones 1968). Many rivers used for spawning are short, but anadromous Atlantic salmon can, in extreme cases such as in the Loire, France, move nearly 900 km inland to breed in the upper Allier, and in the Pechora River northern Russia, it may even migrate twice this distance (Studenov et al. 2008). Both these populations are in a declining state. Anadromous brown trout do not exhibit such extremely long spawning migrations in rivers, and in Scandinavia, they usually spawn below 150 m above sea level (Bohlin et al. 2001).
Fig. 1.1 Atlantic salmon alevins feed on yolk they carry in a sac beneath their belly
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Fig. 1.2 Nest pit of anadromous brown trout. The large stones in the centre are approximately 10 cm in diameter
On the spawning grounds, the females excavate the nests (Fig. 1.2). They perform a forward acceleration, turning on one of their sides, and beat the gravel with rapid flexures of the body and tail. By this behaviour, females make depressions in the bottom substratum, where their eggs are deposited. During digging, the females do not show much aggressiveness, except when they defend their redd location from other females, which approach closer than a couple of meters from their nest pit. Dominance is often associated with prior residence, but in some cases, territory holders are chased away. If so, the intruder will test the territory and select her own spawning site, independent of where the old redd was located. The intruder does not take over the nest of the former territory holder. After having deposited a portion of their eggs, females cover the eggs by digging in front of the nest. After the eggs are spawned and covered, the females leave the breeding ground and display no more parental care, unlike the Pacific salmon, where the females protect their nesting location until they eventually die.
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Fig. 1.3 Spawning pair of anadromous brown trout. The male, with hooked under jaw, is to the left (Photo credit: Anders Lamberg)
Males fight each other for dominance and access to nesting females. They combine chases and bites with threat displays to intimidate rivals. During spawning, the dominant male occupies the position closest to the female (Fig. 1.3) and divides his time between courting and preventing other males from approaching her. When spawning, the female sinks down into her nest pit and the eggs are spawned in a cloud of milt from the dominant male, but subordinate males can also contribute to the fertilization. Those can be other large males, but small parr males can also be sexually mature and spawn.
1.3.2
Alevins and Parr
The embryos develop during the winter and the alevins hatch in the subsequent spring. Incubation time depends chiefly on the water temperature, but environmental stress, e.g. mechanical disturbances or low oxygen levels, can induce early hatching of the alevins. The alevins emerge from the gravel substratum approximately 1 month or so after hatching. The duration of the alevin period increases with decreasing water temperature. The alevins emerge when the yolk is almost consumed, and the young are pigmented and ready for external feeding. A large part of the natural mortality occurs during the first summer from the alevin to the early parr stage. First external feeding is difficult. This is probably
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because the alevins need food items of the correct size at the right time to start exogenous feeding. Parr of Atlantic salmon and brown trout are easily recognized by the dark vertical bars along their flanks (parr marks) (Figs. 1.4a and 1.5a). They are present in both still and running waters and feed on epibenthic and drifting arthropods, such as insect larvae. Other food items are small molluscs and crustaceans. Brown trout parr, more than Atlantic salmon parr, live in lentic habitats; if a lake is accessible, many move there for feeding from their first summer onwards.
Fig. 1.4 Brown trout (a) parr and (b) smolt
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Fig. 1.5 Atlantic salmon (a) parr and (b) smolt
In anadromous populations of both species, some male parr attain sexual maturity, and in brown trout, female parr also mature regularly. In this latter species, such early maturing fish usually become freshwater residents and remain in freshwater during their entire lifespan. These populations are denoted partly migratory. In Atlantic salmon, mature male parr often smolt after having reproduced, and they move to the sea in the subsequent spring. Older freshwater-dwelling brown trout can continue feeding chiefly on insect larvae in the nursery river, but if there are lakes in the watershed, many will move there. In the lake, they feed on epizoobenthos, zooplankton and surface arthropods.
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Large individuals feed predominantly on fish but can also take amphibians and small mammals such as lemmings or other small rodents swimming in water. The food preference varies with size and growth rate of the fish.
1.3.3
Smolts, Post-smolts and Adults
In anadromous populations, the parr transform to smolts at a body length of approximately 15 cm in brown trout (Fig. 1.4b) and Atlantic salmon (Fig. 1.5b). The smolts usually migrate to sea in spring. They have silvery sides, and the belly and pelvic fins are white. Their colouration gives daytime camouflage in the pelagic zone. The smolts move downstream with the water current into estuaries and coastal waters and Atlantic salmon move farther out into the open ocean. Post-smolts of Atlantic salmon feed in the North Atlantic. They can migrate more than 2,000 km in the open ocean away from their home river in the North Atlantic. Many feed north of the Faroe Islands in the Norwegian Sea, off the coast of Greenland and some can move as far north as 80°N to Svalbard. Atlantic salmon seldom return to freshwater for spawning in the year they move to sea. Sea water tends to inhibit early maturation (Lundqvist and Fridberg 1982). They grow at sea for 1–4 years before attaining maturity and returning to their home river for spawning. Typically, Atlantic salmon spawn the year they return to freshwater, but sometimes they return as juveniles, a year prior to sexual maturation and spawning. Such early-returning fish may spawn far upstream in long rivers or enter rivers with difficult migratory conditions where they have to avoid periods of drought or high temperature in the lower part of the water course. Smolts of brown trout are usually somewhat larger than those of Atlantic salmon in the same or nearby rivers with similar environmental conditions. This may be related to their poorer ability to regulate their ionic content in sea water (Hoar 1976). Anadromous brown trout feed chiefly in estuaries and coastal waters and migrate seldom out into the open sea. Most of them feed within 100 km of the river mouth. Migratory duration, however, varies among populations and tagged fish have crossed the North Sea from France to Scandinavia, and as long as from Oslo to north Finnmark in Norway, a migratory distances of approximately 2,000 km (Jonsson et al. 1994; Jonsson and Jonsson 2006b). Contrary to Atlantic salmon, anadromous brown trout often return to their home river the same year as they move to sea for spawning or as immature fish for wintering (Jonsson and Jonsson 2009). Thus, the salt water sojourn does not influence their tendency to attain maturity; a useful adaptation since brown trout typically feed in estuaries not very far from the river mouth. Both Atlantic salmon and brown trout are iteroparous, meaning that many survive reproduction and can spawn again, unlike Pacific salmon, but similar to Pacific trouts (Scott and Crossman 1973). Anadromous brown trout typically spawn every year after attaining maturity whereas large Atlantic salmon typically wait 2 years before spawning again. Few individuals spawn more than three times or live longer than 10 years.
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1.4 Adaptive Variation For hundreds of years, people have noticed that the size and body form of Atlantic salmon vary among water courses and the same holds true for brown trout. Research indicates that this, at least partly, is because natural selection over generations adapts the populations to the prevailing environmental and competitive conditions in the water courses. Such adaptations influence survival and reproductive success in the respective water courses. Although all conspecific individuals are similar, they are also different because they can carry different variants (alleles) of the same genes. Populations differ genetically because they were founded by genetically different individuals (founder effect) and because natural selection has acted differently upon them due to environmental differences. Also, the genetic diversity of populations changes with time due to different genetic mechanisms such as mutations and drift. Mutations (alterations in the DNA sequence of a cell’s genome) change the product or function of genes. Genetic drift can occur when populations are founded by individuals carrying only a small part of the genetic variation of a species or when populations pass through bottlenecks, where only a small part of the population survives. The latter can be caused by accidents of sampling (sensu Mayr 1963), i.e. when large parts of a population are lost and only a few individuals happen, by chance, to survive in a favourable part of the environment. This can occur if a migratory barrier comes into action, and most individuals are unable to return for spawning, and if migratory individuals are led into an ecological trap (sensu Robertson and Hutto 2006). The fish may be trapped in an area with very low temperature in the ocean or if local pollution strikes a habitat and some individuals, by chance, happen to dwell in a refuge. The allelic variation of populations is the foundation for evolutionary adaptations. An important ecological mechanism by which salmonids are able to adapt to local environmental conditions is the precise homing of the fish to natal rivers and spawning grounds to breed with other individuals originating from the same local area (Verspoor et al. 2007). Thus, the same river can support a number of at least semi-isolated populations. The existence of such a structuring is indicated by ecological and genetic investigations. The isolation among local populations of the same species is, however, not absolute. There is a certain degree of straying among salmonid populations resulting in gene flow among them. Fish from conspecific populations can interbreed because of a high degree of genetic similarity. Thus, populations may be locally linked in meta-population groups (Kuparinen et al. 2010). This gene flow makes neighbouring populations genetically more similar than populations originating farther apart. In some cases, phenotypic characters are determined by only one gene. In brown trout, the pattern of dark spots along their flanks is determined by genetics, and one allele gives many small spots whereas another gives fewer and larger spots. Fine-spotted trout inherit the allele for small spots from both parents. Those which inherit one of each type develop a deviating pattern of spots. Characters that are due to one or a few genes are denoted qualitative traits or characters. One population of
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fine-spotted trout is found in the mountain Lake Svartavasstjønn, south Norway (Skaala and Jørstad 1987). These fish thus have a natural genetic tag and can be easily recognized by four spots in each eye forming a cross and have been used to estimate the survival of hatchery fish released into natural populations of wild brown trout (Skaala et al. 1991). Characters that are due to many different genes are denoted quantitative traits. Most phenotypic and ecological characters are such quantitative traits. The effect of the different alleles on quantitative traits varies, and the effect of each single allele can also vary but is usually small. High phenotypic diversity is expected to indicate a large genetic diversity. Only a small part of the phenotypic variation observed in natural populations has been attributed directly to genetic variation. However, in experiments with Atlantic salmon, selection responses have been obtained for a number of traits, such as sea survival and return rate to freshwater, age at sexual maturity, disease and parasite resistance, feed efficiency and percentage of sexually mature male parr (Saunders 1981; Carlson and Seamons 2008). For instance, there is a genetic basis for age and size at sexual maturity in Atlantic salmon and brown trout, and for other salmonids such as coho salmon (Oncorhynchus kisutch [Walbaum]) and sockeye salmon (Oncorhynchus nerka[Walbaum]). There is also adaptive variation for adult body size and morphology, egg size and various aspects of their developmental biology. These, and several similar examples, reveal the importance of genetics for the observed variation in phenotypic and ecological characters of salmonid fish and indicate that at least a part of the diversity in morphology, behaviour and life history patterns observed among natural populations are evidence of adaptations to local environmental conditions (cf. Quinn 2005). Phenotypic variability is also partly nongenetic. As the environmental conditions such as feeding opportunities, water temperature and current velocity - change, morphological, physiological, behavioural and ecological traits are adjusted. Such non-genetic variability is called phenotypic plasticity, and it allows the fish to respond adaptively with consequences for characters such as growth and developmental rates, reproduction and survival (Stearns 1992). This means that fish with similar genetic constitution raised in different environments can vary. For instance, Atlantic salmon parr grown with non-sibling groups in a hatchery environment resemble the body shape of the conspecifics in the hatchery more closely than full siblings grown in their natal stream habitat. Furthermore, wild smolts differ in shape from cultured offspring, but this difference is less pronounced, although still significant, when the fish are captured after 1 year of free swimming at sea (Von Cramon-Taubadel et al. 2005). A similar phenotypic variation was reported from studies on sibling groups of coho salmon reared in hatchery and natural environments (Chittenden et al. 2010). Thus, rearing conditions have significant impact on fish body shape, and some differences are phenotypic and disappear with time when the divergent groups are brought together in a common habitat. Hence, a large part of the ecological variation observed among naturally occurring populations is not a result of changed gene frequencies but an effect of phenotypic plasticity.
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Phenotypic adaptation takes place within a generation as demonstrated by the examples above. Genetic adaptation, on the other hand, occurs across generations by that better-adapted parents produce more and better-adapted offspring. Phenotypic adaptation can be regarded a short-term tactical response by individuals to their encounter with the environment; genetic adaptation is a strategic long-term response observable at the population level but driven by adaptive differences between individuals. Phenotypic plasticity obscures genetic effects, but the plastic response and degree of plasticity are influenced by genetics. Already in 1939, the Swedish scientist, Gunnar Alm, demonstrated that the plastic response to surplus feeding differed among populations of brown trout. All the fish of the populations he studied grew large when extensively fed, but offspring of large, lake-living brown trout grew much larger than offspring of conspecifics coming from small brooks. Similar differences in the growth response to surplus feeding are the basis for the brood-stock selection of farmed Norwegian Atlantic salmon. Fish from a large number of Norwegian salmon stocks were reared under similar conditions in a hatchery, and offspring of the fastest-growing families, such as those from the River Namsen, were selected (Gjedrem et al. 1991). Atlantic salmon from the River Namsen are extremely fast growing and late maturing. Thus, the separation between genetic adaptation and phenotypic plasticity is not simple. The phenotypic plasticity exhibited by the fish has probably evolved to minimize the cost of environmental change. Gunnar Alm also demonstrated how age at maturity changed with the growth rate for several species of freshwater fish, brown trout included (Alm 1959). A similar relationship holds good for many other species, including marine fish. The faster they grow at an early age, the earlier they mature. On the other hand, the later the growth rate levels off, the later they mature (Jonsson and Jonsson 1993). The pattern of phenotypic expression of a genotype across a range of environments is called the norm of reaction. Reaction norm has become a unifying concept in evolutionary biology and used in physiology as well as ecology (Angilletta et al. 2003).
1.5 Ideas, Purpose and Relevance of the Book This monograph on life history variations and reasons for those variations of Atlantic salmon and brown trout is inspired by a need to give a coherent presentation of the life histories of the species. Our knowledge has improved a lot over the last 40 years as we have studied the ecology of these fish. We were motivated by some recent works among which we will mention: Malcolm Elliott’s book Quantitative Ecology and the Brown Trout (1994), summarizing the knowledge on population regulation of brown trout; Evolution Illuminated: Salmon and their Relatives (2004) edited by Andrew Hendry and Stephen Stearns, which has contributed to the understanding of salmonid life history evolution; and The Atlantic Salmon: Genetics, Conservation and Management edited by Verspoor et al. (2007), which gives an up-to-date summary of knowledge about the population genetics of
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Atlantic salmon with very high relevance to management. We also acknowledge the stimulating scientific cooperation with colleagues at the Norwegian Institute for Nature Research and teachers and graduate students at the University of Oslo and the Norwegian University of Science and Technology, Trondheim. Collaboration with leading scientists such as J. Malcolm Elliott and John E. Thorpe from England and Scotland, respectively, and Mart R. Gross, Ian A. Fleming and Thomas G. Northcote, Canada, has also been most helpful and motivating. We have not agreed with them on all aspects concerning salmonid life history variations, but dissimilar opinions have been important for the hypotheses behind and design of our experiments and new results gained. Strength of the present work is that much of it has originated from our own life history studies but supplemented with knowledge based on numerous studies carried out elsewhere. Thus, we have first-rate knowledge about many of the relationships and associations described. This could also be a weakness because our scope could become narrow. We have compensated for this by drawing on knowledge from other species. This makes the lists of references long, but still, we have omitted many papers on the present or similar aspects, not adding new knowledge to the issues discussed. Thus, this is not a catalogue of everything published in recent years on the life history of Atlantic salmon and brown trout but a review of what we consider the state-of-the-art within this discipline. We have treated topics distinguishing the two species separately. Those which are similar were handled together. There are close associations between many ecological characters, between ecological and phenotypic characters, and between these characters and the environment the species exploit. Intraspecific and interspecific variations reveal different adaptations to their habitats, a variation influenced by learning from early experiences as well as genetic adaptations. We wish to bring these associations to as wide an audience as possible, because they are good examples of adaptation and evolution of ecological characters in poikilothermic vertebrates living in relatively young and cold environments. Salmonid populations are continuously facing new challenges threatening their population abundances. Careless human attitudes and actions have exterminated many populations and seriously weakened others. There are now indications of a negative climatic impact on the abundance of Atlantic salmon in the ocean, an impact probably mediated through the food chain due to a reduced abundance of keystone food organisms such as Calanus finmarchicus Gunnerus in the North Atlantic. But there are also negative effects in freshwater due to increased water temperature, especially in the southern part of the natural distribution area of the species (Jonsson and Jonsson 2004). Atlantic salmon and brown trout are two interesting sporting species, and fishing pressure has been high for a long time. However, exploitation of Atlantic salmon in the North Atlantic has declined since the mid 1970s. This is because of both decreased salmon productions and decreased fishing effort, i.e. due to strong regulation of marine fisheries especially during the 1980s and 1990s, but still with little recognizable positive effect on the stock abundances (Klemetsen et al. 2003).
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Salmonids are oxygen demanding and eutrophication, that decreases the oxygen concentration in the water and bottom substrate, threatens and can even exterminate some populations. The problem is highest at the southern end of the endemic distribution area where the oxygen content in the water is already low due to the high temperature. In northern localities, populations have been exterminated because of acid precipitation interacting with labile aluminium ions from the soil. This caused major fish kills during the twentieth century (Hesthagen et al. 2008). The rapid growth of the fish farming industry since the 1980s has created new problems for wild populations of Atlantic salmon (Hansen and Youngson 2009). Cultured salmonids deviate from their wild ancestors because of their hatchery and fish farm experiences and because of genetic changes due to factors such as brood stock selection, altered selecting forces in the artificial environment, genetic drift and inbreeding. Salmonids escape from hatcheries and fish farms, and instead of sporadic straying between populations, this has resulted in massive introgression of foreign alleles into wild populations, and thereby, changed their allele composition with possible consequences for local adaptations. Large numbers of hatchery fish in rivers increase the ecological competition on the spawning grounds as well as among young fish feeding in the river. Another negative impact is that hatcheries and fish farms can spread lethal pathogens to wild fish. There is no observation of a contagious disease that has originated in a fish farm, but the pathogen can multiply in the farm, and escaped fish function as vectors spreading the disease. Damming and regulation of rivers, especially for electricity production, have decreased the abundance of migratory fish (Ugedal et al. 2008). To mitigate this, fish passages and fish ladders have been built in many rivers, but their effects are variable. They are often not used by the migratory fish, possibly because they are ill constructed. Salmonids are water demanding, and when the water is taken out of the river and transferred elsewhere, negative effects can be excessive. With a steadily stronger demand for energy, this pressure on wild populations is expected to increase. Because of all the environmental problems and human-induced mortality factors, the management of Atlantic salmon and brown trout is demanding (Marttunen and Vehanen 2004). New rules and regulations as well as enhancement methods have been implemented in various countries during recent years, but many populations are still threatened and even exterminated, especially in the southern part of their distribution area. The salmon populations in several large rivers such as the River Rhine, once one of the world’s major natural Atlantic salmon producers, are extinct. There is a need to implement conservative catch quotas and adaptive management on a population level based on real-time monitoring instead of past abundance estimates. A new trend in the management of wild populations is the ‘precautionary principle’, which states that in case of uncertainty, one should exercise caution in favour of conservation (Crozier et al. 2004). It is also important that fishery management is built on our best scientific knowledge about the species. Atlantic salmon and brown trout stand as symbols of clean, cold water around the north Atlantic, and their long migrations and their capacity to orient for long distances through the open ocean have challenged the imaginations of biologists and laymen for several centuries. Therefore, they are among the most intensely studied fish species in the world.
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1.6 Organization of the Book After this introductory chapter, Chapter 2 gives an overview of the origin of salmonids, whether it was in freshwater, saltwater, or if the ancestor was an anadromous freshwater fish making feeding excursions to marine habitats. We present knowledge of the systematics of the genus Salmo, building on ecological, physiological and evolutionary knowledge about the species, with Atlantic salmon and brown trout being its two most widespread representatives. There is disagreement about how many other species the genus comprises. We cannot solve this disagreement but will bring the message that natural intraspecific diversity is much greater than perceived by those who have little experience from studying these species in their natural environments. Populations are spatially isolated in environments which differ from each other, and they are founded by genetically different individuals. The geographical distributions of the species are briefly described towards the end of Chap. 2. We feel that knowledge about the origin of the species and the population formation, as the fish invaded new water courses after having survived in refuges during glaciation periods, are a good background for understanding their present geographical distributions and factors important for their success. In Chap. 3, we describe the Atlantic salmon and brown trout habitat use in lotic and lentic environments, in fresh and salt waters. We present their habitat use associated with abiotic variables, such as depth, current velocity, bottom substratum and shelter, and biotic factors including diets and intraspecific and interspecific competition. There are many similarities, but also differences, in habitat use between these two opportunistic species, and we present knowledge about how age, size and sex groups exploit their habitats differently in accordance with variable needs. Growth and size are major life history characters with pervasive effects on others traits such as time of smolting, sexual maturity, fecundity, reproductive success, survival and longevity. We discuss factors associated with developmental rate, growth and body size in Chap. 4. Temperature and quality and quantity of food are the chief environmental factors influencing growth, while size is also highly affected by age at maturity and longevity. We describe both embryonic development and juvenile growth, and how habitat use and season influence growth and also relationships between growth, population structure and density. Fish compensate for decreases in growth that can occur during periods of hostile environmental conditions, although such compensation has a survival cost. Thus, growth is also a population regulatory mechanism which is treated in Chap. 8. Stunting is treated as a special case of density-dependent growth. Smolting, presented in Chap. 5, is the transformation process pre-adapting young anadromous salmonids for sea life. Smolting is a pre-requisite for the long marine migrations of salmonids reproducing and growing up in freshwater. This is a hormonally governed process initiated by the photoperiod given that the fish is in the appropriate physiological state. The speed of the process is heavily affected by water temperature. The size of the smolt varies among localities and flow conditions in the river, but also water temperature influences when smolting occurs. There is a gender difference in propensity to smolt.
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Atlantic salmon and brown trout are famous for their long migrations in fresh and marine environments, here treated in Chap. 6. We provide answers to questions such as how, when, where, which and why Atlantic salmon and brown trout migrate. Feeding, spawning and wintering migrations of Atlantic salmon and brown trout in fresh and salt waters are described together with factors initiating and influencing the runs. Migrations can be obligatory or facultative. Partial migration is the phenomenon whereby a part of the population moves to distant feeding areas while the rest remain resident in the home area. Towards the end of Chap. 6, we present a series of hypotheses proposed to explain how salmonids are able to navigate through the open ocean and along the coast back to their home stream. More than one sense is probably involved, and there are still many experiments to be carried out before we have the definite answers. Reproduction is the process by which new individuals are produced. Chapter 7 describes mechanisms influencing when salmonids attain maturity, changes that occur during maturation and resources allocated for reproduction. Both adaptations of primary and secondary sexual characters are described. Breeding success depends on time and place of spawning and strong and weak aspects of the fish as well as their competitors. We present reproductive strategies of the sexes of both species including mate choice as well as the relationships among phenotype, reproductive success and costs of reproduction. Recruitment is the result of reproduction, presented in Chap. 8. Density regulation is a main focus, and we present density-independent and density-dependent factors and bottlenecks in the life history when mortality is particularly high. We also present models describing recruitment based on parent density and mechanisms for density-dependent population regulation. Climate, being an omnipresent factor, controls biological production. It is dynamic, the change is gradual, and it fluctuates over both short- and long-term periods. For instance, the seasonal change is conspicuous over most of the distribution areas of Atlantic salmon and brown trout (Fig. 1.6). However, recent climate change has been faster than most alterations recorded earlier. At present, there appears to be a trend of global warming, partly due to human emission of carbon dioxide, with relatively more precipitation at high and less at low latitudes. Atlantic salmon and brown trout respond to the altered weather conditions by changes in abundance, growth, size, fecundity and geographical distribution, described in Chap. 9. Climate warming also influences competitors, predators and pathogens as well as abiotic factors, such as snow and ice-cover, the frequency of extreme weather conditions leading to droughts and spates. Our prediction about future change is chiefly based on trends in abundance and life history traits during the last 30–40 years. The growth in Atlantic salmon farming is considered a major threat to wild salmonids, which has been growing over the last 40 years. Escaped Atlantic salmon spread at sea and enter rivers for reproduction. This is now considered to be a further threat to wild conspecifics due to ecological competition, genetic introgression and spreading of pathogens from hatcheries and fish farms. These impacts are presented in Chap. 10. We outline how escaped farmed fish spread and survive
1.6 Organization of the Book
17
Fig. 1.6 The outlet area of the River Imsa (59°N) in (a) late autumn and (b) summer
in nature, and describe their success on the spawning grounds. We also present results from experiments testing interactions between farmed and wild fish. The success of escaped salmon is viewed in light of phenotypic and genotypic changes of the fish, which occur in hatcheries. At the end of the chapter, we give suggestions for how negative effects of salmon farming can be reduced. Hatcheries for releasing salmonids to rehabilitate and enhance wild populations have a history back to about 1850. Anglers often perceive stocking to be the first option to mitigate population declines. More recently, hatcheries have been used as a conservation measure. Chapter 11 gives results of stocking of eggs, alevins, parr, smolts and post-smolts for Atlantic salmon and brown trout. Often, the results from
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1 Habitats as Template for Life Histories
stocking programs have been disappointing, and we discuss possible reasons for this. We also discuss population effects of fishing and present alternatives to stocking such as habitat improvements, building of fish ways and removal of migratory barriers. We end the chapter by describing adaptive management as a method to organize the supervision of harvested fish populations. Habitat, as template for life histories, is the major theme of this book. In Chap. 12, we summarize the major environmental effects on populations of Atlantic salmon and brown trout. However, our knowledge about life histories of these species is far from complete. In this chapter, we, therefore, suggest new research, which should be performed to compliment works already done. We expect many of these issues to be exploited by scientists in the future, when they seek new knowledge about life history variation of the Atlantic trouts. Many technical terms occur in ecological studies. These terms may be a hindrance for our communication to a wider audience. Thus, to increase the accessibility of the book, we provide a glossary, which may be helpful when reading the text or primary literature on which this book is based. In the text, we usually mention species by their common name. Therefore, we have indexed the references to species and give also their scientific name with the author of original description included. References to scientific literature come directly after the text of each chapter. The cited authors are indexed separately before the subject index. Key points are highlighted as summary statements at the end of each chapter. We hope that these will help readers to focus on the messages we convey, whether the reader is a student, manager, researcher or an interested naturalist.
1.7 Summary 1. Habitat is the template for life histories both through effects of abiotic factors, such as water temperature, flow, depth, bottom substrate, ice cover, barriers to migration, nutrient richness, habitat coherence and consistency and biotic functions, such as competition intensity that influence life history traits. 2. Although Atlantic salmon and brown trout have complex life cycles and the complexity varies with the environmental complexity (brook, river, lake, sea), there is a general pattern that they grow up in freshwater but can move to saltwater after a physiological transformation called smolting, which is a pre-adaption of fish for marine life. However, it is also a morphological, ecological and behavioural changes adapting the young fish to feed in pelagic waters. 3. Variation in life history traits is partly environmentally induced and partly inherited. Environmental variation, such as in feeding opportunities, water current velocity and temperature affects the development of individual and population characters independent of their genetic diversity (phenotypic plasticity). But although all individuals of the same species are basically similar, the individuals are also genetically different as they can carry different variants of the same gene (alleles). Populations differ genetically because they were founded by genetically
References
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different individuals (founder effect), natural selection has acted differently upon the founded populations, and the genetic diversity may have changed with time due to different genetic mechanisms such as mutations and drift. The degree of phenotypic plasticity is inherited, and ecologists seek new knowledge about the relative contribution of environment and genetics to the life history diversity observed. 4. The understanding of life histories of Atlantic salmon and brown has improved a lot over the last 40 years, and the progress has been particularly fast during the last two decades because of improved knowledge about ecological genetics including the evolution of ecological characters. 5. The purpose of this book is to provide an accessible, up-to-date review of the life history variation of Atlantic salmon and brown trout based on knowledge published during recent years, from different habitats and geographical areas, with implications for management and conservation of the species. Our own studies, together with colleagues in Norway and elsewhere, form the core of the presentation. The generality of the results and the breadth of presentation are secured by citation of relevant studies performed by others. This is a presentation of the variation in life history patterns of the Atlantic trouts, Atlantic salmon and brown trout, under influence of natural and cultured habitats.
References Alm G (1959) Connection between maturity, size and age in fishes. Rep Inst Freshw Res Drottningholm 40:5–145 Andrews AC (1955) Greek and Latin terms for salmon and trout. Trans Proc Am Philos Assoc 86:308–318 Angilletta MJ Jr, Wilson RS, Navas CA et al (2003) Tradeoffs and the evolution of thermal reaction norms. Trends Ecol Evol 18:234–240 Berg OK (1985) The formation of non-anadromous populations of Atlantic salmon, Salmo salar. J Fish Biol 27:805–815 Bohlin T, Pettersson J, Degerman E (2001) Population density of migratory and resident brown trout (Salmo salmo) in relation to altitude: evidence for a migration cost. J Anim Ecol 70:112–121 Carlson SM, Seamons TR (2008) A review of quantitative genetic components of fitness in salmonids: implications for adaptation to future change. Evol Appl 1:222–238 Chittenden CM, Biagi CA, Davidsen JG et al (2010) Genetic versus rearing-environment effects on phenotype: hatchery and natural rearing effects on hatchery- and wild-born coho salmon. PLoS ONE 5(8):e12261. doi:10.1371/journal.pone.0012261 Crozier WW, Schön PJ, Chaput G et al (2004) Managing Atlantic salmon (Salmo salar L.) in the mixed stock environment: challenges and considerations. ICES J Mar Sci 61:1344–1358 Elliott JM (1994) Quantitative ecology and the brown trout. Oxford Series in Ecology and Evolution. Oxford Univ Press, Oxford Elliott SR, Coe TA, Helfield JM et al (1998) Spatial variation in environmental characteristics of Atlantic salmon (Salmo salar) rivers. Can J Fish Aquat Sci 55(Suppl 1):267–280 Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fish 6:379–416 Gibson RJ (1993) The Atlantic salmon in fresh water: spawning, rearing and production. Rev Fish Biol Fish 3:39–73
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Gjedrem T, Gjerde B, Gjøen HM (1991) Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 98:41–50 Hansen LP, Youngson AF (2009) Dispersal of large farmed Atlantic salmon, Salmo salar, from simulated escapes at fish farms in Norway and Scotland. Fish Manage Ecol 17:28–32 Harden Jones FR (1968) Fish migration. Edward Arnold, London Hendry AP, Stearns SC (2004) Evolution illuminated: salmon and their relatives. Oxford Univ Press, Oxford Hesthagen T, Fiske P, Skjelkvåle BL (2008) Critical limits for acid neutralizing capacity of brown trout (Salmo trutta) in Norwegian lakes differing in organic carbon concentrations. Aquat Ecol 42:307–316 Hoar WS (1976) Smolt transformation: evolution, behaviour and physiology. J Fish Res Board Can 33:348–365 Horton GE, Letcher BH, Bailey MM et al (2009) Atlantic salmon (Salmo salar) smolt production: the relative importance of survival and body growth. Can J Fish Aquat Sci 66:471–483 Jonsson B (1989) Life history and habitat use of Norwegian brown trout (Salmo trutta). Freshw Biol 21:71–86 Jonsson B, Jonsson N (1993) Partial migration: niche shift versus sexual maturation in fishes. Rev Fish Biol Fish 3:348–365 Jonsson B, Jonsson N (2004) Factors affecting marine production of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 61:2369–2383 Jonsson B, Jonsson N (2006a) Life history effects of migratory costs in anadromous brown trout Salmo trutta. J Fish Biol 69:860–869 Jonsson B, Jonsson N (2006b) Life history of anadromous brown trout. In: Harris G, Milner N (eds) Sea trout: biology, conservation and management. Blackwell, Oxford Jonsson B, Jonsson N (2009) Migratory timing, marine survival and growth of anadromous brown trout in the River Imsa, Norway. J Fish Biol 74:621–638 Jonsson N, Hansen LP, Jonsson B (1991) Variation in age, size and repeat spawning of adult Atlantic salmon in relation to river discharge. J Anim Ecol 60:937–947 Jonsson N, Jonsson B, Hansen LP et al (1994) Effects of sea-water-acclimatization and release sites on survival of hatchery-reared brown trout Salmo trutta. J Fish Biol 44:973–981 Klemetsen A, Amundsen P-A, Dempson JB et al (2003) Atlantic salmon Salmo salar L., brown trout Salmo trutta L. and Arctic charr Salvelinus alpinus (L.) a review of aspects of their life histories. Ecol Freshw Fish 12:1–59 Kuparinen A, Tofto J, Consuegra S et al (2010) Effective size of an Atlantic salmon (Salmo salar L.) metapopulation in Northern Spain. Conserv Genet 11:1559–1565 Limburg KE, Landergren P, Westin L et al (2001) Flexible modes of anadromy in Baltic sea trout: making the most of marginal spawning streams. J Fish Biol 59:682–695 Lundqvist H, Fridberg G (1982) Sexual maturation versus immaturity: different tactics with adaptive values in Baltic salmon (Salmo salar L.) male smolts. Can J Zool 60:1822–1827 Marttunen M, Vehanen T (2004) Towards adaptive management: the impacts of different management strategies on fish stocks and fisheries in a large regulated lake. Environ Manage 33:840–854 Mayr E (1963) Animal species and evolution. Belknap Press/Harvard University Press, Cambridge Poff NL, Ward JV (1990) Physical habitat template of lotic systems: recovery in the context of historical pattern of spatiotemporal heterogeneity. Environ Manage 14:629–645 Quinn TP (2005) The behavior and ecology of Pacific salmon and trout. University of Washington Press, Seattle Robertson BA, Hutto RL (2006) A framework for understanding ecological traps and an evaluation of existing evidence. Ecology 87:1075–1085 Saunders RL (1981) Atlantic salmon (Salmo salar) stocks and management implications in the Canadian Atlantic Provinces and New England, USA. Can J Fish Aquat Sci 38:1612–1625 Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Fisheries Research Board of Canada, Ottawa
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Skaala Ø, Jørstad KE (1987) Fine-spotted brown trout (Salmo trutta): its phenotypic description and biochemical genetic variation. Can J Fish Aquat Sci 44:1775–1779 Skaala Ø, Jørstad KE, Borgstrøm R (1991) Fine-spotted brown trout: genetic aspects and the need for conservation. J Fish Biol 39(Suppl A):123–130 Southwood TRE (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46:337–365 Southwood TRE (1988) Tactics, strategies and templets. Oikos 52:3–18 Stearns SC (1992) The evolution of life histories. Oxford University Press, New York Studenov II, Antonova VP, Chuksina NA et al (2008) Atlantic salmon (Salmo salar Linnaeus, 1758) of the Pechora River. SevPINRO, Arkhangelsk Thorpe JE, Mangel M, Metcalfe NB et al (1998) Modelling the proximate basis of salmonid life-history variation, with application to Atlantic salmon, Salmo salar L. Evol Ecol 12:581–599 Townsend CR (1996) Invasion biology and ecological impacts of brown trout Salmo trutta in New Zealand. Biol Conserv 78:13–22 Ugedal O, Næsje TF, Thorstad EB et al (2008) Twenty years of hydropower regulation in the River Alta: long-term changes in abundance of juvenile and adult Atlantic salmon. Hydrobiologia 609:9–23 Verspoor E, Stradmeyer L, Nielsen JL (eds) (2007) The Atlantic salmon: genetics, conservation and management. Blackwell, Oxford Von Cramon-Taubadel S, Ling EN, Cotter D et al (2005) Determination of body shape variation in Irish hatchery-reared and wild Atlantic salmon. J Fish Biol 66:1471–1482
Chapter 2
Species Diversity
2.1 Organization of the Chapter In this chapter, we describe systematics and geographical distribution of Atlantic salmon and brown trout and factors important for their success in natural systems. Both are cold water species from the northern hemisphere, but due to human aquaculture and stocking, they now occur in most parts of the world offering suitable habitats. We begin by describing the origin of salmonid fish, and discuss whether it was marine or freshwater. It has also been suggested that the ancestor was anadromous, migrating between freshwater and the sea. This has long been a controversy and debated at least since the nineteenth century (Day 1887). But recent paleontological, physiological, behavioural, and evolutionary evidence appear to have settled the dilemma. Then, we describe taxonomic relationships within the family Salmonidae and the genus Salmo. The many periods of Pleistocene glaciations, deglaciation and postglacial colonization have shaped the genetic variability of the species. Atlantic salmon and brown trout have survived glaciated periods in refuges south of the glaciated area, redistributed in interglacial periods and colonized the northern river as these became available and hospitable. The systematics of Salmo are not yet settled (Nelson 2006). The species are highly variable. They can specialize trophically, which leads to phenotypic, intraspecific variability (Robinson and Parsons 2002). Although their diet changes as the fish grow, different individuals can specialize on different food items: zoobenthos, zooplankton, surface arthropods and fish, which are reflected by phenotypic dissimilarities. Furthermore, the individuals can use lentic and lotic environments and feed in fresh and salt water. Freshwater residents and anadromous individuals differ not only in habitat and migratory behaviour, but also in growth and phenotypic appearance. As local populations segregate during spawning, gene flow between them is typically low. Therefore, conspecific populations are often phenotypically and genetically differentiated both among rivers and between fish using different spawning areas within the same river (Pakkasmaa and Piironen 2001;
B. Jonsson and N. Jonsson, Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories, Fish & Fisheries Series 33, DOI 10.1007/978-94-007-1189-1_2, © Springer Science+Business Media B.V. 2011
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Ferguson 2006). In old lakes, where trout have existed over a long period, such as in Lake Ohrid situated on the border between Macedonia and Albania, sister species may have evolved (cf. Kottelat and Freyhof 2007). Atlantic salmon have a stronger tendency towards anadromy than brown trout. They have a lower percentage of non-anadromous populations, and they move farther to sea. This niche difference is reflected by their more streamlined body shape with a longer and slimmer caudal peduncle, advantageous in strong currents as well as during long migrations in the ocean (Figs. 2.1 and 2.2). The two species are also distinguished by the larger mouth, smaller pectoral fins and more frequent dark spots beneath the lateral line in brown trout than Atlantic salmon. Parr of brown trout, but not Atlantic salmon, have a red-coloured outer end of the adipose fin. The parr marks along the flanks of young fish are larger and placed more regularly along the flanks in Atlantic salmon than brown trout. Furthermore, there is more often geographical isolation among populations of brown trout, as the species is less migratory than Atlantic salmon and more frequently form isolated non-anadromous populations. While Atlantic salmon can move several thousand kilometres in the ocean before returning to the home stream for spawning, anadromous brown trout are coastal and estuarine fish which usually move less than 100 km from the river mouth (Jonsson and Jonsson 2006). Due to a higher degree of geographic isolation between populations of brown trout than Atlantic salmon, phenotypic variation is higher in brown trout than in Atlantic salmon. This is probably the main reason for the higher degree of taxonomic confusion in brown trout than Atlantic salmon. This chapter describes the original range of the species and how the area of brown trout, in particular, has been extended through population translocations since the middle of the nineteenth century. Brown trout easily become established in new areas. In fact, this is one of the world’s most invasive fish species, thanks to its wide habitat tolerance (Lowe et al. 2000), flexibility in life history traits, migratory behaviour and spawning time (Valiente et al. 2010). For instance, Olsson et al. (2006) demonstrated that high density and scarcity of food influence the onset of migratory behaviour in this species, and this trait seems to be determined more by environmental than genetic factors. Atlantic salmon, on the other hand, have difficulty establishing populations outside their native range (Naylor et al. 2005). This species is less able to form nonmigratory populations and tend to migrate much longer distances than brown trout, which may make it more difficult for them to locate their home stream when transferred to a new area with differing water current systems and geomagnetic properties. One should note, however, that the present geographical distribution of the Atlantic salmon is formed by river invasions from glacial refuges in the North Atlantic drainage during the last 18,000 years, supporting the contention that they are able to inhabit due areas given enough time. Anadromous brown trout and Atlantic salmon have almost identical distribution areas in Europe. Only the long-ranging Atlantic salmon have been able to reach and colonize North America on their own. There, the presence of brown trout is due to human introductions.
2.1 Organization of the Chapter
25
Fig. 2.1 Morphological differences between heads of (a) brown trout and (b) Atlantic salmon parr. The maxillary is shorter and the park spots on the opercula more conspicuous in Atlantic salmon than brown trout.
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Fig. 2.1 (continued) Tails of (c) brown trout and (d) Atlantic salmon parr. The caudal fin has more pointed lobes and the adipose fin lacks the red colour in Atlantic salmon than in brown trout. Brown trout have often a white rim on the anal fin
In the North Atlantic watershed, Atlantic salmon have revealed excellent postglacial colonizing ability contrasting their reputation as ineffective invaders. It is not yet known why they are poor colonizers in other parts of the world, and it remains to be tested whether this is associated with navigational difficulties during long migrations at sea, competition for food or spawning area or presence of specific pathogens lethal to the fish. Atlantic salmon, contrary to brown trout, seldom form freshwater resident populations, and the anadromous fish migrate very far and may go astray in the ocean when introduced to completely new areas. For instance, signals used during homing, whether these are linked to ocean currents or the magnetism of the earth, may be difficult to use when introduced into areas to which they are not adapted. This may be the reason why stocking of the short-distance-migrating anadromous brown trout, but not Atlantic salmon, have been successful when transferred to streams such as those of the Kerguelen Islands in the South Indian Ocean (Ayllon et al. 2004). Also, some factors in the new systems may counteract immigration. This can be interspecific competition with native species, predation or presence of parasites and pathogens to which the species has no natural defence. If so, this
2.1 Organization of the Chapter
27
may parallel the situation for rainbow trout [Oncorhynchus mykiss (Walbaum)] in Europe, where the presence of whirling disease, caused by the endemic myxosporidean parasite Myxobolus cerebralis, in addition to competition with native species and hatchery selection, may contribute to the poor ability of this species to form selfsustaining natural populations there (Jonsson et al. 1993; Jonsson 2006). We end the chapter with a short description of factors constraining the spawning success and geographical range of these species. The temperature conditions appear critical and warm water constrains the distribution at low latitudes. In addition, low oxygen saturation and lack of suitable spawning substrate can limit the geographical distribution of both species in lowland areas.
Fig. 2.2 Morphological differences between heads of male spawners of (a) brown trout and (b) Atlantic salmon. The hook of the under jaw is largest in Atlantic salmon. Brown trout has more brown spots. In Atlantic salmon the spots have often a more reddish colour.
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Fig. 2.2 (continued) Tails of adult (c) brown trout and (d) Atlantic salmon. The caudal fin is more concave and the caudal peduncle is slimmer and longer in Atlantic salmon than brown trout. Brown trout have more dark spots below the lateral line
2.2 Taxonomic Diversity The evolutionary history and taxonomic diversity of Salmonidae have for many years remained matters of controversy (Regan 1914; Norden 1961; Oleinik 1997; Oakley and Phillips 1999; Crespi and Fulton 2004). Species-level and genus-level phylogenetic research have provided insights into some relationships, but still, the systematics of the family and sub-taxa are not settled (Stearley and Smith 1993; Osinov 1999; Nelson 2006; Kottelat and Freyhof 2007). Here, we review knowledge of salmonid history with special emphasis on the genus Salmo.
2.2.1
Salmonid Evolution
The order Salmoniformes can be traced back to the Upper Cretaceous about 100 million years BP. These ancient fish were primitive euteleosts. The salmonid fossil record is, however, incomplete. This is at least partly because the characters – by
2.2 Taxonomic Diversity
29
which the order is recognized - are not easily fossilized (Nelson 2006). Typical taxonomic characters are presence of an adipose fin, physostomous swim bladder and soft-rayed fins. The relationships among the families of the order are uncertain (Greenwood et al. 1973). But the family Salmonidae appears distinct and closely linked to the ancestry of the more advanced neoteleosts (Carroll 1988). According to Wilson and Li (1999), the earliest known salmonine fish is from Eocene, approximately 50 million years BP. This was Eosalmo driftwoodensis Wilson, a small fish similar to today’s graylings (Thymallus). They lived in cold freshwaters in northwestern North America. Salmonids also occur in the fossil records from the Miocene, between 24 and 5 million years ago (Nelson 2006). The Salmonidae have probably evolved from a common ancestor through genome duplication between 50 and 100 million years ago (Svärdson 1945; Allendorf and Thorgaard 1984; King et al. 2007). The evolution of the family has probably been driven by adaptive benefits of this duplication. The species have approximately twice as much DNA per cell as those of other closely related fish families, but their tetraploid genome has evolved in each species to a point where it now behaves as normal diploids. What was the original salmonid habitat? This has been discussed for almost two centuries: Was it fresh or salt water? The reason for this discussion may be the notion that marine fish are generally unable to live in freshwater, and freshwater fish are unable to make a transition to a marine habitat, and yet, salmon, trouts and a number of other species do so. One view is that the Salmonidae has a marine ancestry (Day 1887; Regan 1911; Thorpe 1982, 1988, 1994). For instance, Thorpe (1988) maintained that the salmonid ancestor may have been a pelagic, herringsmelt-like fish (Argentina), which moved into freshwater for spawning and obtained better protection of their young. He viewed the Osmeriformes-like fish (Superorder Protacanthopterygii) to be salmonid ancestors, which moved into freshwater and establish freshwater resident populations, and that the anadromous habit was an intermediate step on the way to become freshwater resident. Thorpe (1982) wrote that there is an evolutionary trend in the family toward total dependence on freshwater and away from a marine dependence. He maintained that salmonids are primitive fish, and that freshwater life was enabled by specific adaptations superimposed on a basically marine organism. By that, he reflected Regan’s (1911) view that salmonids may be regarded as marine fish establishing themselves in freshwater. Thorpe appeared to argue that future evolutionary directions of salmonids were determined by the direction of their evolutionary past. This implies that evolution has momentum and direction, projecting adaptation forwards (McDowall 2001). This is an orthogenetic argument, a form of evolution that is rejected by conventional evolutionary biologists (e.g. Mayr 1982). A somewhat different view was presented by McDowall (1993). He suggested that the salmonid ancestors themselves were anadromous. He argued that the Family Salmonidae has a common ancestry with, and is a sister group of, the northern hemisphere Osmeridae, and also with the southern hemisphere Retropinnidae and Galaxidae, other diadromous Protacanthopterygii families. The latter is a taxonomic assemblage of primitive euteleosts, established by Greenwood et al. (1966) and later
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revised (e.g. Rosen 1974). The species move between fresh and salt water, indicating that the migratory habit is an ancestral character. McDowall (1993), therefore, felt that the present life history style of these sister taxa is informative of their ancestral condition. Thus, he thought that anadromy might be a trait, which the families inherited from a common ancestor. Consequently, it has not been necessary for them to become diadromous in separate evolutionary events; it occurred prior to the evolution of the families. This view, however, has not gained much recent support. The most probable explanation is that the origin of Salmonidae was in freshwater. This is an old view, first presented in the nineteenth century (e.g. Günther 1866) and supported by Tchernavin (1939). Tchernavin (1939) maintained that the freshwater forms of the Salmonidae are more primitive than the sea-run migratory forms. He based his view on the observations that the distribution of salmonids resembles that of many freshwater plants and animals. Furthermore, he knew that salmonids exhibit precise homing migrations and expend great energetic and navigational efforts getting into freshwater to spawn. It is simpler to view this reproductive behaviour as a primitive trait rather than a character developed by marine fish finding a new way of protecting their offspring. His last argument was that young anadromous salmonids (parr) in freshwater are very similar to the adult freshwater forms. Tchernavin’s (1939) hypothesis was supported by physiologists, such as Hoar (1976), who added detailed information on geographic distribution, morphology, biochemistry, physiology and behaviour, which pointed in the same direction. Furthermore, the structure of the glomerular kidney indicates a freshwater origin of salmonid fish. For instance, the glomerulus (the glomerulus in the Bowman’s capsule and associated vessels are the filtration unit of the kidney) has a long distal tubule segment as in freshwater fish. This is lost in marine fish (Tanaka 1985). The distal tubule counteracts the influx of water in freshwater and the loss of monovalent ions (Na+, K+, Cl−) (Holz and Raidal 2005). Marine fish have only kept the proximal tubule segment of the freshwater fish. This segment is responsible for divalent ion secretion (Mg++, Ca++). The kidney of marine fish conserves water and energy relative to that of freshwater fish. Stearley (1992) and Stearley and Smith (1993) addressed the origin of the Salmoninae in cladistic analyses. They concluded that this subfamily indeed had a freshwater origin. This view was also supported by authors such as Greenwood (1993). Furthermore, Ishiguro et al. (2003) analysed mitochondrial DNA from 34 species of euteleosts, protacanthopterygians included. Their analysis showed the Esociformes (pikes), and not the Osmeroides (smelts), as the closest sister group to the Salmoniformes (Fig. 2.3). According to Ramsden et al. (2003), this lends support to the proposition that Salmoniformes have a freshwater origin. They also argued that this evidence, and the fact that anadromous salmonids have mostly freshwater parasites and no marine endoparasites, lend support to the freshwater origin hypothesis, and that anadromy probably evolved in the ancestor of Salmo, Parahucho, Salvelinus, and Oncorhynchus, as well as that of Stenodus and Coregonus (Fig. 2.4). The freshwater origin of salmonids was also supported by Limburg and Elfman (2010) who based their view on the zinc: calcium ratios in the otoliths of Salmoniformes and their sister groups.
2.2 Taxonomic Diversity
31 69 91 3 39 100 39 92 14
82 7 82 9
Clupeomorpha Alepocephaloidea Ostariophysi Esociformes Salmoniformes Argentinoidea Osmeroidei Neoteleostei
Fig. 2.3 The phylogeny of euteleosts based on analysis of the mitochondrial genome sequences. Only Salmonidae and Esociformes belong to the Protacanthopterygians, and Esociformes and not Osmeroidei or Argentinoidea, as formerly hypothesised, are the sister taxon to Salmonidae (From Ishiguro et al. (2003). Reproduced with permission of Elsevier B.V.)
Fig. 2.4 Protacanthopterygii and the evolution of anadromy (A). Anadromy evolved in ancestors to Salmo, Parahucho, Salvelinus, Oncorhynchus, Stenodus and Coregonus. The others taxa are freshwater resident (F). Eosalmo is extinct (From Ramsden et al. (2003). Reproduced with permission of Elsevier B.V.)
In the broader perspective, all teleosts probably had a freshwater origin. According to Fyhn et al. (1999), teleosts colonized the saline oceans by way of marine excursions for feeding and returned to freshwater for spawning. The teleosts were not independent from freshwater before a mechanism for increasing the water content of the yolk in the eggs was developed. This oocyte hydration seems to be a key feature in the adaptive evolution to marine life, an event that probably occurred about 55 million years ago (Kristoffersen and Finn 2008). Thus, the oldest known salmoninine, Eosalmo driftwoodensis, may have been present at about the same time as the teleost radiation into seawater occurred. Before that, all teleosts were
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spawning in freshwater, but many may have exhibited anadromous life histories as McDowall (2001) argued, and as many fish, including Atlantic salmon and brown trout, still do. The salmonids seem to have changed little over the past million years even though they have endured drastic oscillations in climate (Power 2002). Since about 2.5 million years BP, there have been numerous glaciations (Pilou 1991), and during most of the last 0.6 million years, the climate has been glacial. The last glaciation period commenced about 75,000 years ago and culminated 18,000 years BP (Denton and Hughes 1981). The ice cap over northwestern Europe and North America disappeared between 8,000 and 14,000 years ago, and it is unlikely that Atlantic salmon or brown trout survived in most of these regions during maximum glaciation. But ice cover was not continuous and there were several northern refuges, where freshwater fish could survive as well as areas south of the glaciated region, from where they colonized the northern rivers independently as the ice retreated (Ferguson 2006). As a result of isolation over long time periods in the separate refuges, several genetically distinct ancestral lineages evolved (Bernatchez 2001). Some of these evolutionary lineages were further split as a result of shorter periods of isolation within localities. Also interbreeding and introgression across evolutionary lineages seem to have taken place since postglacial colonization, possibly as a result of human interference and environmental perturbations. Breakdowns in the reproductive isolation between the lineages have also occurred (Ferguson 2006).
2.2.2
Salmonidae
The family Salmonidae comprises three subfamilies: Coregoninae, Thymallinae and Salmoninae (Nelson 2006). Mitochondrial genome sequences of various salmonids show that there was an ancestral Coregoninae branching within the Salmonidae, with Thymallinae as the sister group to Salmoninae (Yasuike et al. 2010). Their distributions are Holarctic. Thus they occur in North America, Europe and Asia. Salmonids are medium- to large-sized terete-bodied, but laterally compressed, fish (Scott and Crossman 1973). They have pelvic axillary processes and lateral lines, the last three caudal vertebrae are turned up and cycloid scales cover the body but not the head. The salmonids consist of wide-ranging freshwater and anadromous fish. The biological diversity of the salmonid family is greater than recognized in the current taxonomy because of nomenclatorial limitations (Behnke 1972). The species are highly variable, and they often live in isolated systems supporting few competing fish species. In such environments, different morphs of the same species can exploit different habitats and specialize on different food items such as zooplankton, zoobenthos and fish, as described for whitefish, brook charr, Arctic charr, and brown trout (Fig. 2.5; Lindsey 1981; Ferguson 1986, 2006; Jonsson and Jonsson 1993, 2001; Østbye et al. 2005a, b). The variants can be recognized from their different morphologies and life histories (Hindar and Jonsson 1982, 1993; Sandlund et al. 1992; Østbye et al. 2006). Morphological differences are often
2.2 Taxonomic Diversity
33
Fig. 2.5 Salmonid species that exhibit resource polymorphism and form both freshwater-resident and anandromous populations. (a) European whitefish [Coregonus lavaretus (L.)], (b) brook charr (Salvelinus fontinalis Mitchell), (c) Arctic charr [Salvelinus alpinus (L.)], and (d) brown trout (Salmo trutta L.)
34
2 Species Diversity
related to their different feeding niches and include mouth position, dentition, body form, fin lengths and numbers and size of gill rakers (Lindsey 1981; Snorrason et al. 1994). Life history variation includes different growth rates, age at maturity and reproductive efforts (Jonsson and Hindar 1982; Jonsson et al. 1988). For instance, in quite stable environments such as Thingvallavatn, Iceland, where most of inflowing water is groundwater and water temperatures in summer go up to approximately 10°C, the Arctic charr exhibit strong feeding specialization. Two morphs feed on the snail Lymnaea peregra; the large form lives in the bottom substratum and the small form stays in crevices and interstitial spaces in the lava substratum of the lake during daytime but can feed in epibenthic water at night. There are also one planktivorous and one piscivorous Arctic charr morph in the lake (Jonsson et al. 1988; Sandlund et al. 1992; Malmquist et al. 1992; Snorrason et al. 1994; Jonasson et al. 1998).
2.2.3
Salmoninae
The Salmoninae includes at least five genera (Nelson 2006): Brachymystax (lenox), an Asian freshwater fish (Xia et al. 2007); Hucho (huchen and taimen) that consists of freshwater and anadromous fish found in northern Asia and the Danube basin of Europe (Phillips et al. 2004); Oncorhynchus (Pacific salmon and trouts) (Esteve and McLennan 2007) that are freshwater and anadromous fish in the North Pacific basin; Salvelinus (charrs) (Behnke 1980), circumpolar freshwater and anadromous fish in the northern hemisphere; Salmo (Atlantic trouts) (Stearley and Smith 1993), freshwater and anadromous fish endemic to the North Atlantic basin. According to Nelson (2006), the Salmoninae comprises about 30 species. Four additional genera have been suggested. These are Parahucho, Salvethymus, Salmothymus and Acantholingua (King et al. 2007). However, DNA analysis indicates that Acantholingua ohridana, endemic to Lake Ohrid, should be placed in Salmo. Furthermore, Salmothymus obtusirostris, a widely distributed species in the Adriatic drainage, should be placed in Salmo as a sister species to brown trout (Phillips et al. 2000; Crespi and Fulton 2004), as for instance accepted by Kottelat and Freyhof (2007). Taimen is sometimes classified in the genus Parahucho, but whether taimen should be classified as Hucho or Parahucho is still controversial.
2.2.4
Salmo
Atlantic salmon and brown trout are two of the Atlantic trouts sensu Nelson (2006). Both species were described by Carolus Linnaeus in his 10th edition of the book Systema Naturae, published in 1758. This edition is considered as the starting point of zoological nomenclature. Linnaeus described stream trout (Salmo fario), river trout (Salmo trutta), sea trout (Salmo eriox) and anadromous salmon (Salmo salar) as different species. Today, they are recognized as two species, brown trout or European trout (Salmo trutta L.) and Atlantic salmon (Salmo salar L.).
2.2 Taxonomic Diversity Table 2.1 Synonyms of Salmo salar Linneaus 1758 Synonym Author Smitt 1882 Salmo brevipes S. caerulescens Schmidt 1795 Salmo fario var. samulus Walbaum 1792 S. gloveri Girard 1854 S. goedenii Bloch 1784 S. gracilis Couch 1865 S. hamatus Cuvier 1829 S. hardinii Günther 1866 S. nobilis Olafsen 1772 S. ocla Nilsson 1832 S. renatus Lacèpede 1803 S. rilla Lacèpede 1803 S. salar Linnaeus 1758 S. salar americanus Payne et al. 1971 S. salar infra. biennis Berg 1912 S. brevipes Smitt 1882 S. salar brevipes morpha relictus Berg 1932 S. salar europeus Payne et al. 1971 S. salar var. lacustris Hardin 1862 S. salar var nobilis Smitt 1895 S. salar ouananiche McCarthy 1894 S. salar saimensis Seppovaara 1962 S. salar tasmanicus Johnston 1889 S. salmo Valenciennes 1848 S. salmulus Walbaum 1792 S. sebago Girard 1853 S. strom Bonnaterre 1788 Malmgren 1863 Trutta salar relicta
35
Found in Russia Czech Republic Great Britain Maine, USA Poland, Baltic Sea British Isles Europe Sweden Iceland Sweden France France Europe, North America North America Russia Russia Russia Europe Sweden Russia Canada Finland Tasmania, Australia Belgium, Netherlands, England England, Wales Maine, USA Norway Russia
The taxonomy of Salmo is still a matter of controversy (Kottelat and Freyhof 2007; Webb et al. 2007; McKeown et al. 2010). For instance, more than 60 synonyms for varieties of brown trout and more than 20 for varieties of Atlantic salmon have been described (Tables 2.1 and 2.2). The number of Salmo species recognized varies not the least because of the variable shape and colouration of these fish when found in nature, but because the species inhabit and are adapted to very different habitats over large distribution areas. Kottelat and Freyhof (2007) listed 27 different Salmo species in Europe and called that a very conservative estimate. They maintained that the diversity of Atlantic trouts is underestimated and that life history traits confuse the picture. Nelson (2006), on the other hand, maintains that the genus includes five separate species, and Webb et al. (2007) claim that there are only two valid species in the genus. Because of this confusion, authors often refer to brown trout as the Salmo trutta species complex (Bernatchez 2001; Schöffmann et al. 2007; Meraner et al. 2007; Caputo et al. 2009). The taxonomic confusion is partly founded upon the phenotypic variability of the Atlantic trouts. When a deviating morphological variant is found, taxonomists,
36
2 Species Diversity
Table 2.2 Described species which can be synonyms of Salmo trutta Linneaus 1758. Possible alternative taxonomic names are given as footnotes Synonym Author Found in Valenciennes 1848 France Fario argenteus Salar ausonii Valenciennes 1848 France, Germany, Italy S. ausonii parcepunctata Heckel & Kner 1858 Austria S. ausonii semipunctata Heckel & Kner 1858 Austria S. bailloni Valenciennes 1848 France S. gaimardi Valenciennes 1848 Iceland S. genivittatus a Heckel & Kner 1858 Adriatic basin S. macrostigma Duméril 1858 Algeria S. spectabilis Valenciennes 1848 Russia Salmo albus b Bonnaterre 1788 Great Britain S. brachypoma Günther 1866 England S. caecifer Parnell 1838 Scotland S. cambricus Donovan 1806 Wales S. caspius c Kessler 1877 Caspian Sea watersheds S. cornubiensis Walbaum 1792 England S. cumberland Lacepède 1803 England, Scotland S. dentex c Heckel 1851 Adriatic Basin S. eriox Linnaeus 1758 European seas and rivers S. eriox rhodanensis d Fowler 1974 Western Europe S. estuarius Knox, 1854 England, Scotland S. ezenami e Berg 1948 Russia S. fario Linnaeus 1758 Europe S. fario loensis Walbaum 1792 England S. fario major Walecki 1863 Poland, France S. fario var. forestensis Bloch & Schneider 1801 Russia S. farioides e Karaman 1938 Eastern Adriatic slope S. farioides zrmanjaensis f Karaman 1938 Republic of Macedonia S. gadoides Lacepède 1803 France S. gallivensis Günther 1866 Ireland S. islayensis Thomson 1873 Islay Island, UK S. labrax e Pallas Black Sea and adjacent watersheds S. lacustris Linnaeus 1758 Switzerland S. lacustris var. rhenana Fatio 1890 Switzerland S. lacustris romanovi Kawraisky 1896 Georgia, Eurasia S. lacustris var. septentrionalis Fatio 1890 Switzerland S. lapasseti g Zill 1858 Algeria S. lemanus Cuvier 1829 European lakes S. letnica typicus h Stefanovic 1948 Sebia S. levenensis Yarrell 1839 Scotland S. microps i Hardin 1862 Sweden S. mistops Günther 1866 Norway S. montana Walker 1812 Scotland (continued)
2.2 Taxonomic Diversity Table 2.2 (continued) Synonym
37
Author
Found in
S. obtusirostris var. oxyrhynchus j S. orcadensis
Steindachner 1882
Croatia
Günther 1866
S. oxianus S. orientalis S. pallaryi k S. pallasii l S. phinoc S. polyosteus S. rappii S. saxatilis S. spurius S. stroemii S. sylvaticus
Kessler 1874 McClelland 1842 Pellegrin 1924 Günther 1866 Shaw 1804 Günther 1866 Günther 1866 Schrank 1798 Pallas 1814 Gmelin 1788 Gmelin 1788
S. taurinus S. trutta abanticus l S. trutta caspius m S. trutta ciscaucasicus n S. trutta ezenami S. trutta labrax o S. trutta labrax infra. danubiscus b S.trutta forma major p S. trutta macrostigma morpha lacustris q S. trutta major facies rhodanensisp S. trutta marmoratus morpha lacustris r S. trutta oxianus S. trutta var. pellegrini s S. truttulat S. venernensis S. visovacensisu Trutta fario var. macedonia v
Walker 1812 Tortonese 1954 Kessler 1877 Dorofeyeva 1967 Berg 1948 Pallas 1811 Holcik 1969
Orkney Islands, Scotland Afganistan Afganistan Morocco Ukraine England, Scotland Sweden Switzerland Germany Russia Norway Norway, Germany, Poland Scotland Turkey Caspien watershed Russia Russia Black Sea watershed Slovakia
Roule 1925 Poljakov et al. 1958
Western Europe Albania
Roule 1923
France
Poljakov et al. 1958
Albania
Kessler 1874 Werner 1931 Nilsson 1832 Günther 1866 Taler 1950 Karaman 1924
T. fario macroptera T. fario var. marmoratus r
Chichkoff 1939 Siebold 1863
T. letnica w
Karaman 1924
T. marina T montenigrina x T. obtusirostris kirkens y
Duhamel 1771 Karaman 1933 Karaman 1927
Afganistan Morocco Sweden Sweden Southern Europe Republic of Macedoniae Bulgaria River in the Alps draining south Republic of Macedoniae France Montenegro Croatia (continued)
38 Table 2.2 (continued) Synonym
2 Species Diversity
Author
Found in
T. obtusirostris salonitanaz Karaman 1927 Croatia T. salmanata Strøm 1784 Norway T. taleriaa Karaman 1933 Montenegro T. ungerib Yásárhelyi 1940 Hungary Lunel 1874 Switzerland T. variabilis a Synonym of Salmo marmoratus (Kottelat 1997) b Synonym of Salmo labrax Kottelat (1997) c Valid species (Kottelat 1997; Fricke et al. 2007) d Valid species as Salmo rhodanensis (Kottelat and Freyhof 2007) e Valid species (Kottelat and Freyhof 2007) f Valid species as Salmo zrmanjaensis (Mrakovcic et al. 1995; Kottelat 1997) g Synonym of Salmo cetti (Behnke 1984; Kottelat 1997) h Synonym of Salmo letnica (Kottelat 1997) i Synonym of Salmo lacustris and Salmo truttula (Kottelat 1997) j Synonym of Salmo obtusirostris (Snoj et al. 2002) k Valid species (Delling and Doadrio 2005) l Synonym of Salmo labrax (Fricke et al. 2007) m Synonym of Salmo caspius (Berg 1948; Kottelat 1997) n Valid species as Salmo ciscaucasicus (Reshetnikov Yu et al. 1997; Kottelat and Freyhof 2007) o Synonym of Salmo labrax (Kottelat and Freyhof 2007) p Valid species as Salmo rhodanensis (Kottelat 1997) q Synonym of Salmo farioides (Kottelat 1997) r Synonym of Salmo marmoratus (Kottelat 1997) s Synonym of Salmo cettii (Behnke 1984; Delling and Doadrio 2005) t Synonym of Salmo lacustris (Kottelat 1997) u Valid species as Salmo visovacensis (Mrakovcic et al. 1995; Kottelat 1997) v Valid species as Salmo macedonicus (Kottelat and Freyhof 2007) w Valid species as Salmo letnica (Kottelat and Freyhof 2007) x Valid species as Salmo montenigrinus (Kottelat and Freyhof 2007) y Synonym of Salmo obtusirostris (Kottelat and Freyhof 2007) z Synonym of Salmo obtusirostris (Snoj et al. 2002) or Salmo saloniana (Zupancic 2008) aa Valid species as Salmo taleri (Kottelat and Freyhof 2007)
especially those not acquainted with the wide morphological variation of natural salmonid populations, sometimes describe a new species without reference to their ecology or reproductive isolation when brought together in nature. Some of the phenotypic variation observed is caused by genetic variation and some is due to environmentally induced phenotypic plasticity and interactions between genetic and environmental factors (Langerhans 2008). The relative meaning of the two sources of variation is unclear, but in rainbow trout, Keeley et al. (2007) found genetics to be relatively more important than the environment and the same may hold good for the Atlantic trouts. Much of the genetic variation within salmonid species is maintained through geographic isolation. Populations living in separate water courses are de facto reproductively isolated, and over time, they will adapt genetically to their respective environments given genetic variations in the founder populations. Because of their precise homing ability (philopatry), there can also be restricted gene flow between
2.2 Taxonomic Diversity
39
conspecifics spawning at different locations in the same river, even though geographic isolation other than by distance is missing (Hindar et al. 1991). Sometimes, sympatric populations are adapted to different trophic niches. If the trophic niches are stable over time, the sympatric morphs can persist and also diversify by incipient sympatric speciation due to disruptive selection (Forseth et al. 2003) and assortative mating (Jonsson and Hindar 1982; Jonsson and Jonsson 2001), as demonstrated for threespined sticklebacks (Gasterosteus aculeatus L.) (Rundle and Schluter 2004). But since most salmonid populations largely occupy relatively young systems, the diversification will, in most cases, not have reached complete speciation. Exceptions can be populations occupying some very old systems such as lakes and rivers draining the Adriatic Basin (Fumagalli et al. 2002; Maric et al. 2006; Simonivic et al. 2007). During postglacial times, temperate and northern water courses have been invaded repeatedly by fish coming from different refuges. They have sometimes established separate spawning stocks within the same water courses (Ferguson 2006). Most of the postglacial immigrants were probably of anadromous origin, but there have also been invasions, at least of brown trout, from freshwater refuges along rivers formed as the glaciers retreated (McKeown et al. 2010). The phenotypic diversity in the genus Salmo is highest in the MediterraneanAdriatic area in Europe (Behnke 1968). In addition to Salmo trutta, this area harbours marble trout Salmo marmoratus, a trout with silvery to olive-green sides. Marble trout have irregular brown lines forming a marbled pattern on its dorsal side. Some of them also have red spots along the lateral line (Apostolidis et al. 1997). Marble trout, which exhibits a maximum body mass of approximately 50 kg, is the largest species of the genus (Kottelat and Freyhof 2007). Marble trout exhibit a substantial genetic divergence from other investigated Mediterranean trouts, and the trout lineages of the Danube and Atlantic regions (Giuffra et al. 1994, 1996). Genetic investigations suggest that Salmo marmoratus differentiated from the other Salmo lineages between 1 and 3 million years ago. Marble trout is endemic to the basins in the northern Adriatic rivers in Albany, Croatia, Italy, Montenegro and Slovenia (Crivelli et al. 2000). It is threatened by industrial and agricultural pollution, and it is difficult to find populations that are not introgressed by introduced Atlantic brown trout. The populations are, therefore, critically declining (Bernatchez et al. 1992; Snoj et al. 2000; Bernatchez 2001). There is no reproductive barrier between the two when brought together, and hybrids grow faster than pure marble trout and brown trout, possibly due to heterosis (Meldgaard et al. 2007). The taxonomic status of marble trout is, therefore, uncertain. The Garda Lake in the Po Basin supports one endemic form, Salmo carpio, locally known as carpione (Kottelat and Freyhof 2007). It is a lake dweller and differs from brown trout by spawning deep in the lake and by having two separate spawning seasons a year. Genetic evidence suggests that Salmo carpio originates from hybridization between Salmo trutta and Salmo marmoratus. Its species status remains unclear. However, Salmo carpio appears not to have introgressed with introduced Atlantic stocks of brown trout, indicating that this is a valid species. The taxonomic status of the trout in the Black, Caspian and Aral Seas is unclear. Based on ecological and morphological characters, Berg (1948) viewed them as
40
2 Species Diversity
subspecies of brown trout, Salmo trutta labrax in the Black Sea, Salmo trutta caspius in the Caspian Sea and Salmo trutta oxianus in the Aral Sea. The first two of these were treated as separate species by Kottelat and Freyhof (2007). We are not able to determine which opinion is correct. Lake Sevan of the Caspian Basin supports a distinct form of trout recognized as Salmo ischchan. Bernatchez and Osinov (1995) and Osinov and Bernatchez (1996) provided evidence that this trout is a variant of the same lineage as the other trout in the area and not a species derived from a primitive ancestor of Salmo trutta, as suggested by Behnke (1984). Possible, there are only two valid species in the genus as maintained by Webb et al. (2007) or perhaps three because Acantholingua ohridana might be transferred to Salmo (Crespi and Fulton 2004) as done by Kottelat and Freyhof (2007). Obviously, there is need for revision of the genus. Most of the variants listed by Kottelat and Freyhof (2007) are morphologically similar to forms we have seen in Norwegian waters where most populations are younger than ca.10,000 years. A genetic species concept may be the only useful theory in future revisions of the genus. Populations have been geographically isolated for some time and some developed special features specific to the population (Skaala et al. 1991). These are variations which can be consequences of mutations, natural selection and random phenomena such as genetic drift in addition to direct environmental effects. In some cases, there is more than one population in the same lake but spawning occurs in different areas (Ryman et al. 1979; Ferguson 2006). This may be due to a specific homing tendency together with trophic specialization and assortative mating. The different variants may have evolved within the systems, similar to what was suggested for other salmonids such as Arctic charr (Jonsson and Jonsson 2001) but can also be the result of sequential invasions into the system (McKeown et al. 2010). The one hypothesis does not preclude the other.
2.3 The Species Our view on the taxonomy of the genus Salmo is conservative. The reason is that these species are highly variable within and among localities even within limited geographical areas. This has made us often regard systematic splitting, such as that by Kottelat and Freyhof (2007), erroneous. Frequently, splitters base their view on incomplete and sometimes accidental species descriptions, often interpreted differently than what the authors of the original descriptions did. Thus, we consider two species, Salmo salar and Salmo trutta, but leave open the possibility of other species in the genus.
2.3.1
Atlantic Salmon
Atlantic salmon is recognized as a monophyletic unit distinct from the evolutionary lineages of other salmonid fish. But the phenotypic variability of Atlantic salmon is considerable. This has long been known. For instance, in 1599, a Norwegian
2.3 The Species
41
clergyman, Peder Claussøn Friis, wrote that each river supports a specific type of Atlantic salmon even in cases where the river mouths are only a bowshot apart (Storm 1881). This variation is not only in body form, growth rate and adult size, but also in characters such as spawning colours, distance migrated and time of migration and spawning. Most Atlantic salmon populations are anadromous but non-anadromous populations occur in both Europe and North America. Non-anadromous Atlantic salmon have a polyphyletic origin in different river systems, with independent evolution in different rivers. Often, the populations have been geographically separated for thousands of years, and during this period, they have sometimes evolved a high degree of genetic divergence (King et al. 2007). Although the level of genetic diversity is much greater in anadromous than non-anadromous populations (Tonteri et al. 2007), the genetic diversity among non-anadromous salmon still represents a large part of the genetic diversity of the species. Different levels of long-term gene flow between anadromous and non-anadromous populations seem to have lead to this difference in diversity. The reduced opportunities for gene flow between the non-anadromous populations make them more vulnerable to extinction following a population crash than the anadromous stocks. For instance, the non-anadromous Atlantic salmon in Lake Byglandsfjord probably persists, thanks to a long series of habitat improvements, liming included, and stocking (Barlaup et al. 2005), because without aid, wild conspecifics cannot reach the locality. The genetic population differentiation among regions has probably originated from geographic isolation for long periods of time with little or no gene flow between them. A large part of the molecular variation appears to be the result of stochastic processes such as genetic drift, the mixing of populations through the Pleistocene and recent postglacial colonizations. Early immigrants may have become landlocked associated with physical changes in the rivers, such as the postglacial isostatic rebound of the landscape, as the ice disappeared. Also, some of the early anadromous populations may have been temperately landlocked during a cold period while freshwater was still suitable for salmon and while cold sea temperatures limited the profitability of the marine migration. Later, some of them may have retained their freshwater resident behaviour even in cases when the migratory barrier disappeared. Berg (1985) suggested that non-anadromous Atlantic salmon in Europe developed in a cold period during the younger Dryas period, starting 11,000 years BP. For a long time, anadromous and non-anadromous Atlantic salmon were considered two separate subspecies, Salmo salar salar L. and S. salar sebago Girard. The latter is named after Sebago Lake, the second largest lake in Maine, USA, which supports a population of non-anadromous Atlantic salmon. However, since Wilder (1947) showed no consistent difference in morphology and meristic characters between the two forms, the species has been considered monotypic. Furthermore, anadromous populations have mature parr, which spawn without having been to sea, similar to the freshwater resident form. Also, since the two forms have overlapping and not disjunctive distribution areas, it seems taxonomically wrong to allot the Atlantic salmon populations to these two subspecies (cf. Mayr 1969).
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2 Species Diversity
Phenotypic divergences can be shaped by environmental conditions, particularly early in life. For instance, fin length and body of parr can differ between groups reared in water with different flow velocity. According to Paez et al. (2008), parr living in faster-flowing water exhibit a more robust body shape than conspecifics in slower-flowing water. Pakkasmaa and Piironen (2000) reported that a difference in body shape can be seen after only 1 month in water with differing flow velocities. Mature male parr are more robust in body shape than corresponding immatures irrespective of whether they live in lotic or lentic habitats. Through discriminant function analysis, Von Cramon-Taubadel et al. (2005) found a strong environmental effect on the body form of salmonid parr. Atlantic salmon parr grown from embryos with a nonsibling group in a hatchery environment came to resemble the body shape of their hatchery host more closely than that of their full siblings, grown in the natal stream habitat. Furthermore, wild smolts differed in shape from cultured offspring, but this difference was less pronounced, although still significant, when the hatchery fish were released in nature and captured after 1 year of free swimming at sea. Thus, rearing conditions have significant effects on fish body shapes, and some such differences disappear with time when the divergent groups are brought together in a common environment. Such environmental impacts can at least partly explain differing morphology as observed between wild and hatchery-reared salmonids (Fleming et al. 1994). Phenotypic variation in Atlantic salmon is also partly genetic. Fraser et al. (2007) found genetically based morphological differences between a short- and long-distance migratory population from the same latitude in New Brunswick, Canada. The short-distance migrants exhibited a less streamlined body shape with a shorter caudal peduncle than the long-distance migrants. Hybrids showed intermediate traits. Furthermore, body size of North American Atlantic salmon was found to increase in relation to upriver distance to the spawning grounds (Schaffer and Elson 1975), and the body forms of the smolts seem adapted to the environmental conditions of the fish (Riddell and Leggett 1981). Also, there is genetic variation for ecological characters such as age and size at sexual maturity (Saunders 1981; Gjerde et al. 1994) and timing of the return migration of the adults (Hansen and Jonsson 1991; Jonsson et al. 2007). Invasion of fish from another population, whether these are natural strays or hatchery-reared conspecifics, may, therefore, affect the fitness of the adapted population (McGinnity et al. 2003, 2004). Problems related to intraspecific hybridization are discussed in Chaps. 10 and 11. It is difficult to demonstrate that natural selection is responsible for adaptive traits within populations and to detail the nature of the selective mechanism that has favoured such traits (Futuyama 1986). To be regarded as an adaptation, it must be a derived character, which evolved in response to a specific selective agent (Harvey and Pagel 1991). However, significant correlations between ecological traits and environmental variables, which also hold good when reared in common environments, can be traits adapted through natural selection (Jonsson et al. 1991, 2001; Gjerde et al. 1994). Morphological and meristic variability linked to migratory distance in the natal and spawning habitat and variation in spawning time may be examples of such traits (Riddell and Leggett 1981; Riddell et al. 1981; Heggberget 1988).
2.3 The Species
2.3.2
43
Brown Trout
The systematic status of brown trout is under continuous discussion, not the least because there have been several ice ages with repeated opportunities for genetic divergence in allopatric refuges followed by interbreeding. There have also been varying degrees of reproductive isolation among populations on secondary contact after postglacial colonization (Bernatchez 2001; McKeown et al. 2010). Although the consensus is that postglacial colonization involved multiple lineages originating from separate refuges, hypotheses differ in terms of the number, origin and dispersal dynamics of these lineages. Therefore, the phylogeography is still far from being resolved (e.g. Hamilton et al. 1989; Hynes et al. 1996; García-Marín et al. 1999; Weiss et al. 2000; Cortey et al. 2009; Vera et al. 2010). After the last glaciation period, brown trout invaded streams, lakes and coastal areas. They appear to adapt morphologically to the nature of their trophic habitat and are sometimes categorized accordingly as Salmo trutta forma fario, Salmo trutta forma lacustris and Salmo trutta forma eriox (cf. Sect. 2.2.5). For instance, the stream form, fario, has darker sides with parr marks along their flanks and white leading edges followed by black on the anal and dorsal fins. The lake-living form, lacustris, has a slimmer body shape, lighter more silvery-coloured sides, and they often lack the white edge of the anal and dorsal fins (Alm 1949). The anadromous form, eriox, is even slimmer and the flanks and belly of immature fish are silvery, like herring. However, the names of the forms have no taxonomic meaning, since they are related to feeding habitat and not to reproductive isolation or geographical distribution. This does not mean, however, that their differences have no genetic basis. On the contrary, Alm (1939, 1949) showed that both the smaller maximum body size and the white edges of the fins of the stream form, fario, were inherited traits, distinguishing it from the lake living form, lacustris. This is also the case with the different migratory tendencies of andromous and non-anadromous brown trout from the same river (Jonsson 1982) and among anadromous populations from different rivers (Svärdson and Fagerström 1982). On the local scale, there are genetic differences between populations in different drainages, rivers and spawning sites due to the strong homing instinct and geographical barriers among populations. Thus, the same brown trout morph in different localities is usually similar, but genetically quite different, and different morphs in the same river can be externally different but in some cases genetically similar and in others different. This depends on the degree of reproductive isolation between the morphs (Skaala and Nævdal 1989; Hindar et al. 1991; Cross et al. 1992). It has long been known that brown trout return to their home river for spawning (Stuart 1953, 1957) and that the populations feeding in the same lake can spawn in different tributaries (Jonsson 1985), different parts of the same tributary (Bagliniére et al. 1989; Skaala and Nævdal 1989), tributaries and lake (Andersen 1982) and inlet and outlet rivers (Skurdal and Andersen 1985; Jonsson et al. 1994). Genetic studies by Allendorf et al. (1976) and Ryman et al. (1979) revealed that such sympatric populations can be reproductively isolated, even in small systems such as the
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Swedish mountain lake Bunnersjöarna with a surface area of 0.5 km2. The two sympatric populations of brown trout feeding in the lake exhibited different growth rates. Even more extreme is the situation in Lough Melvin, northwest Ireland. There, Ferguson and Mason (1981) and Ferguson and Taggart (1991) demonstrated at least three partly reproductive isolated ecotypes of brown trout. The local names of the variants are gillaroo, sonaghen and ferox trout. They exhibit different morphology (Cawdrey and Ferguson 1988), food preferences (Ferguson 1986) and spawning areas. For instance, the fish-feeding ferox trout spawned in the lower and deeper sections of one of the tributaries, and the zooplankton-feeding sonaghen spawned farther upstream in the same tributary. Current evidence indicates that the gillaroo and sonaghen sympatric types diverged prior to the colonization of Lough Melvin, and, although limited gene flow has occurred since secondary contact, they have remained largely reproductively isolated due to inlet and outlet river spawning segregation (McKeown et al. 2010). Also, other sympatric morphs of brown trout have been found, such as the Irish Lough Neagh, where two reproductively isolated populations occur (Crozier and Ferguson 1986). Probably, such reproductively isolated sympatric brown trout populations are common, although not so often demonstrated by genetic investigations (Allendorf et al. 1976; Sušnik et al. 2005; Duguid et al. 2006). The reason is that it is difficult to reveal such differences unless there are fixed or large differences in allele frequencies among them. Jorde and Ryman (1996) reported that it took several years of investigation before they eventually showed that two of their study lakes supported multiple genetically isolated, co-existing populations of brown trout. In the nineteenth century, anadromous and non-anadromous brown trout were distinguished as separate species. Dahl (1904), however, observed that inland trout could move downstream and develop into sea trout, and Regan (1911) maintained that anadromous and inland trout were freely interbreeding fractions of a single species. Moreover, Rounsefell (1958) reported that anadromous brown trout released in rivers in North America gave rise to both anadromous and non-anadromous progeny. Further, Skrochowska (1969) demonstrated experimentally that anadromous as well as non-anadromous parents produced both resident and anadromous offspring, although the proportion of anadromous offspring was higher for anadromous than for non-anadromous parents. Also, within single systems, anadromous and non-anadromous trout can spawn together as observed in the field, and demonstrated by population genetic studies (Jonsson 1981, 1985; Hindar et al. 1991; Cross et al. 1992; Petersson et al. 2001). As in Atlantic salmon, characters such as migratory direction of offspring of up-stream and down-stream spawning brown trout, relative to a lake, are genetically influenced as are adult size and age at maturity (Jonsson 1982, 1989; Jonsson et al. 1994). The same holds for morphological differences between trophic variants such as those described from Lough Melvin (Ferguson 1986; Cawdrey and Ferguson 1988). Similar trophic specialization is observed in other salmonid species such as whitefish (Østbye et al. 2005a, b; Derome and Bernatchez 2006) and Arctic charr (Hindar and Jonsson 1982, 1993; Snorrason et al. 1994; Klemetsen et al. 2003). The feeding specialization can have occurred within their respective habitats through
2.4 Geographical Distributions
45
natural selection without geographical isolation (Jonsson and Jonsson 2001). Also in Pacific salmon and trout, there are examples of local adaptations for characters such as spawning time (Ricker 1972; Quinn et al. 2000) and migratory tendency (Brannon 1972; Northcote and Kelso 1981). But there is a need for more exact studies on contrasting populations of the same species for a more detailed knowledge about this phenomenon.
2.4 Geographical Distributions Atlantic salmon and brown trout are native to the northern hemisphere, but have been widely introduced for aquaculture, commercial and recreational fisheries in cold waters around the world. Therefore, their present distributions are larger and widely affected by human activities.
2.4.1
Atlantic Salmon
Atlantic salmon have a wide distribution area (Fig. 2.6) and are divided into three main groups, the West Atlantic group spawning in the rivers in North America, the east Atlantic group spawning in the rivers in West Europe and the Baltic group spawning in rivers around the Baltic Sea. This grouping builds on consistent genetic and geographical separation (Verspoor et al. 2007).
2.4.1.1
Genetic Diversity
The largest genetic difference is between the East and West Atlantic salmon, which were separated more than 0.5 million years ago (King et al. 2007). All three groups exhibit further regional divisions, probably because subgroups survived in different ice-free refuges during long periods of time during successive glaciations. For instance, the east Barents Sea populations appear to cluster genetically together with the northwest European populations whereas the White Sea and east Barents Sea populations are divided in three other clusters (Tonteri et al. 2009). The north Russian anadromous populations exhibit greater genetic variability than the Baltic populations. Among non-anadromous Atlantic salmon, the Baltic populations are genetically more heterogeneous than the north Russian populations. Within the Baltic Sea, the anadromous populations form three groups, one in the Gulf of Bothnia, one in the Gulf of Finland and one in the Baltic Maine Basin (Säisä et al. 2005). The isolation by distance model can explain a part of the differentiation within but not among groups, indicating colonization of the Baltic Sea by at least three lineages originating from different glacial refuge areas.
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Fig. 2.6 Endemic distribution of Atlantic salmon (From MacCrimmon and Gots (1979). Reproduced with permission of the Minister of Public Works and Government Services Canada)
2.4 Geographical Distributions
47
Within regions, the population structure of the species depends on habitat conditions. For example, peripheral populations typically exhibit lower genetic diversity and greater genetic differentiation as a consequence of smaller effective population size and greater geographical isolation relative to geographically more central populations (Eckert et al. 2008). Migration between populations is affected by a range of factors including: geographical characteristics of the habitat (Miller and Ayre 2008) and dispersal capacity of juveniles and/or adults (Derycke et al. 2008). Behavioural traits, such as homing or instinct to return to the natal area for spawning, can also play a significant role. The West Atlantic fish have fewer alleles and fewer unique alleles than the East Atlantic race. This is probably due to differing glacial histories. The North American range was glaciated more recently and the ice cover was more uniform than that in the European range. The East and West Atlantic salmon differ in number of chromosome pairs and arms. West Atlantic salmon usually exhibit 27 chromosome pairs with 72 chromosome arms, whereas the East Atlantic populations typically have 29 chromosome pairs with 74 chromosome arms (Hartley 1987). Based on allozyme loci differences, the intercontinental divergence across the Atlantic is approximately four times greater than the variation among Atlantic salmon found in North American rivers and about twice as large as the variation among European rivers (Verspoor 2005). Studies of mitochondrial DNA have revealed that this intercontinental difference accounts for about 45% of the total genetic variance in Atlantic salmon. Of the remaining variation, 22% is distributed among samples within regions and continents and 33% among individuals within populations (King et al. 2007). Together, these and other genetic investigations illustrate the deep phylogeographic division between European and North American Atlantic salmon. In North America, regions such as Labrador, Newfoundland, the Gulf of St. Lawrence, the Bay of Fundy and Maine represent distinct phylogeographic groups and about 11% of the genetic variance is due to differences among provinces (Verspoor 2005). In Europe, the most striking phylogeographic division is between Atlantic salmon in the Baltic Sea and in the Atlantic Ocean drainages (Ståhl 1987; King et al. 2007); mtDNA data indicate that a little less than 30% of the genetic variance in Europe is due to differences between Atlantic and Baltic populations. There are also subgroupings within these regions, for instance, between Iceland/ Greenland, northern Russia/Norway, south Norway/western Sweden, the northern British Isles, the southern British Isles/northern France and the southern France/ Spain (King et al. 2001).
2.4.1.2
Anadromous Populations
Europe East Atlantic salmon is distributed from Petchorskaya in the northeast, to the Baltic in the east, to the River Minho, north Portugal in the south where a small population
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still exists. They are distributed to Greenland in the west. In the ocean, they migrate as far north as Svalbard (81°N). Anadromous populations are threatened and disappearing in the southern part of the native range. Threats are pollution, dam building, water and substrate removal and increasing water temperature due to climate change (Klemetsen et al. 2003; Webb et al. 2007). From the Portuguese border to the French Pyrenees, there are numerous rivers where the population is endangered due to habitat loss, overexploitation or global climatic change (Dumas and Prouzet 2003). Earlier, the population in the Douro River was recognized as the southernmost stock in Europe. This is now extinct. Spanish salmon populations suffered a severe demographic decline in the 1970s and were exterminated in many rivers. Only four Spanish rivers are currently not considered vulnerable (Sella, Narcea, Deva and Bidasoa) (WWF 2001). French Atlantic salmon have disappeared from almost all large French rivers except for the Allier (Loire), Gave d’Oloron, Nive and Nivelle rivers and the streams of the Massif Armoricain (Brittany and Normandy) (Prouzet 1990). In Belgium, the Netherlands, Germany and Switzerland, all previous Atlantic salmon populations were lost by 1960 (WWF 2001). Now, there are efforts to reintroduce salmon to some rivers, such as the Meuse and Rhine, through stocking and rehabilitation programmes, which recently have started to produce results. The situation for Atlantic salmon in the Baltic region is also very serious with a decline in production of wild smolts estimated at approximately 95% during the twentieth century (WWF 2001). At present, however, there are positive signs indicating a slight increase in natural production of Baltic salmon (Anonymous 2008a). In Denmark, the status for Atlantic salmon is poor with natural production chiefly in three of the former nine salmon rivers. The situation in England and Wales appears less serious although populations are in decline overall (Joint Nature Conservation Committee 2007). In Ireland (Anonymous 2006), Scotland (Anonymous 2008b), Iceland (Guðbergsson 2007) and Norway (DN 2009), stocks are healthier, although population abundances, particularly in the southern part of this area, have decreased due to low sea survival in recent years (Jonsson and Jonsson 2004). In Russia, the status of Atlantic salmon in most rivers is unknown. The general distribution of Atlantic salmon in East Atlantic is similar to that of anadromous brown trout, except that the salmon migrate farther to sea. North America West Atlantic salmon are naturally distributed from the Hudson Ungava Bay (59°N) in the north to Lake Ontario in the west and southwards to the Connecticut River. It occurred along the east coast in the Bay of Fundy between New Brunswick and Nova Scotia, in the Gulf of St. Lawrence and along the coast of Newfoundland and Labrador to the Fraser River. More isolated populations occurred farther north in the Ungava Bay and in the Kogaluk River on the east side of the Hudson Bay. At sea, they move eastwards at least to West Greenland. In Greenland, Atlantic salmon spawn in the Kapisigdlit River at the head of the Godthåb Fjord, and it occurs
2.4 Geographical Distributions
49
northwards from Kap Farvel to Umanak on the west coast (70˚ N) (Reddin and Shearer 1987), and Angmaksralik on the east coast (Webb et al. 2007). Historically, Atlantic salmon occurred naturally in most watercourses from northern Quebec to the Long Island Sound, New York State (41°N) north of the Hudson River. It has been debated whether it also occurred in the Hudson River. Strays from neighbouring rivers, such as the Connecticut River, have been caught there and eggs from the Penobscot River were stocked there in 1880 (Zeisel 1995). But the Hudson River has probably never had a self-sustaining natural population of Atlantic salmon (Limburg et al. 2006). Although Canada still has river systems with healthy populations, mainly in remote locations where human activity is minimal, most North American Atlantic salmon stocks are in various stages of decline, particularly in the Bay of Fundy and USA (Klemetsen et al. 2003). Of 50 historical populations on the east coast of USA, 42 have been extirpated, and the remaining eight are in critical condition. There are probably several reasons for the decline such as acidification of water courses, releases of the predator, striped bass [Morone saxatilis (Walbaum)], climate change, fishing and river regulations.
South America Atlantic salmon occur in the Pacific Ocean along the west coast of North and South America from Chile to Alaska as a consequence deliberate fish releases and escapes from fish farms. An individual has been captured as far north as the Bering Sea (Brodeur and Busby 1998). But, there is no known self-sustaining anadromous population in rivers draining to the Pacific Ocean.
2.4.1.3
Non-anadromous Populations
Europe In Europe, there are non-anadromous Atlantic salmon populations in 14 river systems (Kazakov 1992). In 11 of these, the salmon production is associated with lakes (Webb et al. 2007). They are found in Lake Vänern, Sweden and Lake Saimaa, Finland. In Russia, they are found in the lakes Ladoga and Onega and a number of systems in the Russian Karelia-White Sea area such as Pista, Lizhma, Kem and Vig rivers. Non-anadromous populations of Atlantic salmon often, but not always, inhabit both rivers and lakes, above waterfalls impassable for anadromous fish (Kazakov 1992). The number of European populations of non-anadromous Atlantic salmon is decreasing. For instance, of four Norwegian populations found at the beginning of the twentieth century, only two small populations are left, one in the River Namsen (Berg and Gausen 1988), and one in the River Otra with Lake Byglandsfjord (Nilsen et al. 2003); the latter population is supported by stocking. The extinct population in the River Nidelva expired due to acidification of the water in the
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twentieth century. The population that spawned in the River Trysilelva, downstream of Lake Femund, disappeared due to dam-building in downstream areas in Sweden. Lake Vänern was the main feeding area for the fish, and the Swedish hydropower constructions prevented the fish from returning to the spawning grounds in the upper part of the River Trysilelva. However, in this river, a population still persists on the Swedish side of the border (Ros 1981). Non-anadromous Atlantic salmon have also been lost from Lake Imandra on the Kola Peninsula in Russia.
North America Non-anadromous populations are more numerous in eastern North America than in Europe (Webb et al. 2007). Non-anadromous salmon are found from Lake Ontario eastwards to Newfoundland, North Quebec and Ungava Bay. They are numerous in Newfoundland, eastern Quebec and Labrador. In several cases, anadromous and non-anadromous salmon exist together although there is no barrier against migrations to the sea (Verspoor and Cole 2005). Non-anadromous Atlantic salmon have been widely stocked in rivers in the state of Maine where they thrive. Originally the salmon occurred in four lakes in Maine but is now found in hundreds of lakes in this state. Thus, the higher frequency of non-anadromous Atlantic salmon populations in North America than in Europe seems partly due to North American stockings but may also indicate that the fitness advantage of moving to sea is higher in Europe than in North America. An additional point may be the earlier invasions of Atlantic salmon in Europe than in North America, leaving a longer time for populations to go extinct in Europe.
South America and Australia There are self-sustaining non-anadromous Atlantic salmon in lakes in Chile and New Zealand as a result of fish stocking (MacCrimmon and Gots 1979; Soto et al. 2001; Pascual et al. 2002). Obviously, it is easier to establish freshwater residents than anadromous populations of the species.
2.4.2
Brown Trout
Brown trout is polyphyletic and consists of a number of highly divergent evolutionary lineages. These originate from the many glacial refuges in Europe where major evolutionary lineages of the species evolved and post-glacially spread naturally as the water courses became available when the ice-cap retreated. However, the present biogeography of the species is also heavily influenced by introductions performed over large parts of the world in the nineteenth and twentieth century.
2.4 Geographical Distributions
2.4.2.1
51
Genetic Diversity
Four of the evolutionary lineages of brown trout are located to the Danubian, Adriatic, Mediterranean and Atlantic drainage basins. There is a fifth divergent lineage represented by the morphologically distinct marbled trout occurring in headwater systems of the Adriatic (Bernatchez et al. 1992). These lineages are described as the basic evolutionary significant units (ESUs) of brown trout by Bernatchez (2001). Within the lineages, there is a mosaic of smaller genetic differences. This fact is based on analyses of mitochondrial and nuclear DNA (Bernatchez et al. 1992; Bernatchez 2001; Giuffra et al. 1994, 1996; Bernatchez and Osinov 1995; García-Marin and Pla 1996; Antunes et al. 1999, 2006; Apostolides et al. 2007). In the northern species range, one evolutionary lineage, often referred to as the Atlantic race, appears to be the predominant evolutionary lineage. However, McKeown et al. (2010) postulated even more glacial refuges and suggested that Britain and Ireland alone were postglacially colonized by brown trout from at least five refuges located at: (1) south of England – western France, (2) east of the Baltic Sea, (3) western Ireland, (4) the Celtic Sea, (5) the North Sea. They based their view on analysis of four mitochondrial DNA segments from 83 sites and published literature. The admixture among ancestral clades is extensive throughout the studied area, and some populations contain mixtures of highly divergent clades. The discussions about postglacial immigration and origins of different brown trout clades are not yet settled and will most probably be revised as more material and techniques become available. 2.4.2.2
Dispersal
Natural Distribution By origin, brown trout is chiefly a European species (Fig. 2.7). The early distribution of brown trout is believed to have extended from Iceland, northern Scandinavia and Northwestern Russia southwards to the northern limits of the Mediterranean Sea, the islands of Corsica, Sicilia and Sardinia and the Atlas mountains in Morocco and Algeria, northern Africa. The distribution extended eastward from the Atlantic drainage towards the Ural Mountains and the upper reaches of the Orontes Rives in Lebanon and the northern slopes of Himalayas, Armenia and Afghanistan. Migratory brown trout inhabited the Black, Caspian and Aral Seas and their tributaries (MacCrimmon and Marshall 1968; MacCrimmon et al. 1970; Elliott 1994). In the Atlantic basin, anadromous brown trout occurred from the White Sea and Cheshkaya Gulf, Iceland, Baltic Sea, Irish Sea to south of the Bay of Biscay, northern Portugal. Human Introduction Brown trout have been widely spread by humans. For several thousands of years, the fish were spread to high elevation localities, which they were unable to reach by themselves. Its area was further increased by introductions to countries beyond
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Fig. 2.7 Spatial distribution of brown trout (hatched area). Broken line gives distribution of anadromous populations
its native range. In fact, the dissemination of brown trout in the past 150 years has been so complete that most areas of the world capable of supporting brown trout have received introductions. However, its range is fragmented on all continents where the species has been introduced. International introductions commenced with the transfer from England to Tasmania in 1864 (Frost and Brown 1967; MacCrimmon and Marshall 1968; MacCrimmon et al. 1970; Lake 1971). From a slow start with a release of about 300 offspring of the populations in the rivers Wey and Itchen, UK, it was spread to most waters of Tasmania. From Tasmania, it was further spread to locations above 600 m in Victoria and New South Wales in Australia, and Papua New Guinea. Furthermore, Tasmanian brown trout were exported to the South Island, New Zealand around 1870, and to the North Island in the 1880s (McDowall 1978). From New Zealand, the species was introduced to Fiji where a self-sustaining population was established in 1970. Brown trout were imported in South Africa from the UK in the last quarter of the nineteenth century with transfers from 1890 onwards, which produced viable populations in high elevation streams. From South Africa, successful transfers were made into Malawi, Swaziland and Zimbabwe where the species now occurs in high elevation streams. Plantings in Tanzania were performed in 1934 but continued
2.4 Geographical Distributions
53
releases were considered necessary to maintain the species and in this country. It is questionable whether any self-sustaining population has been established. Brown trout were introduced to Kenya from the UK in 1921 and reintroduced in 1949, and then transferred from Kenya to Ethiopia in 1967. Madagascar received brown trout from France in 1926, and naturalized populations were established in streams higher than 1,700 m above sea level. In Asia, brown trout were brought to India from the 1860s onwards. The success of the early stocks was variable, but an introduction to the Kashmir Valley in 1889 was most successful. Brown trout from Kashmir were distributed to other parts of northern India, Pakistan, Nepal and Bhutan during the twentieth century (MacCrimmon and Marshall 1968). Brown trout were also introduced to western and northern Pakistan from Europe early in the twentieth century (Lone 1983; Ahmad and Niazi 1988; Naveed 1994). Brown trout established self-sustaining populations at high elevations in Sri Lanka. There, fish both from Europe and India have been released. In the 1890s, brown trout were introduced to Japan from North America and it occurs now in 42 rivers in Hokkaido (Hasegawa and Maekawa 2006). Stocked brown trout were also released in Iranian rivers, and the genetics of brown trout in these rivers appear quite different from that of brown trout in the Caspian Sea (Novikov et al. 2008). Several plantings of fertilized brown trout eggs were made in North America during the 1880s and 1890s. The eggs originated from Germany and Scotland (Loch Leven) (MacCrimmon and Marshall 1968). By 1967, brown trout had been introduced into 45 of the 50 states, and naturalized populations occurred in 34 states. Loch Leven trout were introduced to Canada in the 1880s. Canada also received German brown trout from USA at about the same time. The species is now established in nine of the ten Canadian provinces. In South America, brown trout were successfully released in Argentina and Chile in the twentieth century. The fish came from both USA and Europe. In Argentina, it formed self-sustaining populations in nearly all rivers and large lakes of the Patagonian Steepes. In Chile, it established self-sustaining populations over a large area between 19°S and 55°S. In 1928, it was introduced to Peru, where it formed self-sustaining populations at elevations higher than 2,500 m above sea level. Brown trout were transferred to Columbia from the UK in 1892, and it was translocated to Bolivia from the USA in 1939. Now, it occurs in high Andean streams and in Lake Titicaca situated 3,812 m above sea level. Also, brown trout were transferred from Chile to Equador in the 1950s (MacCrimmon and Marshall 1968; MacCrimmon et al. 1970; Elliott 1989). Altogether, this means that self-sustaining populations of brown trout have been established due to human transfers in at least 26 countries beyond its native range. Improved angling opportunities have been the purpose of most known brown trout introductions, and in some countries such as Peru, it has become an important fishery resource. Brown trout readily invade, thrive, and establish self-sustaining populations given that the environmental conditions are suitable. The species is thus considered one of the world’s 100 most invasive alien species. It is blamed for reducing native fish populations, especially other salmonids due to predation,
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displacement and food competition (Lowe et al. 2000), in addition to restructuring invertebrate communities (Townsend 1996). By that, brown trout have suppressed grazing pressure from invertebrates and are responsible for enhancing algal biomass and changing algal species composition. Brown trout are carnivores and tend to dominate fish communities in cold, clear stream localities. Townsend (2003) reported that in New Zealand’s brown trout streams, essentially all annual production of invertebrates is consumed by this fish, with a considerable increase in algal primary productivity as the result. This leads, in turn, to an increased flux of nutrients from the water to the benthic community. The trout invasion has led to strong top-down control of community structure and ecosystem functioning via its effects on individual behaviour and population distribution and abundance. Furthermore, with the translocations of brown trout from Europe to North America, the fish have brought whirling disease caused by the micro-parasite Myxobolus cerebralis. Rainbow trout and other Pacific salmonids are sensitive to this parasite. It has been implicated in population declines and the elimination of local salmonid year-classes where it has become established (Nehring 1996; Vincent 1996). This consequence of increasing the distribution of brown trout is further discussed in Sect. 10.4.4.
2.4.3
Habitat Constraints
Water temperature is probably the most limiting factor for the geographical distributions of Atlantic salmon and brown trout (MacCrimmon and Marshall 1968; MacCrimmon and Gots 1979; Elliott 1994). Limits for growth of the species are approximately 5–25°C (Elliott 1982; Jonsson et al. 2001; Forseth et al. 2009), and the upper limit for survival is between 25° and 30°C with a little higher temperature for Atlantic salmon than brown trout. Limits for embryo development are narrower at about 0–15°C (Elliott 1981; Crisp 1981). Thermal limits are presented in more detail in Sect. 4.2. The oxygen content of the water also influences salmonid success. Free swimming trout tolerate oxygen concentrations down to 5–5.5 mg l−1. According to Mills (1971), oxygen saturation in the water should exceed 80%. During incubation, the embryos need high oxygen concentration in the water. The intergravel water flow rate through the redd containing embryos should be above 9 mg l−1. Silt and low water velocity reduce embryo survival, and absence of satisfactory spawning grounds, which often is the case in low-land reaches of streams, reduces and even prevents offspring survival (Elliott and Hurley 1998; Soulsby et al. 2001; Wood and Budy 2009). Most water courses with Atlantic salmon and/or brown trout are oligotrophic. However, both species will survive in quite nutrient-rich, productive systems given suitable spawning grounds. Sporadic flooding, poor feeding opportunities and high predation intensity can prevent establishment of the species in new habitats. Furthermore, human activities in the watershed can influence the success of the species. Such activities are agricultural land-use, building of impoundments, transfer
2.5 Summary
55
of water from the river, drainage works, land improvements, afforestation, deforestation, overfishing and overstocking (Elliott 1994; Northcote and Hartman 2004). For instance, most wild populations of Atlantic salmon and brown trout in the northern Baltic were lost because of damming of rapids, damage to nursery areas and overexploitation (Jutila et al. 2006; Siira et al. 2006). Poor water quality is another cause of population extinction. Episodes of acidified surface water during the twentieth century decreased salmonid production in northern Europe and North America (Clair et al. 2004; McCormick et al. 2009). As one of the major producers of wild Atlantic salmon in the world, Norway lost approximately 25% of its natural production of this species due to acidification during the twentieth century (Hesthagen and Hansen 1991; Sandøy and Langåker 2001). Atlantic salmon is more susceptible to acid water than brown trout. To maintain viable populations, the pH of the water should be between 6 and 9. Negative effects have been observed even at pH 6.3, and the effect increases with increasing aluminium concentration in the water (Rosseland and Skogheim 1984; Skogheim and Rosseland 1984; Fivelstad and Leivestad 1984; Norrgren and Degerman 1993; Herrman et al. 1993). A pH below approximately 5.5 decreases the hatching success of brown trout, and few populations exist in lakes where the pH is below 5.0 (Norrgren and Degerman 1993; Hesthagen and Jonsson 1998). Smolt is the most sensitive life stage (Rosseland et al. 1986). The fish die due to failure in ionic regulation, acid–base regulation, circulation and respiration. Of these, the first and last are held to be the primary causes of fish death in acid- and aluminium-rich water (McDonald et al. 1983; Exley and Phillips 1988; Berntssen et al. 1997). All in all, this shows that there are both natural and anthropogenic limitations for success of Atlantic salmon and brown trout. More detailed habitat requirements are described in Chap. 3. Since water temperature is a major factor constraining their ranges, we predict a gradual change in the area of the species owing to the predicted climate change (see Chap. 9). As a consequence of the increasing farming of Atlantic salmon in the Pacific Ocean, Atlantic salmon may, with time, colonize rivers outside the Atlantic drainage (see Chap. 10).
2.5 Summary 1. Atlantic salmon and brown trout belong to the Salmoninae, one of three subfamilies of the Family Salmonidae. Whether or not these two are the only species of this subfamily is hotly debated, and there is an urgent need for a revision of the systematics of the Salmoninae. 2. Evidence suggests that the Salmonidae originated in freshwater and evolved through gene duplication and genome duplication between 50 and 100 million years BP. The oldest known salmonid fossil is Eosalmo driftwoodensis. This is a Thymallus-like freshwater fish, which lived in northwestern North America ca. 50 million years ago. The anadromous habit may have evolved before the family originated.
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3. Atlantic salmon is recognized as a monophyletic taxon distinct from the evolutionary lineages of other salmonid fish. Brown trout is polyphyletic with several distinct types. The divergence of the types was probably quite recent and they are viewed as parts of the Salmo trutta species complex. It is uncertain how many species there are in the genus Salmo. 4. Atlantic salmon is more migratory than brown trout, and it is naturally distributed on both sides of the Atlantic drainage. It is a poor colonizer and has difficulty establishing populations outside its original distribution range. Brown trout are naturally distributed in the East Atlantic. However, it is one of the world’s most invasive fish species, has been transferred by humans to at least 26 countries outside its original range and is now present in all major parts of the world except the Antarctic regions. 5. Brown trout are more inclined to form freshwater resident populations than Atlantic salmon. Freshwater resident populations of Atlantic salmon are quite rare in Europe, less so in North America. 6. Both species tolerate water temperatures between approximately 0–25°C, and temperature is viewed as the main abiotic factor limiting their distribution. The geographic distribution of anadromous populations towards the north and south were similar until human releases of fertilized fish eggs and hatchery fish commenced near the middle of the nineteenth century. 7. Both species are oxygen demanding and require gravel bottoms with high water flow through for spawning. Atlantic salmon are more sensitive to acid water than brown trout. The former are negatively influenced by acid water as low as pH of 6.3. The comparable pH for brown trout is 5.5.
References Ahmad MF, Niazi MS (1988) Important edible fishes of Pakistan. Zoological Survey Department, Government of Pakistan, Karachi Allendorf FW, Thorgaard GH (1984) Tetraploidy and the evolution of salmonid fishes. In: Turner B (ed) Evolutionary genetics of fishes. Plenum, New York Allendorf FW, Ryman N, Stennek A et al (1976) Genetic variation in Scandinavian brown trout (Salmo trutta L.): evidence of distinct sympatric populations. Hereditas 83:73–82 Alm G (1939) Undersökningar över tillväxt m.m. hos olika laxöringformer [Investigations on growth etc. by different forms of trout]. Rep Swed State Inst Freshw Fish Res 15:1–93 Alm G (1949) Influence of heredity and environment on various forms of trout. Rep Inst Freshw Res Drottningholm 29:29–34 Andersen R (1982) Lake spawning brown trout Salmo trutta and arctic char SaIvelinus alpinus with common spawning area in Lake Selura, southwestern Norway. Fauna 35:162–168 Anonymous (2006) The status of Irish salmon stocks in 2005 and precautionary catch advice for 2006. Report of the Standing Scientific Committee of the National Salmon Commission, Ireland Anonymous (2008a) Report of the Baltic salmon and trout assessment working group. ICES CM 2008/ACOM:05 Anonymous (2008b) Statistical bulletin: Scottish salmon and sea trout catches, 2007. Fisheries series, No. Fis/2008/1, Aberdeen
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Reshetnikov Yu S, Bogutskaya NG, Vasileva DE et al (1997) An annotated checklist of the freshwater fishes of Russia. J Ichthyol 37:687–736 Ricker WE (1972) Hereditary and environmental factors affecting certain salmonid populations. In: Simon RC, Larkin PA (eds) The stock concept in Pacific salmon. Mitchell Press, Vancouver Riddell BE, Leggett WC (1981) Evidence for an adaptive basis for geographic variation in body morphology and time of downstream migration of juvenile Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 38:308–320 Riddell BE, Leggett WC, Saunders RL (1981) Evidence for adaptive polygenic variation between two populations of Atlantic salmon (Salmo salar) native to tributaries of the S.W. Miramichi River, N.B. Can J Fish Aquat Sci 38:321–333 Robinson BW, Parsons KJ (2002) Changing times, spaces, and faces: tests and implications of adaptive morphological plasticity in the fishes of northern postglacial lakes. Can J Fish Aquat Sci 59:1819–1833 Ros T (1981) Salmonids in the Lake Vänern area. Ecol Bull 34:21–31 Rosen DE (1974) Phylogeny and zoogeography of salmoniform fishes and relationships of Lepidogalaxias salamandroides. Bull Am Mus Nat Hist 153:265–326 Rosseland BO, Skogheim OK (1984) A comparative study on salmonid fish species in acid aluminium-rich water. II. Physiological stress and mortality of one and two year old fish. Rep Inst Freshw Res Drottningholm 61:186–194 Rosseland BO, Skogheim OK, Abrahamsen H et al (1986) Limestone slurry reduces physiological stress and increases survival of Atlantic salmon. Can J Fish Aquat Sci 43:1888–1893 Rounsefell GA (1958) Anadromy in North American Salmonidae. US Fish Wildl Serv Fish Bull 58:171–185 Rundle HD, Schluter D (2004) Natural selection and ecological speciation in sticklebacks. In: Dieckmann U, Doebeli M, Metz JAJ et al (eds) Adaptive speciation. Cambridge University Press, Cambridge Ryman N, Allendorf FW, Ståhl G (1979) Reproductive isolation with little genetic divergence in sympatric populations of brown trout. Genetics 92:247–262 Säisä M, Koljonen ML, Gross R et al (2005) Population genetic structure and postglacial colonization of Atlantic salmon (Salmo salar) in the Baltic Sea area base don microsatellite DNA variation. Can J Fish Aquat Sci 62:1887–1904 Sandlund OT, Gunnarsson K, Jónasson PM et al (1992) The Arctic charr Salvelinus alpinus (L.) in Thingvallavatn. Oikos 64:305–351 Sandøy S, Langåker RM (2001) Atlantic salmon and acidification in southern Norway: a disaster in the 20th century, but a hope for the future? Water Air Soil Poll 130:1343–1348 Saunders RL (1981) Atlantic salmon (Salmo salar) stocks and management implications in the Canadian Atlantic Provinces and New England, USA. Can J Fish Aquat Sci 38:1612–1625 Schaffer WM, Elson PF (1975) The adaptive significance of variations in life history among local populations of Atlantic salmon in North America. Ecology 56:577–590 Schöffmann J, Sušnik S, Snoj A (2007) Phylogenetic origin of Salmo trutta L. 1758 from Sicily, based on mitochondrial and nuclear DNA analyses. Hydrobiologia 575:51–55 Scott WB, Crossman EJ (1973) Freshwater fishes of Canada. Bull Fish Res Board Can 184:1–966 Siira A, Suuronen P, Kreivi P et al (2006) Size of wild and hatchery-reared Atlantic salmon populations in the northern Baltic Sea estimated by a stratified mark-recapture method. ICES J Mar Res 63:1477–1487 Simonivic P, Maric S, Nikolic V (2007) Trout Salmo spp. complex in Serbia and adjacent regions of the western Balkans: reconstruction of evolutionary history from external morphology. J Fish Biol 70:359–380 Skaala Ø, Nævdal G (1989) Genetic differentiation between freshwater resident and anadromous brown trout, Salmo trutta, within watercourses. J Fish Biol 34:597–605 Skaala Ø, Jørstad KE, Borgstrøm R (1991) Fine-spotted brown trout: genetic aspects and the need for conservation. J Fish Biol 39:123–130
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Skogheim OK, Rosseland BO (1984) A comparative study on salmonid fishes in acid aluminium-rich water. I. Mortality on eggs and alevins. Rep Inst Freshw Res Drottningholm 61:177–193 Skrochowska S (1969) Migrations of the sea-trout (Salmo trutta L.), brown trout (Salmo trutta m. fario L.) and their crosses. Pol Arch Hydrobiol 16:125–192 Skurdal J, Andersen R (1985) Influence of temperature on number of circuli of first year scales of brown trout, Salmo trutta L. J Fish Biol 26:363–366 Snoj A, Jug T, Melkic E et al (2000) Mitochondrial and microsatellite DNA analysis of marble trout in Slovenia. J Freshw Biol 29:5–11 Snoj A, Melkic E, Susnik S et al (2002) DNA phylogeny supports revised classification of Salmothymus obtusirostris. Biol J Linn Soc 77:399–411 Snorrason SS, Skulason S, Jonsson B et al (1994) Trophic specialization in Arctic charr Salvelinus alpinus (Pisces: Salmonidae): morphological divergence and ontogenetic shifts. Biol J Linn Soc 52:1–18 Soto D, Jara F, Moreno C (2001) Escaped salmon in the inner seas, southern Chile: facing ecological and social conflicts. Ecol Appl 11:1750–1762 Soulsby C, Youngson AF, Moir HJ et al (2001) Fine sediment influence on salmonid spawning habitat in a lowland agricultural stream: a preliminary assessment. Sci Total Environ 265:295–307 Ståhl G (1987) Genetic population structure of Atlantic salmon. In: Ryman N, Utter F (eds) Population genetics and fishery management. Washington Sea Grant, Seattle Stearley RF (1992) Historical ecology of Salmoninae, with special reference to Oncorhynchus. In: Mayden RL (ed) Systematics, historical ecology, and North American freshwater fishes. Stanford University Press, Stanford Stearley RF, Smith GR (1993) Phylogeny of the Pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae. Trans Am Fish Soc 122:1–33 Storm G (1881) The collected writing by Peder Claussøn Friis. Brögger forlag, Christiania (In Norwegian) Stuart TA (1953) Spawning migration, reproduction and young stages of loch trout. Freshw Salm Fish Res 5:1–39 Stuart TA (1957) The migration and homing of brown trout (Salmo trutta). Freshw Salm Fish Res 18:1–27 Sušnik S, Knizhin I, Snoj A et al (2005) Genetic and morphological characterization of a Lake Ohrid endemic, Salmo (Acantholingua) ohridanus with comparison to sympatric Salmo trutta. J Fish Biol 68(Suppl A):2–23 Svärdson G (1945) Chromosome studies on Salmonidae. Rep Swed State Inst Freshwater Fish Res 23:1–151 Svärdson G, Fagerström Å (1982) Adaptive differences in the long-distance migration of some trout (Salmo trutta L.) stocks. Rep Inst Freshw Res Drottningholm 60:51–80 Tanaka M (1985) Factors affecting the inshore migration of pelagic larvae and demersal juvenile red sea bream Pagrus magor to a nursery ground. Trans Am Fish Soc 114:471–477 Tchernavin V (1939) The origin of salmon: is its ancestry marine of fresh water? Salm Trout Mag 95:120–140 Thorpe JE (1982) Migration in salmonids with special reference to juvenile movements in fresh water. In: Brannon EL, Salo EO (eds) Proceedings of the salmon and trout migratory behaviour symposium. School of Fisheries, University of Washington, Seattle, pp 86–97 Thorpe JE (1988) Salmon migration. Sci Prog Oxf 72:345–370 Thorpe JE (1994) Reproductive strategies in Atlantic salmon, Salmo salar L. Aquacult Res 25:77–87 Tonteri A, Veselov AJ, Totov S et al (2007) The effect of migratory behaviour on genetic diversity and population divergence: a comparison of anadromous and freshwater Atlantic salmon Salmo salar. J Fish Biol 70(Suppl C):381–398 Tonteri A, Veselov AJ, Zubchenko AV et al (2009) Microsatellites reveal clear genetic boundaries among Atlantic salmon (Salmo salar) populations from the Barents and White Seas, northwest Russia. Can J Fish Aquat Sci 66:717–735
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Townsend CR (1996) Invasion biology and ecological impacts of brown trout Salmo trutta in New Zealand. Biol Conserv 78:13–22 Townsend CR (2003) Individual, population, community, and ecosystem consequences of a fish invader in New Zealand streams. Conserv Biol 17:38–47 Valiente AG, Juanes F, Nuñez P et al (2010) Brown trout (Salmo trutta) invasiveness: plasticity in life-history is more important than genetic variability. Biol Invasions 12:451–462 Vera M, Cortey M, Sanz N et al (2010) Maintenance of an endemic lineage of brown trout (Salmo trutta) within the Duero river basin. J Zool Syst Evol Res 48(2):181–187 Verspoor E (2005) Regional differentiation of North American Atlantic salmon (Salmo salar) at allozyme loci. J Fish Biol 67(Suppl A):80–103 Verspoor E, Cole LJ (2005) Genetic evidence for lacustrine spawning of the non-anadromous Atlantic salmon population of Little Gull Lake, Newfoundland. J Fish Biol 67(Suppl A):200–205 Verspoor E, Stradmeyer L, Nielsen JL (eds) (2007) The Atlantic salmon: genetics, conservation and management. Blackwell, Oxford Vincent ER (1996) Whirling disease: the Montana experience, Madison River. In: Bergersen EP, Knoph BA (eds) Feral trout populations in Colorado. Proceedings: Whirling disease workshop – where do we go from here? Colorado Cooperative Fish and Wildlife Research Unit, Fort Collins Von Cramon-Taubadel S, Ling EN, Cotter D et al (2005) Determination of body shape variation in Irish hatchery-reared and wild Atlantic salmon. J Fish Biol 66:1471–1482 Webb J, Verspoor E, Aubin-Horth N et al (2007) The Atlantic salmon. In: Verspoor E, Stradmeyer L, Nielsen JL (eds) The Atlantic salmon: genetics, conservation and management. Blackwell, Oxford Weiss S, Antunes A, Schlötterer C et al (2000) Mitochondrial haplotype diversity among Portuguese brown trout Salmo trutta L. populations: relevance to the post-Pleistocene recolonization of northern Europe. Mol Ecol 9:691–698 Wilder DG (1947) A comparative study of the Atlantic salmon, Salmo salar Linnaeus, and the lake salmon, Salmo salar sebago (Girard). Can J Res Ser D 25:175–189 Wilson MVH, Li GQ (1999) Osteology and systematic position of the Eocene salmonid Eoslamo driftwoodensis Wilson from western North America. Zool J Linn Soc 125:279–311 Wood J, Budy P (2009) The role of environmental factors in determining early survival and invasion success of exotic brown trout. Trans Am Fish Soc 138:756–767 WWF (2001) The status of wild Atlantic salmon: a river by river assessment. http://www.panda. org/news_sacts Xia YZ, Chen YY, Sheng Y (2007) Phylogeographic structure of lenok (Brachymystax lenok Pallas) (Salmoninae, Salmonidae) populations in water systems of Eastern China, inferred from mitochondrial DNA sequences. Zool Stud 45:190–200 Yasuike M, Jantzen S, Cooper GA et al (2010) Grayling (Thymallinae) phylogeny within salmonids: complete mitochondrial DNA sequences of Thymallus arcticus and Thymallus thymallus. J Fish Biol 76:395–400 Zeisel W (1995) Angling on a changing estuary: the Hudson River, 1609–1995. Final Report to the Hudson River Foundation, New York Zupancic P (2008) [Rare and endangered freshwater fishes of Croatia, Slovenia and Bosnia Hercegovina – Adriatic Basin]. Dolsko. Agencija AAZV, Dolsko (In Slovenian)
Chapter 3
Habitat Use
3.1 Organization of the Chapter Habitat use is a central aspect in the ecology of a species. There are close associations between how individuals and population exploit, compete for, and share habitats and food resources in time and space, and their ability to survive and reproduce (Kramer et al. 1997; Cuthill and Houston 1997). For instance, individuals exploiting rich habitats can grow larger, compete better and give birth to more offspring than conspecifics exploiting poorer, more hostile environments. The literature on salmonid habitat exploitation has grown markedly during the last 25 years. This is in particular true for stream-dwelling juveniles due to direct underwater observations in combination with electrofishing (Fig. 3.1; Keenleyside and Yamamoto 1962; Bohlin et al. 1989; Heggenes et al. 1999). There have also been several descriptive field studies on habitat use in lakes by use of systematic fishing with gill nets and acoustic surveys (Jonsson 1989; Encina and Rodriguez-Ruiz 2003). The habitat use of post-smolts in estuaries and ocean is less well studied, but novel telemetric and acoustic techniques (Lacroix and McCurdy 1996; Gerlier and Roche 1998; Moore et al. 2000; Enders et al. 2007; Thorstad et al. 2007; Hubley et al. 2008), including the use of data storage tags (Riley 2007), have improved the situation (Box 3.1). Some of the results from the descriptive studies have been tested experimentally in the field or laboratory (Forseth et al. 1999; Kemp et al. 2003; Hedger et al. 2005). This chapter does not attempt to survey all the literature on food and habitat use. Instead, emphasis is placed on showing principles and major differences between Atlantic salmon and brown trout. The chapter presents habitat use of Atlantic salmon and brown trout, first in running then in still water: lakes, estuaries and ocean. Habitat use differs between spawning and feeding fish, and between fish exploiting lentic and lotic environments. Habitat use of spawning fish is described in Chap. 7. Here, we focus on habitat use of feeding fishes. In running water, they are largely territorial, but as they grow larger, the tendency to form dominance hierarchies increases. The territoriality disappears when the fish enter still water.
B. Jonsson and N. Jonsson, Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories, Fish & Fisheries Series 33, DOI 10.1007/978-94-007-1189-1_3, © Springer Science+Business Media B.V. 2011
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Fig. 3.1 Electro-fishing for sea trout
In streams and rivers, Atlantic salmon and brown trout segregate partly in habitat by depth, water velocity and significance of overhead cover. Although the species are phenotypically similar, morphological adaptations make young Atlantic salmon better able to exploit swift water than brown trout. Thus, the two segregate partly in nursery rearing habitat as they use different parts of rivers and lakes with respect to depth, distance from the shore and substrate. With increasing age and size, the parr typically move from the nursery area where they hatch and start feeding in a spectrum of habitats: from small streams to large rivers, lakes and estuaries. If there are suitable, brackish feeding habitats outside their river of origin, they can move there already as pre-smolts. After being transformed to smolts (smolting), the young can also feed in the ocean. After smolting, they are able to regulate the ionic content of their body fluids also in sea water (see Chap. 5). While brown trout seldom leave estuarine and coastal areas, Atlantic salmon move to feeding areas in the North Atlantic Ocean. Habitat and food preferences change as the fish grow. This is the reason for their ontogenetic niche shifts (Huntingford 1993). Furthermore, to ensure growth and
3.1 Organization of the Chapter
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Box 3.1 Fish Tagging Electronic tagging has provided irreplaceable insight into fish behaviour and habitat use during the most recent 20 years, and its use in habitat ecology is still growing. Electronic devices, such as radio transmitters, geolocation positioning systems, temperature and depth loggers and passive integrated transponders, are in extensive use. The tags are attached to the animal externally or implanted internally. For instance, telemetric tags are often inserted into the peritoneal cavity. Often, such tagged fish also carry a conventional tag that is specifically designed to be seen when the fish are caught. However, users should be aware that there are also negative effects of the tagging. Survival of tagged fish can be reduced. For instance, conventional Carlin tags, placed on smolts in the River Imsa, reduced survival rate by approximately 50%. In fact, the mere handling of the fish reduced the survival (Hansen 1988). Implanted electronic tags are certainly bigger burdens for the carriers. They increase mortality (Knight and Lasee 1996), decrease swimming capacity (McCleave and Stred 1975; Mellas and Haynes 1985; Peake et al. 1997) and reduce growth rate (Greenstreet and Morgan 1989). Both in study design and interpretation of results, one must acknowledge potential adverse effects of the tagging. Before wild fish are tagged, they must be caught, e.g. in a trap, hooked, netted or sampled with an electric fishing gear. All these sampling methods are harmful, and in particular smolts are sensitive to stress associated with capture, handling, anaesthetization, tagattachment, transport, fish release and the carrying of the tag. Most probably, the shorter time the fish are being handled, the more gently they are released back into nature, and the less invasive the tagging technique is, the better the fish will survive, and the less their behaviour will be modified by the operation. Also, the first time after the fish are released, the data may be of less use because of behavioural changes such as frequent, vertical movements the fish may perform. This may be because the fish search a preferred depth (van der Kooij et al. 2007). Such behaviour may render results of studies lasting only 3–4 days useless, or at least influence the interpretation of the findings.
survival, animals need to respond (often rapidly) to changing environmental conditions, such as those caused by a variable climate. They exhibit diel changes in feeding behaviour and habitat use, and seek shelter or move to a more favourable habitat under hostile conditions (Davenport 1992; Reebs 2002). Juveniles also exhibit seasonal habitat changes not the least due to variation in temperature. Both Atlantic salmon and brown trout are more day active in summer than winter. This variation is associated with water temperature as both species become more nocturnal when water temperature sinks below ca. 10°C. For each of the major environments used by Atlantic salmon and brown trout, we also describe their main diet. Although both species are recognized as flexible,
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opportunistic feeders, their diets and feeding habits vary according to requirements influenced by fish size, season and feeding areas utilized. The abilities to capture, handle and consume different food items differ with size and experience of the fish, and their main food items vary somewhat among habitats. Diets therefore change as the fish grow older and larger. There are also gender dissimilarities in habitat use associated with difference in aggressiveness between males and females, which is reflected by sexual differences in food selection. We describe the habitat use as the basis for understanding associated life history variation presented in subsequent chapters. Use of different habitats results in dissimilar growth rates, mortality rates and associated life history traits.
3.2 Rivers and Streams After the alevins have emerged from their nests, they find shelter among stones on the bottom, in crevices and interstitial holes, in undercut banks, among tree roots, in mosses and macro-vegetation in streams and rivers (Beland et al. 2004). The availability of slow flowing habitats at the stream margins is critical for the survival of the young during the first months (Armstrong and Nislow 2006). This is due to poor ability of small, newly emerged parr to hold their position and feed successfully in fast-moving water, particularly at low temperature characteristic for the spring emergence period. According to Nislow et al. (2000), marginal, slow-flowing habitats yield higher growth and survival potentials for the fish in the post-emergence period, than do more fast-flowing habitats. As they grow, the parr typically hold position in the immediate vicinity of a cobble particle or other large stones when such cover items are available. In areas with limited cobble cover, they often stay among or close to rooted aquatic macrophytes or dead wood. In the absence of cobble cover, areas with moderate levels of aquatic vegetation are used. The spatial niche occupied by an individual, influences survival and growth and thereby overall fitness (for general niche definitions, see Box 3.2). Thus, niche availability is therefore an important factor for density-dependent population processes (Armstrong and Nislow 2006). Niche dimensions, often used to describe salmonid feeding habitats in streams and rivers, are water depth, current velocity, substrate particle size and overhead cover (review in Heggenes et al. 1999). In small streams, brown trout can be distributed along the entire stream transect. In larger streams, juvenile brown trout are typically located along the bank areas, although large individuals often exploit deep, slow-flowing pool areas. Compared with brown trout, Atlantic salmon parr use a wider range of depths and water velocities and exploit deeper areas as well as stretches with faster current velocities farther from shore. This is probably one of the reasons why parr production per unit area is generally higher in small than larger streams (Sweka and Mackey 2010).
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Box 3.2 Spatial Niche The fundamental niche was defined by Hutchinson (1957) as a hypervolume with n dimensions. Each dimension corresponds to a single, potentially limiting, environmental variable. The environmental factors are abiotic such as oxygen content, temperature, salinity and water velocity, and biotic such as the size spectrum of potential food items. The fundamental niche defines the ranges of relevant environmental variables within which a population, in absence of natural enemies, will maintain itself by natural recruitment. For a given niche dimension, this range is usually smaller than the zone of tolerance. According to Hutchinson, there are bionomic axes and scenopoetic axes. The bionomic axes are represented by variables directly involved in the lives of organisms such as food and space, i.e. resources that individuals compete for. The scenopoetic axes relate to tolerance limits to physical and chemical variables such as temperature, oxygen content and water velocity. The latter axes are important for the presence of species, but are not factors they compete for. The spatial niche is the physical characteristics of the habitat. The feeding niche includes potential food items and competitive relationships. It is often difficult to distinguish between competition for food and competition for space. In running water, an optimal holding station for a salmonid parr is one in a low velocity habitat where the fish can hold its position without using much energy, but still being close to a swift current carrying downstream drifting food items, and close to cover where the fish can hide and reduce the risk of predation (Jenkins 1969; Bachman 1984; Fausch 1984). The realized niche is restricted to the subset of the fundamental niche that is occupied by the population in presence of natural enemies being predators, pathogens and interspecific competitors (Giller 1984).
3.2.1
Size and Age Structured Habitat Use
Current velocity, water depth, substrate structure and composition and shelter opportunities are major habitat variables influencing the habitat use of stream-living salmonids. Their habitat use is expected to maximize their net energy intake-rate, balancing foraging opportunities, behavioural costs and shelter (Jenkins and Keeley 2010). Shelter opportunities are most important for their position in the river (Jenkins 1969), and densities and growth of Atlantic salmon parr are highly influenced by shelter availability. For instance, strength of density-dependent population regulation, measured as carrying capacity, has been found to increase with decreasing number of shelters (Finstad et al. 2007, 2009). Feeding opportunities also influence by habitat use. Juvenile Atlantic salmon and brown trout feed to a large extent on drifting and epibenthic invertebrates (Elliott 1973; Keeley and Grant 1995). The drift is positively correlated with
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current velocity (Allan 1987; Lancaster et al. 1996), and the epibenthic zoobenthos density depends both on porosity and stability of the substrate and water depth (Jowett 2003; Xiaoxia et al. 2007; Duan et al. 2008). Presence of appropriate shelter, not only reduces the risk of predation, but provides also a metabolic benefit to the fish. Likely, this has implications for growth performance and activity budgets (Millidine et al. 2006). Substrate composition and overhead cover are all contributing to the shelter of the fish, but the effect will vary between species as well as sizes of the fish. Here, we discuss responses of Atlantic salmon and brown trout to single hydraulic variables. This is important knowledge in understanding the habitat use of the fish, and when managing or restoring salmonid habitats. But variables such as water depth and current velocity interact, and presence of competitors and predators complicates the situation even more. Thus, habitat selection judged from the effect of a single factor alone can be fallacious. Under natural conditions it can misrepresent the complexity of fish behaviour, especially as they grow older and their repertoire of behavioural responses increases (Ayllón et al. 2009). Thus, single characters should be used with care when judging the suitability of habitats, or when making flow management decisions (Box 3.3).
3.2.1.1
Depth and Current Velocity
Salmonid habitat use is often size and age structured. The smallest and youngest parr typically exploit shallower areas closer to shore, than older and large parr. They switch to faster/deeper stream habitats as they become larger (Morantz et al. 1987; Keeley and Grant 1995). Most studies agree that salmonid parr exhibit intraspecific differences in habitat selection (Bremset and Berg 1999; but see Bremset 2000). To date, however, habitat data are biased toward summer/daytime sampling; this is unfortunate because the population ecology of salmonids is heavily influence by winter events, especially in northern areas where most winter activity occurs at night (Cunjak et al. 1998; Huusko et al. 2006).
Box 3.3 Physical Habitat Simulations An often used model to simulate potential available habitat for stream-living salmonids is the ‘Physical Habitat Simulation System (PHABSIM)’ (Milhous et al. 1989). This system estimates available habitat for species and life stages as a function of discharge. It requires information about water depth, water velocity, bottom substratum, overhead cover and habitat preference curves for the cohorts in question. The system couples a hydraulic and a biological model of habitat selection (the habitat suitability criteria cf. Figs. 3.2 and 3.3). The standard output of PHABSIM simulations is a curve that relates the weighted usable area with stream flow. The simulation is particularly sensitive to the accuracy of the habitat suitability criteria.
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Atlantic Salmon When the alevins emerge from the gravel bed, they seek areas of the stream with low water velocities (Heland et al. 1995; Armstrong and Nislow 2006). At the end of the emergence period, they maintain positions in the spawning area at sites where velocities in the water column are below ca. 0.5 m3s−1, but substantially lower near the bottom where they stay (Gustafson-Greenwood and Moring 1990). About 2 weeks later, most of them have moved off the nest and established territories, usually located within 1–5 m from the redd. The size of the defended area increases with the size of the parr. The alevins occur at depth between 2 and 60 cm, but when the yolk is consumed, they gradually expand their habitat into deeper water (Gibson 1993; Scruton and Gibson 1993; Baran et al. 1997; Bremset and Berg 1997; Mäki-Petäys et al. 1997). During the first summer, most Atlantic salmon parr live mainly along stream banks to ca. 1 m depth (Fig. 3.2a). Larger parr occur down to ca. 1.5 m or more. At low fish density, the parr appear to prefer pool before riffles, but this evens out as density increases (Blanchet et al. 2006). In pools, small individuals held position near river beds and river banks. Their height above the bottom and distance from the river bank increase with increasing fish size (Bremset and Berg 1997). Although Atlantic salmon typically grow up in large streams and rivers, the parr can enter smaller tributaries as they grow older. For instance, in the River Tana, the large border river between North Norway and Finland, 0–2 year old parr live in the main stem of the river, whereas 2–4 year olds can enter tributaries for feeding in summer. The oldest parr typically move to the uppermost sections. Most of them leave the tributaries in the autumn to spend the winter in the main stem (Erkinaro 1995). In sympatry with brown trout, Atlantic salmon parr are largely exploiting depths between 15 and 40 cm, and they appear to be scarcer than brown trout in the deep pools (Kennedy and Strange 1982). Pool-dwelling fish are generally larger than similar aged conspecifics. Pools appear to be profitable feeding areas, giving shelter for large individuals, and being less energy demanding than riffles. Thus, river pools appear to be favourable habitats for large parr of Atlantic salmon, but also for brown trout, as described below. Critical current velocity for the smallest parr of Atlantic salmon is 25 cm s−1 (Heggenes and Traaen 1988b). Flow-sensitivity gradually decreases with fish development; when the parr have reached 4–5 cm in length, they are able to tolerate water velocities higher than 50 cm s−1, and they actively seek out the low-velocity niches (0–10 cm s−1) (Crisp and Hurley 1991). Up to a total length of 7 cm, they occur mainly at water velocities between 10 and 70 cm s−1 with mean water column velocities in the range of 20–40 cm s−1 (Fig. 3.2b). Larger parr (>7 cm) can use river stretches with water velocity of more than 1 m s−1 (Heggenes and Saltveit 1990). There may be little spatial segregation by size relative to water velocity, although large parr held positions in faster flowing water than smaller ones (Huntingford et al. 1988). The current velocity in rivers decrease towards the bottom, where the salmonids held their stations, and the water flow near the snout of the young Atlantic salmon is usually between 0 and 20 cm s−1 for parr shorter than 7 cm in length, between 3 and 25 cm s−1 for those between 7 and 10 cm in body length, and 5–25 cm s−1 for parr longer than 10 cm (Heggenes et al. 1999).
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Fig. 3.2 Habitat suitability index curves for Atlantic salmon age-0 (7 cm, blue line) in relation to (a) total water depth (cm), (b) mean water velocity (cm s−1), and (c) type of bottom substratum: 1 = organic matter, 2 = clay, 3 = silt, 4 = sand, 5 = gravel and pebbles, 6 = cobble, 7 = boulders, 8 = rock (From Heggenes (1995). Reproduced with permission of the Norwegian Research Council)
Brown Trout Brown trout parr shorter than 7 cm (age-0) are abundant in shallow water at depths between 5 and 30 cm. Preferred depth increases with fish size and depth of the suitable habitat (Greenberg 1994; Mäki-Petäys et al. 1997; Riley et al. 2009).
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The largest brown trout select the deepest stream area. Large brown trout can be depth constrained in small streams because of lack of suitable habitat (Heggenes et al. 1999). Thus, as a species, brown trout prefer relatively deep streams and rivers (Fig. 3.3a). Brown trout parr inhabit less fast-flowing areas than Atlantic salmon parr (Fig. 3.3b). In small streams, brown trout shorter than 7 cm occur in shallow riffles with water velocities beneath 50 cm s−1, but the water velocity near their snouts is usually between 0 and 10 cm s−1. Brown trout rarely stay in habitats where the current velocity exceeds 20 cm s−1 near their snouts (Heggenes et al. 1999), and they are less flexible relative to water velocity than the Atlantic salmon parr (Heggenes and Saltveit 1990; Heggenes 2002). Furthermore, during nights they held positions closer to the bottom than during the day, and they use shallower areas with lower water velocities and finer substrata (Heggenes and Saltveit 2007). In large rivers brown trout parr live close to the river bank and in sloughs and backwaters, with low water velocities and few older brown trout. Larger fish can
Fig. 3.3 Habitat suitability index curves for brown trout in relation to (a) total water depth (cm), (b) mean water velocity (cm s−1) and (c) type of bottom substratum: 1 = organic matter, 2 = clay, 3 = silt, 4 = sand, 5 = gravel and pebbles, 6 = cobble, 7 = boulders (From Heggenes (1995). Reproduced with permission of the Norwegian Research Council)
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use faster-flowing water (Greenberg 1994; Mäki-Petäys et al. 1997), but more commonly, they use slow flowing, deeper pool-areas (Bremset and Berg 1997; Heggenes et al. 1999). In pools, small individuals stay near the river bed and the river bank like Atlantic salmon parr, and their height above the bottom and distance from the river bank increase with increasing fish size (Bremset and Berg 1999). But brown trout held position significantly higher above the bottom substratum and closer to the river bank than Atlantic salmon. This partial segregation between brown trout and Atlantic salmon parr is most pronounced among the smallest individuals.
3.2.1.2
Substratum
A stony bottom substratum is preferred by stream living Atlantic salmon and brown trout. They hide among the stones which shelter against hostile abiotic conditions such as strong current velocity as well as inspection by possible predators. The stones can also give visual isolation between individuals, which may decrease the level of aggression in populations. For instance, Venter et al. (2008) found that boulders reduced reaction distance of Atlantic salmon parr to a novel stimulus, supporting the hypothesis that visual isolation among individuals influences the density of young salmonids in rivers. A similar result was reported by Dolinsek et al. (2007). Juvenile stream-living salmonids typically aggregated in areas with large substrate particle size, where shelters probably are abundant, although growth decreased with increasing densities. Thus, they appeared to favour the availability of shelter over maximization of growth (Teichert et al. 2010). Atlantic Salmon The parr are mainly found on a bottom substratum consisting of gravel, pebbles and cobble (Fig. 3.2c). Although there are individual differences in substrate preference (Johnsson et al. 2000), most small parr (0.05); (k) passable river length (RL km) (Regression line: S = 156.729 + 0.0873RL, r2 = 0.269); (l) yearly mean water discharge (Q m3 s−1) (Regression line: S = 154.724 + 0.1497Q, r2 = 0.152). All regression lines are significant (P < 0.05) (From L’Abée-Lund et al. (1989). Reproduced with permission of JStor)
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appeared to govern the smolt age of Atlantic salmon over such a large geographical area. A similar approach did not improve the smolt-age prediction for European brown trout over that of latitude alone (Jonsson and L’Abée-Lund 1993). A climatic difference between North America and West Europe is probably the main reason why the index of growth opportunity fitted the Atlantic salmon data better than those of European brown trout. Within rivers, there are annual differences in smolt age. Climatic conditions encountered during embryonic development influence the subsequent growth rate and thereby smolt age. Correlation studies in the River Imsa indicated that the warmer and wetter the winter before hatching, the better the offspring grew in the subsequent first year of life, and the higher the proportion of the cohort smolted as 1-year-olds (Jonsson et al. 2005). Strothotte et al. (2005) reported a similar association between first year’s growth and smolt age in Canadian Atlantic salmon. Owing to high water temperature during embryonic development, the embryos hatch early, extending the first growth season, as e.g. found in brown trout (Elliott et al. 2000). Furthermore, feeding opportunities may be good after mild, wet winters with high flow and large water-covered areas. Thus, the parr may become large at the end of the first growth season resulting in relatively more 1-year-old smolts.
5.4.2
Size and Growth
The decision to undergo smolting and migration to the sea is associated with fish size and growth trajectories. Elson (1957) assumed that Atlantic salmon had to reach a minimum length of 10 cm in the preceding autumn to smolt in the subsequent spring. Fahy (1985) also maintained that parr smolted as quickly as possible after having passed this threshold length. This rule of thumb has been shown useful for hatchery managers, but is too simple when applied to wild populations (Økland et al. 1993). The main reason is that wild fish are often more variable in size than hatchery fish, and typically, they smolt over a longer size and age span than those from hatcheries. Fast-growing parr tend to smolt younger and smaller than slowergrowing parr (Jonsson 1985). This holds for brown trout, and often also for Atlantic salmon, although results vary among rivers (Figs. 5.5 and 5.6) Very fast-growing parr can smolt before reaching 10 cm, whereas slow-growing parr can pass 10 cm more than a year before they smolt. This illustrates that growth rate also influences smolt size. Based on this, Økland et al. (1993) hypothesized a functional relationship between growth rate and smolt size of Atlantic salmon and brown trout where fitness is maximized (Fig. 5.7). Populations that consist of fast-growing parr often have large smolts (Jonsson and L’Abée-Lund 1993). Furthermore, there is tendency for smolt size to increase with increasing latitude and decreasing water temperature in the sea entered by the smolts (L’Abée-Lund et al. 1989). This among population regression holds for limited geographical areas such as the Norwegian coastline (58–71°N) (Fig. 5.3e), but not for much larger regions such as Norway, the British Isles and the Baltic Sea area (Fig. 5.4b). The reason may be that the ocean is not uniformly warmer from the British Isles to Norway, and the Atlantic Ocean has higher salinity than the Baltic Sea.
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Fig. 5.5 Annual body length increment (mm) of Atlantic salmon parr grouped according to smolt age (years). The end of the lines gives mean age and length at smolting. The horizontal dotted line gives the mean length of the shortest smolt age group in the Norwegian rivers (a) Beiarelva, (b) Saltdalselva, (c) Lærdalselva and (d) Sandvikselva (From Økland et al. (1993). Reproduced with permission of Wiley-Blackwell)
Among rivers, mean smolt sizes of Atlantic salmon populations vary from about 12 cm to 22 cm (Power 1969; Jensen and Johnsen 1986). Individual fish, however, can vary from ca. 8 cm to more than 30 cm (Jonsson et al. 1998a). In brown trout, population means in smolt size are between 7 and 25 cm (Jonsson 1985; Jonsson and L’Abée-Lund 1993; Jonsson et al. 2001), and the within-population variation is typically greater than that of Atlantic salmon. When these two species occur in the same river, smolts of Atlantic salmon are usually smaller than those of brown trout. For instance, in the River Imsa, most Atlantic salmon smolts weigh between 30 and 60 g, while brown trout smolts are approximately twice this heavy (Jonsson and Jonsson 2009). The size difference may be associated with the fact that Atlantic salmon has better ionoregulatory capacity in seawater than brown trout (Hoar 1988). In addition, pre-smolts of brown trout can enter brackish water early in life. For instance, in the Baltic Sea, brown trout not longer than 30 mm (0.3 g wet mass) have been observed
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Fig. 5.6 Annual body length increment (mm) of anadromous brown trout parr grouped according to smolt age (years). The end of the lines gives mean age and length at smolting. The horizontal dotted line gives the mean length of the shortest smolt age group in the Norwegian rivers (a) Beiarelva, (b) Saltdalselva, (c) Lærdalselva and (d) Sandvikselva (From Økland et al. (1993). Reproduced with permission of Wiley-Blackwell)
entering brackish water from the small stream Arån on the Swedish island, Gotland. The brown trout emigrated in summer, from about 3 months after hatching (Landergren 2001). Brown trout may even spawn in brackish water and leave viable offspring in areas with salinity below 4 psu (Landergren and Vallin 1998; Limburg et al. 2001). We know of no similar observation from Atlantic salmon. Some of the smallest Atlantic salmon smolts have been found in cold, glacier-fed rivers where the fish are slow-growing, and they enter relatively warm seawater with good growth opportunities (Jensen and Johnsen 1985, 1986). The largest Atlantic salmon smolts, on the other hand, occur in high latitudes rivers such as the Koksoak River, where the smolts enter the very cold Ungava Bay, Canada (Power 1958, 1969; Dempson et al. 2010). There, they migrate into extremely cold seawater, only warm enough for Atlantic salmon to survive during a few weeks in the summer.
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Fig. 5.7 A hypothetical cost/benefit model of smolting at different sizes. It is assumed that the net benefit of smolting decreases with increasing distance to an optimal smolt size. Smolting when body size is too small increases post-smolt mortality, smolting when too old and large results in decreased post-smolt growth and higher accumulated mortality before smolting. Fast-growing parr are probably constrained earlier by limited food resources in the river due to their higher metabolic requirements, and therefore have a smaller optimal smolt size than slower-growing parr (From Økland et al. (1993). Reproduced with permission of Wiley-Blackwell)
Also in brown trout, the largest smolts are reported from rivers as far north such as the sub-Arctic River Tana. Those that enter a cold sea area are larger than those migrating into a warmer sea (Fig. 5.3h). There is no similar significant correlation between smolt size and river temperature or the length of the growth season (Fig. 5.3i, j). Large smolt size in populations that migrate into particularly cold seawater probably reflects that ionoregulation in cold seawater is energetically expensive for the fish. Growth opportunities and temperature at sea are both important factors influencing smolt size. Inter-population variation in smolt size appears both to reflect a phenotypic plasticity response to variation in growth rate (Jonsson 1985), and inherited among population variation adapted to local growth and survival opportunities (cf. Refstie et al. 1977).
5.4.3
Habitat Constraints
In small streams, mean smolt size and age (the two are significantly correlated) of brown trout increase with increasing mean annual water discharge, but the trend levels off at mean annual water flows of approximately 0.1 m3 s−1 (Fig. 5.8) (Jonsson et al. 2001). Furthermore, the variation in smolt length (CV) correlates negatively with mean annual water discharge of the streams. The greater heterogeneity in small streams may reflect more variable success of large smolts in these
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Fig. 5.8 Relationships between mean annual water discharge of the nursery stream (Q m3 s−1) and (a) mean smolt length (S mm) (Regression line: S = 180.9 – 3.87/Q, r2 = 0.633, P = 0.001); (b) coefficient of variation in smolt length (CVs) (Regression line: ln CVs = −0.395 ln Q – 2.1, r2 = 0.61, P = 0.001); (c) mean smolt age (A years) (Regression line: A = 2.54 – 0.0377/Q, r2 = 0.492, P = 0.002); (d) coefficient of variation in smolt age (CVa) (Regression line: ln CVa = −0.23 ln Q – 1.736, r2 = 0.46, P = 0.003) of anadromous brown trout from Norway (From Jonsson et al. (2001). Reproduced with permission of Wiley-Blackwell)
streams. The small streams included in the study by Jonsson et al. (2001) sometimes dry out during summer, except for some scattered pools. To survive, the fish often leave early. The significant correlation between smolt size and water flow is weak for streams with mean annual water discharge above 1 m3 s−1 (Fig. 5.3m). Large streams probably have enough water to sustain even large parr, reducing the importance of flow variation for size at seaward migration. Thus, stream size can restrict smolt size in small streams, whereas the effect is minute (if any) in large streams and rivers. In streams with mean annual water discharge above 1 m3 s−1, brown trout smolt size correlates positively with river length, and the correlation is stronger than that between water flow and smolt size (Fig. 5.3e). This may reflect a cost of migration which increases with the distance from the sea. We know of no similar study for Atlantic salmon.
5.4 Ecological Characters
5.4.4
233
Sex Ratio
Females are more abundant than males among downstream migrating smolts. This is general for Atlantic salmon (Dahl 1910; Österdahl 1969; Jonsson et al. 1998a) and brown trout (Jonsson 1985; Dellefors and Faremo 1988). Approximately 60% females and 40% males are common among populations of anadromous brown trout and Atlantic salmon, although some variation is observed (Jonsson and Jonsson 1993). This is partly due to an inherited difference in life history tactics between the sexes. Given the same growth rate, females have a higher tendency to smolt than males, whereas males have a higher tendency to attain parr maturity. In males, mortality can increase as a cost of reproduction, and the fish can re-mature instead of smolting and migrating to sea (Hansen et al. 1989; Jonsson 1989). The higher proportion of migratory females than males is partly because the mortality of mature parr is higher than that of similar aged juveniles as a cost of reproduction, partly because male parr can remature in the subsequent year instead of migrating to sea. The latter is common in brown trout (Jonsson 1985; Dellefors and Faremo 1988), but can also occur in Atlantic salmon (Hansen et al. 1989). Thus, smolting and sexual maturation can be alternative tactics in partly migratory populations.
5.4.5
Smolting Versus Sexual Maturation
Are smolting and sexual maturation competing processes? Landgrebe (1941) concluded that there is a genetic basis for when Atlantic salmon smolt, and that smolting and sexual maturation are not competing processes. Also, there is a large literature demonstrating that in Atlantic salmon, mature parr often go through a smolting process subsequent to maturation (e.g. Österdahl 1969; Hansen et al. 1989; Berglund et al. 1991). For instance, with some annual variation, about 50% of the male smolts in the River Imsa are previously mature parr. This was demonstrated by colour marking of mature and immature parr in the autumn and monitoring of the downstream migration during the subsequent spring (Bohlin et al. 1986), and by inspecting the gonads of every tenth smolt descending to sea in the Rive Imsa since the early 1980s (Jonsson et al. 1998b). However, some mature parr re-mature, and this seems influenced by the hormonal status of the fish. The fraction of mature male parr that smolted was increased when the testes were stripped for spermatozoa in the autumn (Hansen et al. 1989), and when they were kept in relatively warm water over winter (>4°C) (Berglund et al. 1991), probably decreasing the level of steroid hormones in the fish. Do Atlantic salmon or brown trout attain maturity the same year as they smolt? In Atlantic salmon post-smolts can mature the first autumn after smolting, but usually smolted fish postpone maturation one or more years (Jonsson et al. 1993). Brown trout, on the other hand, mature regularly in the first autumn subsequent to smolting (Jonsson 1985; Jonsson et al. 2001). The ultimate reason for the species difference
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is probably that the fitness advantage by feeding at sea and/or the cost of maturation and returning to fresh water for spawning is higher in Atlantic salmon than brown trout. For instance, the mass of Atlantic salmon increases about 30 times during the first year at sea, from about 50 g to 1.5 kg. The corresponding figures for brown trout staying at sea a similar length of time are approximately eight times, from about 75 g to 600 g (Jonsson 1985; Jonsson et al. 1991, 2001). The increase in mass reflects the increase in reproductive effort and success for the fish (Fleming et al. 1996; Wootton 1998). As parr in fresh water, brown trout grow faster than Atlantic salmon. The relative difference in sea survival between Atlantic salmon and brown trout is smaller than that in growth. In the River Imsa, where most Atlantic salmon and brown trout return to the river after only 1 year at sea, sea survival of Atlantic salmon was estimated at 8.9% between 1976 and 1994 (Jonsson et al. 1998b). The corresponding figure for brown trout from 1976 to 2003 was 11.4% (Jonsson and Jonsson 2009). For parr in fresh water, survival, if different, may be higher for brown trout than Atlantic salmon due to higher growth rate and more sheltered habitat use. Thus, the fitness advantage of feeding at sea (c.f. Eq. 7.1) is higher for Atlantic salmon than brown trout, particularly thanks to the large difference in growth rate at sea. Due to the longer sea migration in Atlantic salmon than brown trout, the cost of returning to freshwater for spawning is also higher selecting against an early maturation and return in this species. Also, in other salmonids, such as Arctic charr and sockeye salmon, sexual maturation in parr typically precludes subsequent smolting. As with brown trout, sexually mature parr do not smolt, but become freshwater resident. In sockeye salmon, the fastest growing individuals may smolt at the youngest age (Ricker 1938). Slower growing individuals mature sexually as parr, whereas even slower-growing individuals smolt the year thereafter. A similar difference in growth between resident and anadromous brown trout was reported for brown trout females from Vangsvatnet Lake, Norway (Fig. 5.9). The fastest-growing fish should be able to acquire enough resources to mature and spawn, but still they smolt and move to sea. Possibly, maturation is postponed according to their genetic program because the expected lifetime fitness increases if they stay immature and go to sea. This observation is in apparent contrast to Thorpe and co-worker’s (e.g. Thorpe 1994, 2007; Thorpe and Metcalfe 1998; Thorpe et al. 1998) view that smolts are individuals that fail to reach the required energy threshold for maturation while in freshwater. However, the relative lipid deposits of the migrants may be lower than that of residents as reported for anadromous Arctic charr by Rikardsen et al. (2004). The fish deplete their lipid deposits during smolting, and in this species, migrants also have lower energetic density in the autumn than corresponding residents which attain maturity in the subsequent summer and autumn. Thus, regulatory mechanisms for the energy allocation for individuals choosing different life history patterns probably exists, but are as yet poorly understood (Matty and Lone 1985; Post and Parkinson 2001; Jonsson and Jonsson 2003; Claireaux and Lefrançois 2007). Individuals from freshwater resident salmonid populations can show signs of smolting in spring. For instance, Arctic charr from a freshwater resident population in the River Imsa can move to sea in spring like regular smolts. However, none
5.4 Ecological Characters
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(a) 20
15
Length increments
10
5
0
(b) 20
15
10
5
0
1
2
3
4
Age
Fig. 5.9 Estimated mean length increment (cm) of (a) female parr smolting at age-2 and ³3 years (solid lines) and those attaining maturity at age ³3 years (broken line) and become freshwater resident; (b) male parr smolting at ages 2, 3 and 4 years (solid lines) and those attaining maturity at age 2 and ³3 years (broken lines) and becoming freshwater resident in Vangsvatnet Lake, Norway (Based on data from Jonsson (1981))
of them returns to the river, but some have been captured in other rivers, which they cannot reach without moving through full seawater (35‰ salt) (Jonsson et al. 1989). This behaviour disperse freshwater resident fish among water courses. Kiiskinen et al. (2002) showed that non-anadromous Atlantic salmon in Lake Saimaa, Finland, go through a smolting process in the spring, similar to anadromous populations. These fish attain maturity without having been to sea. This supports the view that smolting in Atlantic salmon is a seasonal phenomenon independent of sexual maturation. On the other hand, landlocked Atlantic salmon from other systems, such as Lake Byglandsfjord, Norway, do not exhibit increased levels in the growth hormone and cortisol axes similarly to anadromous salmon (Nilsen et al. 2008), illustrating that in this trait, there are genetic differences among populations.
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There are also genetic differences among conspecific populations in the tendency to migrate (Jonsson 1982; Svärdson and Fagerström 1982). Probably the hormonal status of parr in spring must exceed a minimum level for the fish to smolt and go to sea. This level may be determined through natural selection, and the hormonal level appears to depend on the age and size of the fish. Young fish show increased gill Na+/K+-ATPase activity and cortisol each spring, and the process proceeds faster and to a greater extent every year the young fish remain in fresh water (Wedemeyer et al. 1980). As a consequence, large smolts migrate to sea earlier in spring and in colder water than smaller smolts (Jonsson et al. 1990; Bohlin et al. 1993), in line with their improved ability of ionoregulation in cold seawater.
5.5 Is Smolt-Age Inherited? There is heritability for age at smolting, as experimentally documented from both Atlantic salmon and Chinook salmon (Refstie et al. 1977; Clarke et al. 1992, 1994). However, the genes involved have not been identified (Ferguson 2006). Inheritance studies also suggest that both timing of and propensity for smolting are under genetic control. On the other hand, a change in gene expression does not mean that the process of smolting is entirely under genetic control (Ferguson 2006). The fact that juveniles leave the nursery area, when there are poor feeding opportunities or hostile environmental conditions (Forseth et al. 1999; Juanes et al. 2004; Jonsson and Jonsson 2009), illustrates that phenotypic plasticity may be also important for the emigration from rivers. In Chinook salmon, crosses between life-history variants have indicated that smolting in the first year of life was dominant and probably controlled by few loci (Clarke et al. 1992, 1994). These authors used body morphology and coloration to discriminate between fish smolting at age 1 and 2 years. In sockeye salmon and rainbow trout, crosses between resident and anadromous forms, also suggest that there is a genetic basis for the propensity to undergo smolting (Foote et al. 1992). In these species, hybrids were intermediate between freshwater and migratory forms in their ability to hypo-osmoregulate in seawater, suggesting that the propensity for smolting is under additive rather than dominant genetic control. This is further supported by the observation that transplanted offspring of anadromous brown trout retained their ability to smolt and migrate to sea when released among non-anadromous conspecifics above an upstream passable waterfall, contrary to the non-anadromous offspring that held their position in the river instead of migrating to sea when released among migratory fish downstream of the waterfall (Jonsson 1982). But, phenotypically plastic aspects of the trait are suggested by the observation that releases of offspring of non-migratory brown trout have given rise to anadromous populations where environmental conditions at sea are suitable (McDowall 1988). On the other hand, the tendency to smolt and migration to sea can be retained in populations even when migrants are unable to return to their river of origin for spawning. Furthermore, it has been shown that non-anadromous populations can
5.6 Summary
237
bring about the physiological changes necessary to adjust to marine conditions after having been in fresh water for more than 1,000 generations (Staurnes et al. 1992; Jonsson et al. 1989; Kiiskinen et al. 2002), and offspring of non-anadromous populations of brown trout survive and grow equally well in the ocean as conspecific offspring from anadromous populations (Jonsson et al. 1994a, b, 1995). The fact that growth rate influences age and size at smolting signifies that there are also environmental influences on the expression of the trait. However, it is difficult to determine whether environment influences the gene expression, operates through the neuroendocrine system, or whether it is an endogenous gene control by other genes, or both. But the observation that different populations differ in ability to survive in seawater lends support to the hypothesis that smolting is under genetic control (Burton and Idler 1984; Nilsen et al. 2003). Thus, there is evidence for that the tendency to smolt is inherited, but that the expression of the trait can be modified by environmental influences.
5.6 Summary 1. The parr-smolt transformation (smolting) is characterized by changes in morphology, physiology and behaviour. Smolts are silvery due to crystals of two purines, guanine and hypoxanthine. Improved hypo-osmotic capacity is caused by increased expression of Na+-K+adenosine triphosphatase (ATPase) in chloride cells of the gills. Smolts lose the positive rheotaxis characteristics of parr. 2. Smolting is controlled by an endogenous rhythm, itself controlled by the nervous and endocrine systems, and synchronized by external factors such as photoperiod and temperature. Increasing and decreasing photoperiods are major predictive, proximate factors indicating the season. Water temperature influences developmental rate, and is responsible for variation in seasonal time of smolting. 3. Smolts are restless, exhibit reduced feeding, cease territoriality, exhibit decreased aggressiveness and move away from the bottom and up into the higher strata of the water column. Smolts move downstream in small schools. The migration is active, but the smolts use the water current when moving downstream. 4. In European brown trout, latitude is a good predictor for smolt age, at least from the British Isles to northernmost Norway. In Atlantic salmon, an index based on temperature and photoperiod is a good predictor of smolt age. 5. Size at smolting depends on growth rate and age. Smolt length tends to increase with increasing age and decreasing growth rate within and among populations of brown trout and Atlantic salmon. Smolt size of brown trout increases along the Norwegian coast, but this trend does not hold when populations from the British Isles and Baltic region are included. Within populations, large fish smolt and move to sea earlier in spring than smaller ones, probably because they are better able to ionoregulate in cold seawater. 6. In streams with annual mean annual flow below 0.1 m3 s−1, smolt size of brown trout increases with increasing water discharge. Parr can escape from small streams into brackish water during drought or poor feeding conditions.
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7. There is a larger proportion of female than male smolts in both brown trout and Atlantic salmon due to an inherited difference in life history tactics between the sexes. Many males attain maturity instead of smolting. In Atlantic salmon, but not in brown trout, a large proportion of previously mature male parr can smolt after having spawned. 8. There is an inherited tendency for the propensity to smolt, but the genes involved are not identified. However, the smolting process is not entirely under genetic control. Juveniles also exhibit phenotypic plasticity for the trait. 9. Smolts desmolt if retained in freshwater past their normal time of seawater migration. They lose their silvery colour and exhibit reduced gill Na+, K+-ATPase activity. Also, their tissue composition changes back towards that of parr. Desmolting is often related to sexual maturation, indicating a link between hormones influencing de-smolting and sexual maturation.
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Bohlin T, Dellefors C, Faremo U (1993) Date of smolt migration depends on body-size but not age in wild sea-run brown trout. J Fish Biol 49:157–164 Burton MP, Idler DR (1984) Can Newfoundland landlocked salmon, Salmo salar L. adapt to sea water? J Fish Biol 24:59–64 Claireaux G, Lefrançois C (2007) Linking environmental variability and fish performance: integration through the concept of scope for activity. Philos Trans R Soc Lond B 362:2031–2041 Clarke WC, Withler RE, Shelbourn JE (1992) Genetic control of juvenile life history pattern in Chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci 49:2300–2306 Clarke WC, Withler RE, Shelbourn JE (1994) Inheritance of smolting phenotypes in backcrosses of hybrid stream-type X ocean-type chinook salmon (Oncorhynchus tshawytscha). Estuaries 1A:13–25 Conte FP, Wagner HH (1965) The development of osmotic and ionic regulation in juvenile steelhead trout Salmo gairdneri. Comp Biochem Physiol 14:603–620 Dahl K (1910) The age and growth of salmon and trout in Norway as shown by their scales. Salmon and Trout Association, London Dann SG, Allison WT, Levin DB et al (2003) Identification of a unique transcript down-regulated in the retina of rainbow trout (Oncorhynchus mykiss) at smoltification. Comp Biochem Physiol 136B:849–860 Davidsen JG, Plantalech Manella N, Thorstad EB et al (2009) Vertical movements of Atlantic salmon postsmolts relative to measures of salinity and water temperature during the first phase of the marine migration. Fish Manage Ecol 16:147–154 Dellefors C, Faremo U (1988) Early sexual maturation in males of wild sea trout, Salmo trutta L., inhibits smoltification. J Fish Biol 33:741–749 Dempson JB, Braithwaite VA, Doherty D et al (2010) Stable isotope analysis of marine feeding signatures of Atlantic salmon in the North Atlantic. ICES J Mar Sci 67:52–61 Dickhoff WW, Beckman BR, Larsen DA et al (1997) The role of growth in endocrine regulation of salmon smoltification. Fish Physiol Biochem 17:231–236 Duston J, Saunders RL (1990) The entrainment role of photoperiod on hypo-osmoregulatory and growth-related aspects of smolting in Atlantic salmon (Salmo salar). Can J Zool 68:707–715 Ebbesson LOE, Ekström P, Ebberson SOE et al (2002) Neural circuits and their structural and chemical reorganization in the light-brain-pituitary axis during parr-smolt transformation in salmon. Aquaculture 222:59–70 Ebbesson LOE, Björnsson BT, Ekström P et al (2008) Daily endocrine profiles in parr and smolt Atlantic salmon. Comp Biochem Physiol A 151:698–704 Elliott JM, Hurley MA (1997) A functional model for maximum growth of Atlantic salmon parr, Salmo salar, from two populations in Northwest England. Funct Ecol 11:592–603 Elliott JM, Hurley MA, Maberley SC (2000) The emergence period of sea trout fry in a Lake District stream correlates with the North Atlantic Oscillation. J Fish Biol 56:208–210 Elson PF (1957) The importance of size in the change from parr to smolt in Atlantic salmon. Can Fish Culturist 21:1–6 Englund V, Niemelä E, Länsman M et al (1999) Variations in Atlantic salmon, Salmo salar L., smolt age in tributaries of the River Teno, Finland. Fish Manage Ecol 6:83–86 Eriksson T (1984) Adjustments in annual cycles of swimming behaviour in juvenile Baltic salmon in fresh and brackish water. Trans Am Fish Soc 113:467–471 Eriksson LO, Lundqvist H (1982) Circannual rhythms and photoperiod regulation of growth and smolting in Baltic salmon (Salmo salar L.). Aquaculture 28:113–121 Fahy E (1985) Cyclic fluctuations in the abundance of trout (Salmo trutta L.). Arch Hydrobiol Suppl 3:404–428 Fängstam H, Berglund I, Sjöberg M et al (1993) Effects of size and early sexual maturity on downstream migration during smolting in Baltic salmon (Salmo salar). J Fish Biol 43:517–529 Ferguson A (2006) Genetics of sea trout, with particular reference to Britain and Ireland. In: Harris G, Milner N (eds) Sea trout: biology, conservation and management. Blackwell, Oxford Finstad B, Ugedal O (1998) Smolting of sea trout (Salmo trutta L.) in northern Norway. Aquaculture 168:341–349
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Finstad B, Staurnes M, Reite OB (1988) Effect of low temperature on sea water tolerance in rainbow trout, Salmo gairdneri. Aquaculture 72:319–328 Fleming IA, Jonsson B, Gross MR et al (1996) Experimental tests of the reproductive impact of farmed on wild Atlantic salmon (Salmo salar). J Appl Ecol 33:893–905 Folmar LC, Dickhoff WW (1980) The parr-smolt transformation (smoltification) and seawater adaptations in salmonids. Aquaculture 21:1–37 Foote CJ, Wood CC, Clarke WC et al (1992) Circannual cycle of seawater adaptability in Oncorhynchus nerka: genetic differences in smoltification of sympatric sockeye salmon and kokanee. Can J Fish Aquat Sci 49:99–109 Forseth T, Næsje TF, Jonsson B et al (1999) Juvenile migration in brown trout: a consequence of energetic state. J Anim Ecol 68:783–793 Franklin CE, Davison W, Forster ME (1992a) Seawater adaptability of New Zealand’s sockeye (Oncorhynchus nerka) and chinook salmon (O. tshawytscha): physiological correlates of smoltification and seawater survival. Aquaculture 102:127–142 Franklin CE, Forster ME, Davison W (1992b) Plasma cortisol and osmoregulatory changes in sockeye salmon transferred to sea water: comparison between successful and unsuccessful adaptation. J Fish Biol 41:113–122 Gorbman A, Dickhoff WW, Mighell JL et al (1982) Morphological indices of developmental progress in parr-smolt coho salmon, Oncorhynchus kisutch. Aquaculture 28:1–19 Handeland SO, Wilkinson E, Sveinsbø B et al (2004) Temperature influence on the development and loss of seawater tolerance in two fast-growing strains of Atlantic salmon. Aquaculture 233:513–529 Hansen LP, Jonsson B (1985) Downstream migration of reared smolts of Atlantic salmon (Salmo salar L.) in the River Imsa. Aquaculture 45:237–248 Hansen LP, Jonsson B, Morgan RIG et al (1989) Influence of parr maturity on emigration of smolts of Atlantic salmon (Salmo salar). Can J Fish Aquat Sci 46:410–415 Hasler AD, Scholz AT (1983) Olfactory imprinting and homing in salmon. Springer, Berlin Higgins PJ, Talbot C (1985) Growth and feeding in juvenile Atlantic salmon (Salmo salar L.). In: Cowey CB, Mackie AM, Bell JG (eds) Nutrition and feeding in fish. Academic, London Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall D (eds) Fish physiology, vol XIB. Academic, New York Høgåsen HR (1998) Physiological changes associated with the diadromous migration of salmonids, Canadian Special Publication of Fisheries and Aquatic Sciences 127. National Research Council, Ottawa Huntsman AG, Hoar WS (1939) Resistance of Atlantic salmon to sea water. J Fish Res Board Can 4:409–411 Hutchison MJ, Iwata M (1998) Effect of thyroxine on the decrease of aggressive behaviour of four salmonids during the parr-smolt transformation. Aquaculture 168:169–175 Ibbotson AT, Beaumont WRC, Pinder A et al (2006) Diel migration patterns of Atlantic salmon smolts with particular reference to the absence of crepuscular migration. Ecol Freshw Fish 15:544–551 Iigo M, Ikuta K, Kitamura S et al (2005) Effects of melatonin feeding on smoltification in masu salmon (Oncorhynchus masou). Zool Sci 22:1191–1196 Iwata M (1995) Downstream migratory behavior of salmonids and its relationship with cortisol and thyroid hormones: a review. Aquaculture 135:131–139 Järvi T, Holmgren K, Rubin RF et al (1996) Newly-emerged Salmo trutta fry that migrate to the sea – an alternative choice of feeding habitat? Nord J Freshw Res 72:52–62 Jensen AJ, Johnsen BO (1985) Growth and smolt age of Atlantic salmon (Salmo salar L.) in the glacier river Beiarelva, Northern Norway. Rep Inst Freshw Res Drottningholm 62:86–90 Jensen AJ, Johnsen BO (1986) Different adaptation strategies of Atlantic salmon (Salmo salar L.) populations to extreme climates with special reference to some cold Norwegian rivers. Can J Fish Aquat Sci 43:980–984 Johnston CE, Saunders RL (1981) Parr-smolt transformation of yearling Atlantic salmon (Salmo salar) at several rearing temperatures. Can J Fish Aquat Sci 38:1189–1198
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Porter MJR, Randall CF, Bromage NR et al (1998) The role of melatonin and the pineal gland on development and smoltification of Atlantic salmon (Salmo salar) parr. Aquaculture 168:139–155 Post JR, Parkinson EA (2001) Energy allocation strategy in young fish: allometry and survival. Ecology 82:1040–1051 Power G (1958) The evolution of the freshwater races of the Atlantic salmon (Salmo salar L.) in eastern, North America. Arctic 11:86–92 Power G (1969) The salmon of Ungava Bay. Arctic Institute of North America, Technical paper 22, Montreal Power G (1981) Stock characteristics and catches of Atlantic salmon (Salmo salar) in Quebec, and Newfoundland and Labrador in relation to environmental variables. Can J Fish Aquat Sci 38:1601–1611 Prunet P, Boeuf G, Bolton JP, Young G (1989) Smoltification and seawater adaptation in Atlantic salmon (Salmo salar): plasma prolactin, growth hormone, and thyroid hormones. Gen Comp Endocrinol 74:355–364 Raine JC, Hawryshyn CW (2009) Changes in thyroid hormone reception precede SWS1 opsin downregulation in trout retina. J Exp Biol 212:2781–2788 Refstie T, Steine TA, Gjedrem T (1977) Selection experiments with salmon. II. Proportion of Atlantic salmon smolting at 1 year of age. Aquaculture 10:231–242 Richards JG, Semple JW, Bystriansky JS et al (2003) Na+/K+-ATPase a-isoforms switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486 Ricker WE (1938) “Residual” and kokanee salmon in Cultus Lake. J Fish Res Board Can 4:192–218 Rikardsen AH, Thorpe JE, Dempson JB (2004) Modelling the life history variation of Arctic charr. Ecol Freshw Fish 13:305–311 Saunders RL (1965) Adjustment of buoyancy in young Atlantic salmon and brook trout by changes in swim-bladder volume. J Fish Res Board Can 22:336–352 Saunders RL, Henderson EB (1969) Growth of Atlantic salmon smolts and post-smolts in relation to salinity, temperature and diet. Fish Res Board Can Techn Rep 149:1–20 Saunders RL, Henderson EB (1970) Influence of photoperiod on smolt development and growth of Atlantic salmon (Salmo salar). J Fish Res Board Can 27:1295–1311 Saunders RL, Henderson EB (1978) Changes in gill ATPase activity and smolt status of Atlantic salmon (Salmo salar). J Fish Res Board Can 35:1542–1546 Schmitz M (1992) Annual variations in rheotactic behavior and seawater adaptability in landlocked Arctic char (Salvelinus alpinus). Can J Fish Aquat Sci 49:448–452 Seidelin M, Madsen SS, Byrialsen A et al (1999) Effects of insulin-like growth factor-I and cortisol on Na+, K+-ATPase expression in osmoregulatory tissues of brown trout (Salmo trutta). Gen Comp Endocrinol 113:331–342 Shrimpton JM, Björnsson BT, McCormick SD (2000) Can Atlantic salmon smolt twice? Endocrine and biochemical changes during smolting. Can J Fish Aquat Sci 57:1969–1976 Sigholt T, Asgard T, Staurnes M (1998) Timing of parr-smolt transformation in Atlantic salmon (Salmo salar): effects of changes in temperature and photoperiod. Aquaculture 160:129–144 Soivio A, Virtanen E, Mouna M (1988) Desmoltification of heat-accelerated Baltic salmon (Salmo salar) in brackish water. Aquaculture 71:89–97 Solbakken VA, Hansen T, Stefansson SO (1994) Effects of photoperiod and temperature on growth and parr smolt transformation in Atlantic salmon (Salmo salar L.) and subsequent performance in seawater. Aquaculture 121:13–27 Spencer RC, Zydlewski J, Zydlewski G (2010) Migratory urge and gill Na+, K+-ATPase activity of hatchery-reared Atlantic salmon smolts from the Dennys and Penobscot River stocks, Maine. Trans Am Fish Soc 139:947–956 Staurnes M, Lysfjord G, Berg OK (1992) Parr-smolt transformation of a nonanadromous population of Atlantic salmon (Salmo salar) in Norway. Can J Zool 70:197–199 Stefansson SO, Berge AI, Gunnarsson GS (1998) Changes in seawater tolerance and gill Na+, K+ATPase activity during desmoltification in Atlantic salmon kept in freshwater at different temperatures. Aquaculture 168:271–277
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Strothotte E, Chaput GJ, Rosenthal H (2005) Seasonal growth of wild Atlantic salmon juveniles and implications on age at smoltification. J Fish Biol 67:1585–1602 Sundell K, Jutfelt F, Ágústsson T et al (2003) Intestinal transport mechanisms and plasma cortisol levels during normal and out-of-season parr-smolt transformation of Atlantic salmon (Salmo salar). Aquaculture 222:265–285 Svärdson G, Fagerström Å (1982) Adaptive differences in the long-distance migration of some trout (Salmo trutta L.) stocks. Rep Inst Freshw Res Drottningholm 60:51–80 Symons PEK (1979) Estimated escapement of Atlantic salmon (Salmo salar) for maximum smolt production in rivers of different productivity. J Fish Res Board Can 36:132–140 Thorpe JE (1994) An alternative view of smolting in salmonids. Aquaculture 121:105–113 Thorpe JE (2007) Maturation responses of salmonids to changing developmental opportunities. Mar Ecol Progr Ser 335:285–288 Thorpe JE, Metcalfe NB (1998) Is smolting a positive or a negative developmental decision? Aquaculture 168:95–103 Thorpe JE, Ross LG, Struthers G et al (1981) Tracking Atlantic salmon smolts Salmo salar L. through Loch Voil, Scotland. J Fish Biol 19:519–537 Thorpe JE, Metcalfe NB, Fraser NHC (1994) Temperature dependence of the switch between nocturnal and diurnal smolt migration in Atlantic salmon. In: Mackinlay DD (ed) High performance fish. Fish Physiology Association, Vancouver Thorpe JE, Mangel M, Metcalfe NB et al (1998) Modelling the proximate basis of salmonid lifehistory variation, with application to Atlantic salmon, Salmo salar L. Evol Ecol 12:581–599 Tipsmark CK, Madsen SS, Seidelin M et al (2002) Dynamics of Na+, K+, 2Cl– cotransporter and Na+, K+ -ATPase expression in the branchial epithelium or brown trout (Salmo trutta) and Atlantic salmon (Salmo salar). J Exp Zool 293:106–118 Tipsmark CK, Jørgensen C, Brande-Lavridsen N et al (2009) Effects of cortisol, growth hormone and prolactin on gill claudin expression in Atlantic salmon. Gen Comp Endocrinol 163:1270–1277 Titus RG, Mosegaard H (1989) Fluctuating recruitment and variable life history of migratory brown trout, Salmo trutta L., in a small, Baltic coast stream. J Fish Biol 35(Suppl A):351–353 Titus RG, Mosegaard H (1992) Fluctuating recruitment and variable life history of migratory brown trout, Salmo trutta L., in a small, unstable stream. J Fish Biol 41:239–255 Uchida K, Kaneko T, Yamauchi K et al (1996) Morphometrical analysis of chloride cell activity in the gill filaments and lamellae and changes in Na+, K+-ATPase activity during seawater adaptation in chum salmon fry. J Exp Zool 276:193–200 Ura K, Mizuno S, Okubo T et al (1997) Immunohistochemical study on changes in gill Na+, K+ATPase a-subunit during smoltification in the wild masu salmon, Oncorhynchus masou. Fish Physiol Biochem 17:397–403 Wagner HH (1974) Photoperiod and temperature regulation of smolting in steelhead trout (Salmo gairdneri). Can J Zool 52:219–234 Webb PW (1984) Form and function in fish swimming. Sci Am 251:58–68 Wedemeyer GA (1996) Physiology of fish in intensive culture systems. Chapman & Hall, New York Wedemeyer GA, Saunders RL, Clarke WC (1980) Environmental factors affecting smoltification and early marine survival of anadromous salmonids. Mar Fish Rev 42:1–14 Woo NYS, Burns HH, Nishioka RS (1978) Changes in body composition associated with smoltification and premature transfer to seawater in coho (Oncorhynchus kisutch) and king salmon (Oncorhynchus tshawytscha). J Fish Biol 13:421–428 Wootton RJ (1998) Ecology of teleost fishes, 2nd edn. Kluwer, Dordrecht Young G (1988) Enhanced response of the interrenal of coho salmon (Oncorhynchus kisutch) to ACTH after growth hormone treatment in vivo and in vitro. Gen Comp Endocrinol 71:85–92 Zydlewski GB, Haro A, McCormick SD (2005) Evidence for cumulative temperature as an initiating and terminating factor in downstream migratory behavior of Atlantic salmon (Salmo salar) smolts. Can J Fish Aquat Sci 62:68–78
Chapter 6
Migrations
6.1 Organization of the Chapter Migration is long-distance movements made by many individuals more or less in the same direction and at the same time of the year (Endler 1977). The movements are normally followed by a return migration. Migrations are under genetic control (Northcote 1981; Svärdson and Fagerström 1982; Jonsson 1982; Kallio-Nyberg et al. 2002), but are also modulated by environmental influences experienced by the fish such as temperature and water flow extremes. Seasonal movements between spawning, wintering and feeding areas are characteristics of salmonid life histories (Fig. 6.1). The species exhibit both freshwater resident and anadromous populations. In brown trout, both sexes frequently mature and become freshwater resident instead of migrating to sea. For freshwater resident populations, the scale of such movements ranges from a few meters to many kilometres, between the natal rearing and spawning grounds to distant feeding and wintering areas. Post-smolts of anadromous populations remain during feed in estuaries and coastal waters. They seldom migrate to the ocean (Fig. 6.1a). Their sea sojourn lasts from a few months to 4–5 years, and occurs repeatedly until death. They spawn in fresh water and typically spend the winter in fresh and brackish water. Also Atlantic salmon can form freshwater resident populations, but have higher tendency than brown trout to form anadromous populations making excursions for feeding at sea. Post-smolts spend 1–4 years in the ocean before attaining sexual maturity and returning to fresh water for spawning (Fig. 6.1b). Post-spawners (kelts) can return to sea for feeding soon after spawning or wait until the subsequent spring before returning to their feeding area at sea. The same individual can spawn in up to at least four different years. The Atlantic trouts migrate because dissimilar habitats are suitable for reproduction, feeding and shelter during adverse conditions. Hence, individual fish can maximize their fitness by moving between habitats at appropriate times of the year. To what degree a population undertakes the various migrations depends on the nature of its habitats. Their iteroparous life histories distinguish them from Pacific salmon.
B. Jonsson and N. Jonsson, Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories, Fish & Fisheries Series 33, DOI 10.1007/978-94-007-1189-1_6, © Springer Science+Business Media B.V. 2011
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(a)
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(b)
Fig. 6.1 Schematic illustration of the seasonal migratory pattern of (a) brown trout and (b) Atlantic salmon. Further explanation is given in the text
The nursery area of Atlantic salmon and brown trout is usually streams and rivers (see Chap. 3). These habitats are suitable for early juvenile feeding and as refuge for small individuals. But to grow large they often seek better feeding opportunities. If lakes are present, they can move there for feeding, and brown trout can also feed in estuaries. Atlantic salmon can feed in lakes, but to grow really large, they smolt and migrate to feeding areas in the ocean. In this chapter, we describe migrations performed by the two species and how they can differ among populations and species. Time of migration depends on environmental conditions, fish size and distance between the habitats used. For instance, there are pre-smolt migration with the autumn flood and smolt migration with increasing temperature and/or flow in spring, and return migrations influenced by similar variables, and smolt migrations with increasing day length and temperature in spring. Migration can be obligatory or optional. Anadromous Atlantic salmon females move to sea for feeding. Males of anadromous populations, on the other hand, split environmentally and can either stay in fresh water throughout life or move to sea for feeding. In anadromous brown trout, migration is truly optional for both sexes, indicating that the fitness is similar for individuals selecting any of the two life history tactics (Jonsson 1981). Here, we discuss to what degree the migratory tendency is inherited or a conditional life history tactic or both. We also elucidate why sexes can differ in migratory tendency.
6.2 Migration
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The homing of salmon through open ocean with few if any fixed point for navigation is one of the great wonders of nature (Harden Jones 1968). It seems reasonable to suggest, for instance, that Atlantic salmon need some sort of compass orientation, whether this is magnetoreception or visual signals from celestial objects, sun and polarized light included, to find the coast of Europe or North America. From there, to find the right estuary and river, they may use olfaction and vision as well as unidirectional flow in rivers and the tidal stream currents in the sea (Hasler and Scholz 1983). The literature on salmonid homing is extensive, but the mechanisms involved are not yet fully understood. How accurately do salmonids return to their natal river? A majority of the returning adults appear usually to enter their river of origin, but some fish move into another river. Precise homing is fundamental for isolation between populations and genetic adaptation to local environments. Straying is a way by which new rivers are colonized and genetic variation maintained. Based on published literature, we discuss whether this is a navigational mistake or a strategy particularly for fish inhabiting small or unstable systems. We finalize the chapter by describing how released hatchery salmon migrate in nature, and reasons for why they stray more to other rivers than wild conspecifics.
6.2 Migration To successfully reach their destination, migratory fish must have evolved an appropriate genetic program coding for suitable developmental, morphological, physiological, biomechanical, behavioural and life-history traits. They must respond to environmental changes or reproductive requirements and interact successfully with biotic and abiotic factors in their environment. Important questions are why, when, where, how and which fish migrate? We see why fish migrate in relation to the problem of habitat selection and costs and benefits associated with utilizing different localities. The question about when is not only related to the resource development in optional environments, but also when the fish can move safely and efficiently between them. The fish may be either transported between areas with the help of currents, move actively themselves, or use a combination of the two, and the movement can be vertical to another depth layer, or horizontal between different geographical areas. The answer to the question about which fish migrate is chiefly related to the physiological state of the organisms. In the following, we summarize knowledge related to the questions presented above.
6.2.1
Habitat Selection
Mobile organisms are expected to select the most profitable habitat or geographical area. Fish should use the habitat where the relationship between mortality, m, over growth, g, is lowest, i.e. minimizing m/g (Werner and Gilliam 1984). The relative
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value of habitats in terms of survival and growth often changes seasonally or in relation to the developmental stage of the individual. Thus selection can favour migration and habitat change. However, animals are only experiencing the situations where they currently are, and do not know the conditions in distant feeding areas or spawning grounds. Migrants must therefore rely on cues present to bias their movements towards the appropriate heading (Dodson 1988). Predictive information about environments is based on the interaction between personal experience and instinct. The latter is fine tuned through natural selection. Growth can be limited by low food availability. When growth is restrained, sexual maturation usually occurs as soon as possible after the inflection point of the growth curve is reached (Jonsson and Jonsson 1993). An alternative is that the fish can switch to a new feeding niche within the habitat or migrate to a more distant habitat where feeding opportunities are so much better that the improved growth more than balances any increased migratory costs and mortality risk, i.e. minimizing m/g. In this case, maturity should be delayed if the overall lifetime fitness thereby is increased (see Sect. 6.6).
6.2.1.1
Benefits of Migration
An advantage of migration can be access to better feeding opportunities (Gross et al. 1988; Frier 1994), or avoidance of adverse environmental conditions such as during winter when icing-up of streams or low water flow can cause high mortality in northern rivers. Due to the improved feeding opportunities in an alternative feeding habitat, environmentally constrained growth due to high population density and intraspecific competition can be released (Jonsson 1985). With larger body size, gonadal production and reproductive success are increased (Hutchings and Myers 1985; Gross 1987). For instance, mean fecundity of sea migratory brown trout females from Vangsvatnet Lake, Norway was estimated at 1,790 eggs. Mean fecundity of the corresponding residents was 330 eggs, or less than 20% of that of the sea-run fish (Jonsson 1985). This means that an advantage of migration is a five-time increase in fecundity. In addition, egg size increases with the size of the parent, and with that, early offspring growth and viability (Einum and Fleming 1999). Similar advantages of migration have been found for other salmonids such as rainbow (steelhead) trout, Dolly Varden charr, Arctic charr, brooks charr and sockeye salmon (Hutchings and Morris 1985).
6.2.1.2
Costs of Migration
On the other hand, migration augments energy use and leads to increased mortality. For anadromous brown trout in streams, Jonsson and Jonsson (2006) illustrated this by showing that the condition factor of anadromous brown trout decreased with increasing migratory distance inland (Fig. 6.2a). Also, the gonadosomatic index of males [IG = 100 (mass of gonads/somatic mass)], but not females, decreased with
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251
Fig. 6.2 Relationships between (a) condition factor (CF%) and migratory distance (D km) of Norwegian first-time spawning anadromous brown trout (Regression line: CF = −0.004D + 1.026, r2 = 0.89, P 0.04 m3 s−1) in southern Norway. Such early smolting and emigration from small streams may be an adaptation to drought and low water levels in the nursery stream.
6.2.2
When Migrate?
Fish should migrate at a time maximizing fitness. For instance, fish migrate when they approach growth constraints in their present habitat. By investigating the energy budget of brown trout migrating from a tributary to Lake Femund, Forseth et al. (1999) found that prior to migration the proportion of the surplus energy available for growth was much lower in migrant than non-migrant fish (cf. Fig. 3.7). In this case, the migrants were among the largest of the cohorts. This finding indicated that they migrated to the lake to escape food constraints in their present habitat. Small individuals of similar age seemed less constrained by the present feeding opportunities. On the other hand, fish that move early are small and the mortality risk probably higher than for larger individuals, decreasing their expected fitness in the alternative lake habitat. Thus, age and size for the time of migration should be adapted through natural selection. The precise seasonal time of migration, however, is regulated by environmental cues such as photoperiod, temperature and water flow (cf. Sect. 6.4).
6.2 Migration
6.2.3
255
Which Fish Migrate?
Within populations, fast growers often migrate at younger age, and smaller sizes than slow growers (cf. Fig. 7.4b). Thus, there may be an inherited association between migration and growth rate (Gunnes and Gjedrem 1978; Refstie and Steine 1978). Furthermore, metabolic requirements vary among individuals: fast growers need more energy than similar-sized slow growers. Experiments indicate that initially fast-growing Atlantic salmon parr already have higher metabolism at the egg stage than slower-growing parr from the same brood (Metcalfe et al. 1992). This supports the results of Forseth et al. (1999) that fast growers are constrained by scarcity of food sooner and smaller than slow growers, and should at an earlier age and smaller size migrate to richer feeding opportunities, as also found for partially migratory sockeye salmon (Ricker 1938). However, sometimes it is the smallest and not the largest individuals in cohorts that migrate. This was observed for Arctic charr from Visjön, Sweden, and may also occur elsewhere. In such cases, larger individuals may have access to a richer food source making migration less profitable, or they may be in an adult stage where the opportunity for migration is lost. Populations can also be environmentally split between residents and movers. This is further described in Sect. 6.6.
6.2.4
Vertical Migrations
There is little knowledge about a possible diel, vertical migration associated with shifting light intensity from Atlantic salmon or brown trout in fresh water, contrasting observations from some other salmonids such as sockeye salmon and Dolly Varden charr (Clark and Levy 1988; Andrew et al. 1992). These fishes stay closer to the surface during the night than during the day, and the vertical migrations probably reflect a dynamic strategy minimizing the ratio of predation risk to forage gain that changes during the diel cycle, particularly in pelagic ecosystems (Scheuerell and Schindler 2003). But both brown trout and Atlantic salmon may very well perform diel vertical migrations as observed in hatchery-reared, farmed Atlantic salmon in response to shifting light intensity. This has been observed both for first-feeding alevins in fresh water (Stefansson et al. 1990) and during feeding in net pens at sea (Huse and Holm 1993). In marine net pens in summer, farmed Atlantic salmon stay closer to the surface when they feed than when they do not feed, and even 20-m-deep nets are not deep enough to cover the range of vertical movements. The fish do not perform the same vertical movements during winter when they starve, and the main environmental factors impacting this vertical migration appears to be temperature, food, and light intensity (Fernö et al. 1995; Juell and Fosseidengen 2004; Johansson et al. 2006; Oppedal et al. 2007; Føre et al. 2009).
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Further, farmed salmon released into nature stay closer to the surface during the night than during the day in summer (Skilbrei et al. 2009). It is not known whether this behaviour is influenced by previous experience from the fish farm, as the data from nature are variable. Reddin et al. (2006) observed that post-smolts swam deeper during the day than at night, and suggested that they thus avoided bird predators. Furthermore, Reddin et al. (2004) found that in two of three Newfoundland stocks, Atlantic salmon kelts spent more time in warm water close to the surface at night than during the day. However, Sturlaugsson and Thorisson (1997) observed that spawning migrants along the coast of Iceland were closest to the surface around noon, and Karlsson et al. (1996) failed to find any diurnal pattern in depth preference of Atlantic salmon during the spawning migration in the Baltic Sea. Thus, there may be adaptive differences among populations, or differences related to their ontogeny or prior experience of the fish. Migrating salmonids are known to perform occasional vertical dives (Sturlaugsson 1995; Sturlaugsson and Thorisson 1997; Karlsson et al. 1996). Although the fish spend most of their time in near-surface water, such excursions can go down to more than 100 m depth. This is not recognized as vertical migration, but may be helpful in controlling depth and navigating during horizontal migrations (Westerberg 1982). Horizontal migrations, on the other hand, are well known in Atlantic salmon and brown trout. These are feeding migrations, wintering migrations, and spawning migrations, and there is a close relationship between habitat selection and these migrations; these are described in more detail below.
6.3 Horizontal Migrations Salmonids migrate between areas in fresh water, and between fresh and salt water and at sea. Migrations in fresh water are often denoted potamodromous as ‘potamo’ means ‘river’ and ‘dromos’ means ‘running’ in Greek. Salmonid parr in small streams can also move between fresh and brackish water to escape summer drought and have thus an amphidromous behaviour (‘amphi’ means ‘both’ in Greek). But the most conspicuous horizontal salmonid migration is the diadromous migration (‘dia’ is ‘between’ in Greek) between salt and freshwater. Species that migrate to sea for feeding and return to freshwater for spawning are called anadromous (‘ana’ is ‘up’ in Greek), species that migrate to fresh water for feeding and return to sea water for breeding are called catadromous (‘kata’ is ‘down’ in Greek).
6.3.1
Potamodromous Migrations
The habitat use of brown trout varies with the environment, whether it is an isolated brook, or a brook connected to a larger river, as described for brown trout in the Søre Osa river system, eastern Norway (Jonsson and Sandlund 1979). There, brown
6.3 Horizontal Migrations
257
trout used the small tributary, Østre Æra, as spawning and nursery grounds and migrated to the larger River Søre Osa for feeding. The young of lake-feeding brown trout that spawn in inlet or outlet streams perform an alternative migration when they move from the natal feeding grounds into the lake as they grow older (Arawomo 1981; Haraldstad and Jonsson 1983; Schei and Jonsson 1989; Forseth et al. 1999; Jonsson et al. 1999). For instance, Näslund (1993) describes such a life history from Lake Storvindelen, northern Sweden. This lake supports a population of freshwater migratory brown trout (Näslund 1993). Spawning and early rearing take place in the main river, Vindelälven, whereas most of the growth takes place in Lake Storvindelen. But in early spring, brown trout often leave ice-covered lakes to feed in warmer inlets for a few days before returning to the lake. This phenomenon was denoted spring gracing by Sømme (1941). During the summer, they can migrate to feed in rich distant lakes, when such are available, and return to their home area for spawning when sexually mature. At what age do migratory brown trout leave the nursery stream? The first-summer old brown trout often remain in their natal habitat, but if they have access to better growth opportunities in a larger river or a lake, many age-0 fish can move there (Jonsson and Sandlund 1979; Jonsson 1989). Jonsson and Gravem (1985) reported that the largest first-year parr moved lakewards first. In the lake, the youngest parr stay in littoral waters, but as they grow older and larger they disperse into sub-littoral and pelagic areas. Lake feeding populations typically spend the winter in the littoral zone. The wintering migration occurs from the tributaries and pelagic lake waters to the shallow water where the fish remained until shortly before ice break-up, when they again dispersed (Fig. 6.4a). Bagliniére et al. (1994) reported that first-year old brown trout moved from a nursery stream to the larger River Scorff in France, and Thorpe (1974) and Arawomo (1981) observed a displacement of first and second year old brown trout from tributaries into Loch Leven, Scotland. However, in other cases, the movers may be older, particularly if there are predators such as pike, Esox lucius L., present in the lake the fish are heading for. For instance, in Lake Femund, south-east Norway, most brown trout leave the tributaries mainly at ages 2 (40%) and 3 (27%) years, and with a total range of variability from 1 to 8 years (Jonsson et al. 1999). Brown trout spawning in the afferent stream to Windermere, the largest natural lake in England, migrated to the lake at ages 1 + (16% of the population), 2 + (70%) and 3 + years (14%) (Craig 1982). Thus, in addition to improved feeding opportunities, mortality risk appears to influence the age when fish leave their nursery area. Also Atlantic salmon can move between habitats in fresh water, from the main river to tributaries in spring, and return in the autumn (Erkinaro 1995; Johansen et al. 2005) and from tributaries into lakes in summer, where they feed together with brown trout in the littoral zone. They typically return to running water in the autumn when they stay in a relatively large river (Fig. 6.4b). The oldest and largest parr seem to move earlier in the season than smaller individuals, and they may also move farther away from their nursery area. For instance, 2-year-old parr entered Vangsvatnet in June whereas 1-year-olds first appeared in August (details in Sect. 3.3.1.2).
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(a)
RIVER
LAKE Summer Feeding Autumn Wintering
Small streams Juvenile rearing Spawning Autumn Spawning
Summer Feeding
Littoral zone
Pelagic zone
Feeding/wintering Autumn Spawning Autumn Wintering
Spring/summer Feeding
Larger river
Summer Feeding
Feeding Autumn Wintering
Sub-littoral zone Feeding
Feeding/wintering
(b) Small tributaries Feeding Autumn Wintering
Summer Feeding
Large river Juvenile rearing Spawning/wintering
Summer Feeding
Littoral zone Feeding Autumn Wintering
Fig. 6.4 Wintering migrations of brown trout and Atlantic salmon parr in the Vosso River. (a) Brown trout move from tributaries and the pelagic zone to the littoral zone of the lake in November-December and return from March onwards. (b) Atlantic salmon parr move from the littoral zone of the lake to the main tributary in November-December and return to the lake during April–August (Based on information in Figs. 3.10 and 3.13)
6.3.2
Anadromous Migrations
Most Atlantic salmon populations are anadromous, and anadromy is also common in brown trout (McDowall 1988). The tendency to smolt and migrate is adaptive (Jonsson 1982). To spread in populations, anadromy must maximize the lifetime product of reproductive success and survivorship. The gain in fitness from using a second habitat minus migratory and physiological costs of moving and being able to regulate the ionic content in both fresh and salt water must exceed the fitness obtained from living only in fresh water. In some populations of brown trout anadromy appears obligatory, but as in most populations, anadromy is facultative (Jonsson et al. 2001). Natural mortality is typically higher at sea than in fresh water, especially for eggs and young stages. For brown trout, ionic regulation in cold sea water is also difficult (Finstad et al. 1988; Koed et al. 2007). Thomsen et al. (2007) concluded that low temperature compromises the hypo-osmoregulatory ability of anadromous brown trout, as indicated by insufficient compensatory adjustments of ion-transport mechanisms at least partly driven by compromised osmoregulatory physiology. But because other members of a population remain in sea water, the phenomenon may also reflect diverging life strategies. The decision whether individual gain greater advantage from migration or residence depends on the balance between growth and mortality (Jonsson 1981; Jonsson and Jonsson 1993; Thorpe 1994). The greater
6.3 Horizontal Migrations
259
fecundity of anadromous fish and reduced mortality of eggs, embryos, and parr in fresh water are the apparent rewards for undertaking the risks of anadromy (Gross 1987; Gross et al. 1988). 6.3.2.1
Pre-smolt Migration to Sea
Parr of brown trout and Atlantic salmon can move to brackish water. This can occur as early as within their first year (Landergren 2004; Pinder et al. 2007), but also later, for instance during high autumn flows as observed in the Girnock Burn, Scotland (Youngson et al. 1983) and the River Imsa (Jonsson and Jonsson 2002). In the River Imsa, relatively more pre-smolt brown trout than Atlantic salmon move downstream during the autumn flood (Jonsson and Jonsson 2009), probably because Atlantic salmon defend fast currents better than brown trout due to their more stream-lined body form and larger pectoral fins; morphological adaptations to life in stronger water currents. The sea survival of the autumn migrating pre-smolts can most years be very low (Jonsson and Jonsson 2009), possibly because they have poor ability to regulate their ionic concentration in cold sea water (Hoar 1988; Zydlewski et al. 2005; Thomsen et al. 2007). Salmonid parr tend to escape droughts and floods by moving, but the direction of movement may vary among populations and appears to depend on stock-specific adaptations and the life stage of the fish. At very high autumn and winter flows, pre-smolts can be displaced downstream to sea, although they are unable to properly regulate their ionic concentration in sea water. In such cases, their sea survival should be very low. In Britain, it was found that as much as 25% of the Atlantic salmon parr could move from rivers into tidal rearing-habitats in the autumn at age-0 and older (Pinder et al. 2007; Riley et al. 2008). It is not known to what extent parr of Atlantic salmon survive when they enter brackish water in the autumn, but obviously these fish are not physiologically adapted for survival in full sea-water strength (35 psu) (Riley et al. 2008). Juvenile hatchery-reared Atlantic salmon parr, released to sea at the outlet of the River Imsa in autumn and winter, exhibited poor survival and homing ability (Hansen and Jonsson 1989, 1991a), indicating that such early displacement can be maladaptive. In small streams supporting anadromous brown trout, the migration to lower parts is often initiated early in spring, and the fish stay in pools near the outlet. There, the smolting process is completed and the fish apparently wait for the suitable time for seaward migration. In very long rivers, the smolt migration must start early so that the fish can enter the sea when environmental conditions there are suitable. Such adaptations should be most pronounced in localities at the edge of the distribution area where conditions for seaward migration may be suitable only during a very short time window (Power 1958, 1969). 6.3.2.2
Smolt Migration
Anadromous brown trout (sea trout) migrate to the estuary or coastal areas for feeding (Jensen 1968; Jonsson 1985; Berg and Berg 1987; Jonsson and Jonsson 2002).
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Fig. 6.5 (a) Downstream Wolf trap in the River Imsa catching all salmonids longer than ca. 10 cm in body length. (b) The opening to the box trap is on the right side of the stream besides the Wolf trap (arrow). (c) A fish ladder leads upstream migrating fish into the box trap in the basement of the small red house upstream the Wolf trap on the right bank of the river
The smolts usually move downstream in small schools. The duration of the migratory period varies, but in small systems such as the River Imsa, where the fish migrations are monitored by use of fish traps (Fig. 6.5), most Atlantic salmon smolts move downstream during 2 weeks in early to mid May, and the entire smolt migration period lasts for about 1 month (Fig. 6.6). In larger, more complicated systems, the period with downstream migrating smolts can last longer. For instance, in the Tana River, northern Norway, the smolt migration period lasts about 1.5 months, and in the Burrishoole system, western Ireland, the mean duration of the annual smolt run lasted approximately 100 days during 1970–2000 (Byrne et al. 2003). There is a tendency to earlier emigration at low than high latitudes. In the Girnock Burn, Scotland (57° N), most smolts leave the stream in April. In southern rivers, the smolts must escape into the sea before the river temperature becomes too high or the water level too low for migration and survival. In the Hals River (70° N), northern Norway, the smolts move to sea in July. Thorpe and Morgan (1978) hypothesized that downstream migration of smolts is passive and related to a smolting-associated reduction in swimming stamina. Their results indicated that Atlantic salmon smolts would not swim at speeds greater than 2 body lengths (BL) s−1 (approximately 0.3–0.4 m s−1). Tytler et al. (1978) and Thorpe et al. (1981) proposed that Atlantic salmon smolts were
6.3 Horizontal Migrations
261
Fig. 6.6 Time of the seaward migration of Atlantic salmon smolts in the River Imsa in year with early (1980), medium (1976) and late (1979) smolt run. Most smolts descend within 2 weeks (From Jonsson and Ruud-Hansen (1985). Reproduced with permission of Canadian Journal of Fisheries and Aquatic Sciences)
unable, or unwilling, to maintain their position in spring run-off currents and were therefore passively displaced downstream to the ocean. However, Peake and McKinley (1998) re-examined the swimming capacity of Atlantic salmon smolts. They found that the smolts swam indefinitely against current up to 1.26 m s−1, maintained velocities as high as 1.64 m s−1 for 2–10 min, and made short bursts at speeds up to 1.95 m s−1, which is about 10 BL s −1. The huge difference between these results may be because Thorpe and Morgan (1978) used hatchery smolts that had not previously been exposed to high current velocities and were therefore not behaving adequately when challenged by fast current velocities (e.g. see Youngson et al. 1989a). Evidence indicates that the water flow provides downstream movement of the juvenile fish. Hansen and Jonsson (1985) found that Atlantic salmon smolts actively move out into the main current of the river to avoid being caught by backwaters and sloughs. Svendsen et al. (2007) showed that smolts migrated in a non-random spatial pattern independently of stream discharge distributions. Vertically, brown trout and Atlantic salmon smolts often exhibit preference for bottom-orientated positions in the river. Horizontally, all smolts preferred the mid-channel positions. These discharge-corrected preferences for certain spatial positions suggest that smolt emigration is not a matter of passive displacement. Moore et al. (1998) followed Atlantic salmon smolts downstream the River Test, England. They found that the smolts moved close to the surface and within the fastest moving section of the water talweg, similar to observations by Davidsen et al. (2005). Furthermore, smolts
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migrate more quickly during high than low water flows (Youngson et al. 1989b). Raymond (1968) compared the migration rate of yearling Chinook salmon in the Snake and Columbia Rivers during periods of low and moderate discharges. The rate of migration was directly related to the current velocity, i.e. 21 km day−1 at low and 37 km day−1 during moderate river discharges. A similar result was found in yearling Chinook salmon and steelhead trout in the lower Snake River, where the travel time was strongly correlated with water flow (Smith et al. 2002; Connor et al. 2003b). Thus, the seaward migration is not passive, but current velocity has major impact on the speed of river descent. Brown trout can migrate to sea concurrently with or slightly before Atlantic salmon (Nordeng 1977; Berg and Jonsson 1989). The period of seaward migration of brown trout can be less concentrated than that of Atlantic salmon, as observed in the River Imsa (Jonsson and Jonsson 2009). The smolt migration period is typically preceded by the seaward migration of veteran migrants spending the winter in the river. In brown trout the veteran migrants can be immature and/or spent fish, in Atlantic salmon it is spent individuals (kelts) only. The seaward migration often starts in cool temperatures in spring (Table 6.1). In the Imsa, the seaward migration begins at water temperatures between 5°C and 11°C and ends at temperatures about 15°C (Jonsson and Ruud-Hansen 1985). In the River Orkla, mid-Norway, migration begins at water temperatures as low as between 2°C and 4°C (Hesthagen and Garnås 1986; Hvidsten et al. 1995), similar to that in the Girnock Burn, Scotland (Youngson et al. 1983). On the other hand, in the Arctic Porya River, Russia, the smolts migrate to sea at water temperatures between 15°C and 20°C (Bakshtansky et al. 1980, 1983). Thus, there is no universal temperature initiating the annual smolt run. Rather, it varies among populations, and also among years in the same river, as temperature is not the only factor influencing the time of the smolt run. Table 6.1 Water temperatures at the beginning of the smolt migration of Atlantic salmon River Temperature °C Reference Alta 10 Næsje et al. (1998) Burrishoole 5–8 Byrne et al. (2003) Chapoma 8.5 Melnikova (1970) Girnock Burn 1–5 Youngson et al. (1983) Imsa 5.8–11.2 Jonsson and Ruud-Hansen (1985) Luvenga 8–13 Leonko and Chernitsky (1986) Orkla 1.7–4.4 Hvidsten et al. (1995) Penobscot 5–9 Fried et al. (1978) Piddle 10–12 Solomon (1978) Porya 15–20 Bakshtansky et al. (1980, 1983) Tana 10 Erkinaro et al. (1998) Umba 9–9.5 Melnikova (1970) Varzuga 8–13 Veselov et al. (1998) West 5–8 Whalen et al. (1999)
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263
Differences in the time of the smolt migration appear to be genetic. For instance, in Canada Riddell and Leggett (1981) observed that juvenile Atlantic salmon from a tributary distant from the sea started their migration sooner than those growing up in a tributary closer to sea. Similarly, Stewart et al. (2002) reported that smolts from an upper tributary of the River Tay, Scotland started to migrate sooner than those farther downstream. Furthermore, when alevins derived from the lower tributary were transferred to a location in the upper catchment, smolt migration was later than for native fish. Likewise, when alevins from the two populations were stocked in a common, upper catchment location, fish originating from the lower tributary migrated at a later date. These differences are indicative of a genetic basis for the timing of smolt migration and suggestive of local adaptation. Individuals entering sea water when growth opportunities are good and predator presence low are probably favoured by natural selection.
6.3.2.3
Veteran Migrants
Atlantic Salmon Post spawning anadromous Atlantic salmon (kelts) can enter the estuary from shortly after spawning is finished in the autumn until the subsequent summer. Kelts from populations spawning in small streams (0.5–3 m3 s−1) typically leave right after spawning. The population in the River Imsa (5.1 m3 s−1) is split between fish moving to sea soon after spawning and individuals that spend the winter in the river and move to sea between March and May in the subsequent spring (Fig. 6.7), when the water temperature is between 4°C and 10°C (Jonsson et al. 1990b). The relative
Fig. 6.7 Mean monthly descent (%) of post-spawning male (broken line) and female (solid line) Atlantic salmon in the River Imsa between November and May 1976–1988 (From Jonsson et al. (1990b). Reproduced with permission of Elsevier B.V.)
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amount of fish moving to sea in the autumn relative to spring can be influenced by water level and temperature after spawning. In large rivers such as the River Drammen (300 m3 s−1), kelts usually spend the winter in the river and survivors return to sea for feeding in the subsequent spring. Autumn emigrating Atlantic salmon kelts can move to their feeding areas in the north Atlantic in late autumn and winter. This has been shown by recaptures of tagged fish from the River Imsa caught in the fishery north of the Faroe Islands only a few weeks after they left the river. Svärdson (1966) maintains that relatively more kelts move to sea in autumns with low water level and high temperature than when there is more water and lower temperature. This may both hold within and among rivers. Brown Trout Anadromous brown trout can spend the wintering in fresh water and return to sea in early spring (Went 1949, 1967; Alm 1950; Jensen 1968; Campbell 1977). In the river, they usually dwell in pools in the river or a lake adjacent to the spawning area in the river. This is often observed in streams that have suitable wintering habitats. Usually, such fish migrate to sea in the subsequent spring prior to the main smolt migration (Alm 1950; Berg and Jonsson 1989; Jonsson and Jonsson 2002, 2009), and old and large individuals tend to migrate earlier than younger and smaller ones (Nordeng 1977; Jonsson 1985; Jonsson and Gravem 1985; LeCren 1985; Potter 1985; Rasmussen 1986; Bohlin et al. 1993, 1996), as illustrated by brown trout leaving the River Vardneselva, northern Norway (69° N) (Fig. 6.8). In this system, the smolts and veteran migrants leave the river in the spring/early summer and
100 90 80
Per cent
70 60 50 40 30 20 10 0 A
M
J
J
A
S
Months Fig. 6.8 Cumulative catch of first time migrant (broken line) and veteran migrant brown trout (solid line) moving from fresh to salt water in May–June and return to the River Vardneselva, northern Norway, between July and September (From Berg and Jonsson (1989). Reproduced with permission of Springer Verlag)
6.3 Horizontal Migrations
265
return after approximately 2 months at sea. The fish spend the winter in lakes in the river system. In small streams without lakes (70 cm long) do not enter the river before the flow starts to increase in the autumn, at approximately 10 m3 s−1. Onesea-winter salmon (