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Fisheries Research
j o u r n a l h o m e p a g e :w w w . e l s e v i e r . c o m / l o c a t e / f i s h r e s
Gender-specific responses of mature Atlantic cod (Gadus morhua L.) to feed deprivation
Tatiana N. Ageeva
a,c,∗, Malcolm Jobling
b, Ragnar L. Olsen
c, Margrethe Esaiassen
caNofimaAS,Muninbakken9-13,Breivika,P.O.Box6122,NO-9291Tromsø,Norway
bTheDepartmentofArcticandMarineBiology,UiTTheArcticUniversityofNorway,N-9037Tromsø,Norway
cNorwegianCollegeofFisheryScience,UiTTheArcticUniversityofNorway,N-9037Tromsø,Norway
a r t i c l e i n f o
Articlehistory:
Received6September2016
Receivedinrevisedform5December2016 Accepted12December2016
HandledbyGeorgeA.Rose
Keywords:
Live-storedcod Starvation Weightloss Filletprotein Sexdifferences
a b s t r a c t
Atlanticcod(GadusmorhuaL.)isoneofthemostimportantcommercialfishspeciesinNorwayand thepeakfishingseasoncoincideswithspawningfromJanuarytoApril.Live-storageofcodmayextend themarketingseasonforfreshcodproducts.Codcanbeheldforupto12weeksaftercapture,and currentregulationsallowthefishtobeheldwithoutfeedingforfourweeks.Weinvestigatedwhether theresponsetolong-termfeeddeprivationdifferedbetweenmaturemalesandfemales.Thefish,caught offAndenes(Norway)inMarch2015usingDanishseine,wereheldwithoutfeedingfor82days,and samplesweretaken2,26,54and82daysaftercapture.Ateachsampling,theweightsofwholeand guttedfish(headon),liverandgonadsweremeasured.Additionally,filletproteinconcentrationswere analysed.Femaleslosttotalweight,guttedweightandlivermassmorerapidlythanmales,butthe reductioningonadmasswassignificantlyhigherinmalesthaninfemales.Attermination,after82days, filletproteinconcentrationinmaleswashigher(16.3%±0.4)thaninfemales(14.9%±0.4).Withregard tolossofguttedweightandreductioninmuscleproteinconcentration,thetolerablefastingperiodof maturespawningAtlanticcodofgoodbiologicalconditionis54days,butthiscanvarydependingon upontheinitialconditionofthefish
©2016ElsevierB.V.Allrightsreserved.
1. Introduction
Atlanticcod(GadusmorhuaL.)is oneofthemostimportant commercialspeciesinNorwaywithseasonalsuppliesbeinglinked to the annual spawning cycle. Northeast Atlantic cod migrate fromfeedingareasintheBarentsSeatotheNorwegiancoastto spawn,andspawningoccursfromtheendofJanuarytoApril/May (NordeideandBåmstedt,1998;Brander,2005).Mostcodarecaught duringthefirstfivemonthsoftheyearandthesupplyoffreshcodis limitedfortheremainderoftheyear.Extendingtheseasonthrough live-storagecouldcreatenewpossibilitiesformarketingfreshcod products.
Atlanticcoddisplaynaturalseasonalvariationsinweightand conditionrelatedtofishsize,seasonalfeedingpatternsandspawn- ing(FordhamandTrippel,1999;SchwalmeandChouinard,1999;
MelloandRose,2005),withsomaticweightandconditionusually decreasingduringmaturationandspawning.Codisaleanfishand
∗Correspondingauthorat:Muninbakken9-13,Breivika,P.O.Box6122,NO-9291 Tromsø,Norway.
E-mailaddress:tatiana.ageeva@nofima.no(T.N.Ageeva).
theliveristhemainorganforenergystorageintheformoflipids (Love,1988).Variationsinliverweightcanbelinkedtofoodsup- ply(BlackandLove,1986;Joblingetal.,1991),andifthefishare deprivedoffood,liverlipidsaremobilizedandusedasanenergy source.Muscletissue,primarilymuscleprotein,isalsomobilised (BlackandLove,1986).
MostAtlanticcodtakenintheNorwegiancoastalfisheriesare caughtinspringduringthespawningseason.Norwegianregula- tions(FOR-2004-12-22-1878,2004)allowwild-caughtfishtobe heldinseacagesforupto12weeks,withaninitialfourweeks withoutfeeding.Itiscurrentlyunknownwhatimplicationsthese regulationshaveforthewelfareofthelivefishandfilletquality afterslaughter.Consequently,itisofinteresttoinvestigatechanges that occurwhen maturecod areheld without foodfor several weeks,andtoexaminewhethertherearegender-specificdiffer- ences.Atpresent,littleisknownabouthowthenutritionalstatus offemalesandmalesaffectsmobilizationandutilizationofenergy reservesduringfeeddeprivation.
Theobjectiveofthepresentstudywastoinvestigatewhether maturefemaleandmaleAtlanticcoddifferintheirresponsesto feeddeprivationduringthespawningandpost-spawningperiods.
http://dx.doi.org/10.1016/j.fishres.2016.12.010 0165-7836/©2016ElsevierB.V.Allrightsreserved.
Biologicaldataofexperimentalfishsampledatdifferenttimesduringfeeddeprivation.
Fooddeprivation
Sampling 2days 26days 54days 82days
Sex ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂
N 10 15 21 39 20 40 20 40
Bodyweight(g) 6730±471 6881±641 6543±340 6048±284 5827±309 5506±218 4772±311 4914±256
range 4780–9400 3140–11340 3452–10106 2708–9640 2902–8024 2738–8626 2474–7342 2168–8094
Bodylength(cm) 91.3±2.2 90.1±2.6 91.9±1.6 89.2±1.3 92.7±1.9 89.4±1.2 89.1±1.9 87.3±1.4
range 79–102 74–103 75–104 72–104 75–104 66–99 70–104 67–104
HSIa 5.4±0.6 4.7±0.5 6.1±0.4 4.3±0.3 5.6±0.5 4.1±0.3 2.8±0.3 3.1±0.3
range 1.3–8.4 1.3–7.3 1.5–8.9 0.9–8.9 1.6–10.9 1.2–11.6 0.8–5.0 0.8–7.6
GSIb 13.8±2.1 12.7±0.9 7.7±1.0 5.6±0.6 2.0±0.1 1.8±0.4 1.8±0.1 1.1±0.2
range 1.8–24.6 7.9–18.7 1.9–18.2 0.9–13.9 1.4–2.7 0.5–11.1 0.5–2.8 0.2–5.8
(Mean±SEofmean).
aHSI(Hepatosomaticindex)=(liverweight/bodyweight)×100.
b GSI(Gonadosomaticindex)=(gonadweight/bodyweight)×100.
2. Materialsandmethods
2.1. Captureandhandlingprocedures
TheworkwascarriedoutincompliancewithNorwegianlaws andregulationsrelatingtoanimalwelfare,andwasapprovedby veterinaryauthorities(Codenumber:7327).
Atlanticcodwerecaughton18March2015ontheRørafishing ground(69.3◦N,15.6◦W)offthecoastofAndenes,Norway,using Danishseine.Thecapturedfish(ca10t)werehauledfromadepth of100–130mataninitialspeedof1.6ms−1followedby0.7ms−1. Theyweretransferredtoaseacage(70mdiameterPolarcirclepen) atBjarkøy(Troms)withinadayofcapture.Followingsevendays ofrecovery,thefishweretransportedbywell-boattotheAqua- cultureResearchstation(Skulgambukt,Tromsø).On26March400 codweretransferredtotheonshorefacilityatKraknes,Tromsø.
ThenextdaythefishweretaggedwithexternalT-BarAnchorTags (FD-68B,FloyTag&ManufacturingInc.,Seattle,WA,USA)under anaesthesia(MS222,0.1mgL−1),weighedandlengthmeasured.
Then,thefishweredistributedequallybetweentwoindoortanks (4mdiameter,totalvolume20000L)withflow-throughseawater at4.0–5.6◦Cand81–100%oxygensaturation.Thefishwerethen heldwithoutfeedingfortheremaining73daysofthetrial.Anatural photoperiodregimewasusedthroughoutthetrial.
2.2. Samplingprocedures
TwentyfivefishweresampledfromtheseacageatBjarkøy 2daysaftercapture.Thefishwerekilled,weighed,measuredand dissected.Then,thesexandweightsofguttedfish(head-on)liver andgonadswererecorded,andthegastro-intestinaltractofeach fishwasexaminedforthepresenceoffoodremains.Aftertrans- fertotheonshoresiteatKraknes,60fishweresampledondays 26,54and82aftercapture(Table1).Atslaughter,30fishwere takenatrandomfromeach tankandstunnedbya blowtothe head.Next,totalweightandlengthweremeasuredandindividu- alswereidentifiedbyreadingtheirtagnumber.Thefishwerethen exsanguinatedbycuttingtheventralanddorsalaortafollowedby bleedingfor30mininacontainer(600L)withrunningseawater (∼5◦C).Followinggutting,thesex,weightofliver,gonadsandgut- tedfish(head-on)wererecorded,andthegastro-intestinaltract wascheckedforthepresenceofremnantsofprey.Theweightsof gonadsandliverwereusedtocalculatethegonadosomaticindex (GSI)andhepatosomaticindex(HSI)asapercentageoftotalbody weight(Table1).
The fish were then packed in plastic boxes containing ice (8–10kgice per 16–18kg fish), transported toNofima, Tromsø (approx.35minbyroad),filletedandskinned.Theloinfromeach
fillet(∼500g)wasputinazipperbag(300×400mm)andfrozen at−30◦Cuntilanalysedforproteinconcentration.
2.3. Proteincontentinfillet
Filletsampleswereanalysedforfemalesandmalessubjected to food deprivation for 2 (♀=5; ♂=5), 56 (♀=10; ♂=10) and 82days(♀=10;♂=10).Proteinconcentrationwasdeterminedfrom nitrogen(N×6.25)usingtheAOACOfficialMethod981.10(AOAC, 1983)withminormodifications.Priortoanalysis,approximately 200gfromeachfrozenloinwasthawed(1◦C,18h)andminced (3×1min)usingahandheldmixerBRAUNMultimix(Type4642, Spain).Thenthreetechnicalreplicatesofeachminceweremixed with15mL95–97%sulphuricacidandcoppercatalystadded.The sampleswerethenanalysedusingaTecatorDigestormodel2020 anddistillingunit2300(FossAnalytical,Hillerød,Denmark).
2.4. Calculationsandstatisticalanalysis
Relativeweight(RW)andrelativelength(RL)weredetermined to explore the changes in fish length and weight during feed deprivation(Table2).Thevalueswerecalculatedbydividingan individual’slengthandweightatthetimeofsamplingbyvalues obtainedforthesameindividualatthetimeitwastagged.Atwo- samplet-testwasusedtoexaminefordifferencesinRWandRL betweenfemalesandmalesateachtimeofsamplingandone-way ANOVAwasusedtoinvestigatewhetherthereweredifferences within a sex over time (AppendixA, Table A.1 in Supplemen- tarymaterial).RLdidnotchangewithtimesocalculationrelating tochangesinfishandorganweightwerebasedona standard- izedbodylength90cm;thisrepresentstheaveragebodylength offemalesandmalesusedintheexperiment(Table1).Calcula- tionswerecarriedoutusingregressionanalysiswithdatabeing log-transformedpriortoanalysis.
Instudieswithanallometric scalingcomponent,as wasthe casehere,analysesare oftencarried outusinglinearregression following logarithmic transformation of thedata (Peters, 1983;
Table2
Relativeweight(RW)andrelativelength(RL)offishusedinthetrial,fromthe taggingdaytothetimeofsampling.
Number Dayssincetagging RW RL
Males 38 17 0.896±0.008 1.001±0.005
40 45 0.787±0.013 0.992±0.004
40 73 0.753±0.006 1.001±0.004
Females 21 17 0.812±0.002 0.997±0.002
20 45 0.728±0.006 1.001±0.006
20 73 0.702±0.003 0.993±0.003
Fig.1.Therelationshipsbetweenlog-transformedtotal(lnTotalweight)andgutted(lnGuttedweight)weightsandbodylength(lnLength)forfemales(䊉)andmales ()ondays2and82aftercapture.ThelnLengthof4.5isequivalenttofishwithbodylength90cm.Informationaboutregressionandstatisticalcomparisonsisgivenin Supplementarydata(AppendixA,TablesA.2andA.3).
Schmidt-Nielsen,1984;Reiss,1989).OrdinaryLeastSquare(OLS) regressionwasusedtoanalyzedatacollectedforfemalesandmales atdifferenttimesaftertheonsetoffeeddeprivation(AppendixA, TablesA.2–A.5inSupplementarymaterial).Theregressionlineisln Weightmetric=lna+b*lnLength,wheretheweightmetricrefers tototalbodyweight,guttedweight,liverweightorgonadweight.
TheOLSestimatesoflna(intercept)andb(slope)minimizethesum ofsquareddeviations(SS)betweenobservedand predictedval- ues(QuinnandKeough,2002),andoncetheestimatesareknown, predictionscanbemadeforafishofastandardizedlength(90cm).
Analysisofcovariance(ANCOVA)wasusedtocompareregres- sionsforweightmetricsforthesexesateachsamplingtime;sex wasusedasthecategoricalpredictorvariable(factor)andlength asthecovariate.ANCOVAwasalsousedtoexaminechangesinthe metricsforeachsexovertime;intheseanalysesthecategorical predictorvariablewasdayssincecapture.TheTukeypost-hoctest wasusedtoidentifywherethereweresignificantchangesinthe responsevariables.
Atwo-samplet-testwasusedtoexaminefordifferencesinpro- teinconcentrationbetweenfemalesandmaleswithinthesampling timesand one-wayANOVAwasusedtoexplore fordifferences withinasexovertime(AppendixA,TableA.7inSupplementary material).
3. Results
Therewasawiderangeoffishsizesineachsample(Table1) sincethefishwerenotsize-sortedpriortothetrial.Onthetag- gingday,thebodyweightsofsampledfishvariedfrom2818gto 11378g,andlengthvariedfrom70to104cm.Thenumbersofsam- pledmalesexceededthatoffemales,butitisnotknownwhether thisisrepresentativeforthepopulationasawhole.Noneofthefish thatwereexaminedduringthecourseofthetrialhadfoodremains inthegastro-intestinaltract.
Atthefirstsampling,2daysaftercapture,therewerenosignif- icantdifferencesinthetotalweight-lengthrelationshipsbetween the sexes (F (1, 22)=0.4; p=0.510) (Fig. 1A), but relationships forguttedweightsweresignificantlydifferent(F(1,22)=15.81;
p=0.001)(Fig.1B).Foranygivenbodylengththeguttedweightof amalewasgreaterthanthatofafemale.Whenfishweresampled
attheendofthetrial,82daysaftercapture,maleshadhighertotal weights(F(1,57)=5.7;p=0.02)andguttedweights(F(1,57)=6.92;
p=0.016)thanfemalesofthesamelength(Fig.1C,D).
Relativeweight(RW)decreasedovertimeandthedecreasewas significantlygreaterforfemalesthanmales(Table2,AppendixA, TableA.1inSupplementarymaterial).Ontheotherhand,therewas noevidencethatrelativelength(RL)changedovertime.Theresults indicatethat,duringtheexperiment,eachindividualdecreasedin body masswhilethebody lengthwasstable.Thisconfirms the validityofreferencetoafishofstandardized length(90cm)for presentationandcomparisonofweightmetricsofmaturemaleand femalecod.
Thechangesintheweights ofliver,gonads,totalandgutted weights overtimeare presentedforfishofstandardized length (90cm)(Fig.2).Intheinitialsample(March20),theestimatedtotal weightof90cmfemales(6397g)appearedtobeslightlylowerthan thatofmales(6551g),andtheweightsofgonadsandliversseemed tobehigherinfemales(950gand358g)thaninmales(812gand 281g).Therewere,however,nosignificantdifferencesbetweenthe sexesforanyoftheseweightmetricsatthestartofthetrial,butthe guttedweightoffemales(4568g)wassignificantlylowerthanthat ofmales(4981g)(AppendixA,TablesA.2–A.6inSupplementary material;Figs.1and2).
Duringfeeddeprivation,bothfemalesandmalesdecreasedin totalweightandonthelastdayofsamplingthebodyweightof 90cmfemales(4776g)wassignificantlylowerthanthatofmales (5159g)ofthesamelength(Figs.1Cand2).Bodyweightlossduring thefirst54dayswaslinkedtoasubstantialreductioninthesizeof thegonadsofbothsexes(Fig.2)withgonaddepletionbeingsignifi- cantlyhigherinmalesthaninfemales(F(1,53)=63.904;p=0.000).
Significantdifferencesbetweenthesexesforgonadweightwere alsodetectedinfishthathadbeendeprivedoffoodfor82days(F (1,55)=11.397;p=0.001).
A slightdecline in liverweight wasevident duringthefirst 54daysoffeeddeprivationbutwasmorepronouncedduringthe last28daysofthetrial(Fig.2).Weightofguttedfish(head-on) decreasedwithprolongedfeeddeprivation(Fig.2)withthegutted weightoffemalesbeingsignificantlylowerthanthatofmalesat theendofthetrial(F(1,57)=6.917;p=0.016).
Fig.2.Changesinpredictedtotalandguttedweights,theweightsofgonadsandliversinmaturefemale(䊉)andmale()Atlanticcodofstandardisedlength90cmduring 82daysoffeeddeprivation.Lowercaselettersindicatesignificantdifferences(p<0.05)betweensampledayswithinsexes,andasterisks(*=p<0.05)showthesignificant differencesbetweensexesonagivensamplingdate.
Muscleproteinconcentrationsweresimilaratthestartofthe trial(females: 17.4%±0.2;males:17.4%±0.5)(Fig.3).Inmales, proteinconcentrationwasstablefor54daysoffooddeprivation, butproteinconcentrationinfemalesdecreased,leadingtosignif- icantlylowerproteinconcentrationsinfemales(16.5%±0.3)than inmales(17.7%±0.4)(F(1,18)=6.306;p=0.022).Thedifferences betweenthesexesincreasedthereafter and onthefinal dayof samplingtheproteinconcentrationinfemaleswas14.9%±0.4and 16.3%±0.4inmales.
4. Discussion
Thefishusedinthetrialweresexuallymatureandingoodcon- dition,basedonassessmentofGSIandHSI(Table1).HSIcanbeused toassessthenutritionalstatusoffishspeciesthatstoreenergyin theliver(Jobling,1988;Hemreetal.,1993).RWdecreasedinthe absenceofthefoodbutRLwasstable(Table2),andthisformedthe basisforcomparisonsbasedonfishofstandardizedlength(90cm)
Fig.3. Changesinmuscleproteinconcentrationofmaturefemale(䊉)andmale ()Atlanticcodduringlive-storagefor82dayswithoutfeeding.Lowercaselet- tersindicatedifferences(p<0.05)betweensampledayswithinsexes,andasterisks (*=p<0.05)showthesignificantdifferencesbetweensexesonagivendayofsam- pling.
(Fig.2).Alackofchangeinbodylengthinspawningcodwasalso registeredbyRakitinetal.(2001)andFordhamandTrippel(1999).
Therewerenosignificantdifferencesbetweenmaleandfemale cod regardingsize of gonadsand liversat thestart ofthe trial eventhoughtheliversandgonadsoffemalestendedtobelarger (Fig.2).Giventheknowledgeaboutthedifferencesbetweenthe sexesingrowthandmaturation(Love,1988;Karlsenetal.,1995), thematurefemalecodwouldhavebeenexpectedtohavelarger liversandgonadsthanthemales.
Although individual organ sizes did not differ significantly betweenthemalesandthefemales,thetendencyfortheliverand gonadsofthefemalestobelargerhadanoveralleffectongutted weights.Atthestartofthetrial,theguttedweightsofthemales werelargerthanthoseoffemalesofthesamebodylength(Figs.1B and2).
Femalesrespondeddifferentlytofeeddeprivationthanmales.
Females lost more body weight and much of the weight loss occurredduringthefirst54daysofthetrial(Fig.2).Duringthis period,theweightlosswaslinkedmainlytoareductioninthesize ofthegonadsinbothsexes(Fig.2).Matingbehaviorwasobserved duringthesamplingcarriedoutafter26daysoffeeddeprivation, withsome malesand females swimming withtheirurogenital openingscloselyaligned(Brawn,1961;Hutchingsetal.,1999).The fishusedinthetrialwerecaughtinMarch,partwaythroughthe spawningseason(NordeideandBåmstedt,1998;Brander,2005), sothefishwereprobablyspawningactivelyduringthefirstfew weeksofthetrial.
Gonadsize variedconsiderableboth overtime and withina givensample(Table1).Apossibleexplanationforthiscouldbe relatedtoacombinationoftheAtlanticcodbeingamultiplebatch spawner(Kjesbu,1989;JoblingandPedersen,1995;Rakitinetal., 2001)andthatindividualfishwereindifferentphasesofspawn- ingatthetimeofcaptureandsampling.Asaresultofbeingbatch spawnersfemalescanexhibitdifferentstagesofeggripeningdur- ingthespawningseason.Malestendtobeinspawningcondition foralongerperiodthanfemales(HutchingsandMyers,1993).
During extended periodsof feeddeprivation,the nutritional reservesof fishbecomedepleted.Theliverisamajororganfor energystorageincodandliversizeisrelatedtofeedintakeand
HSIcan,therefore, provide anindicationof thenutritionalsta- tusofthefish(BlackandLove,1986;Joblingetal.,1991).During feeddeprivationthereismobilizationofliverreserves(Table1;
Fig. 2)along withwhite muscle glycogen, and thesegradually becomedepleted(BlackandLove,1986).Thereafter,musclepro- teins become increasing utilized to supply energy needs. Our findingsindicatethatenergywastakenfromboththeliverand muscleinbothsexes.Thelatterisdemonstratedin theformof botha reductionin guttedbody weight(Figs.1B,Dand 2)and muscleproteinconcentration(Fig.3).Reliance onproteinasan energysourceincreasedas time progressed.Inaddition, sexual dimorphism became obvious after 54days of feed deprivation whenfemaleshadlowermuscleproteinconcentrationsthanmales, and differences increased towardsthe end of the trial(Fig.3).
TheseresultsconcurwiththoseofHagenandSolberg(2010)who reporteddecreasedproteinconcentrationinthemuscleoffarmed codthathadbeendeprivedoffoodfor11weeks.
Patternsoffeeding,growth,metabolismandenergystoragein codvaryduringthecourseof ayear(Eliassenand Vahl,1982a;
EliassenandVahl,1982b;Love,1988;FordhamandTrippel,1999;
SchwalmeandChouinard,1999;SolbergandWillumsen,2008).
Forexample,SolbergandWillumsen(2008)reportedthatfarmed cod of both sexesdecreased in body weight betweenFebruary andAprildespitebeingfedtosatiation.Femalecod exhibiteda reductioninguttedweight,andfemaleslostmoremuscleprotein thanmales.AccordingtoFordhamandTrippel(1999)bothsexes showlittleinterestinfoodatthestartofthespawningseason,but towardstheendofspawning,thefishbegintofeed,withmales consuminglessthanfemales.Ontheotherhand,thereisevidence thatwildcoddofeedwhilstonthespawninggrounds(Michalsen etal.,2008;Krumsickand Rose,2012)althoughthereisuncer- taintyaboutwhetheritismalesorfemalesthataremostproneto feed.Michalsenetal.(2008)reportedfeweremptystomachs,and greaterlevelsofstomachfullness,infemalesthanmales,whereas Krumsickand Rose(2012)concludedthat femalesatelessthan males.Inourstudy,noneofthefishexamined2daysaftercapture hadfoodremainsintheirgastro-intestinaltract,andthefishwere deprivedoffoodthereafter.Thismayprovideanexplanationfor thereductioninguttedweightseenduringspawninginbothsexes andthegreaterreductioninmuscleproteinconcentrationseenin thefeed-deprivedfemalestowardstheendofourstudy.
Whensummarizingourresults,itappearsthatfeeddepriva- tionaffects maturefemale cod toa greaterdegree thanmales.
Whenviewedfromtheperspectiveofreductionsinguttedweight andmuscleproteinconcentration,thetolerablefastingperiodfor Atlanticcodduringspawningandpost-spawningisapproximately 54days.However,thelengthoftimeoverwhichfeeddeprivation canbetoleratedis likelytovarydependingonupon theinitial nutritionalconditionandsizeoftheenergyreservesofindividual fish.
Acknowledgements
The work is part of a project CATCH: Market-oriented and sustainablevaluechainsforcodproductsbasedonlive-storage, and was supported by the Research Council of Norway (No.
233751/E50).WewouldliketothankthestaffatNofimaASfor theircontributiontothestudy.
AppendixA. Supplementarydata
Supplementarydataassociatedwiththisarticlecanbefound, intheonlineversion,athttp://dx.doi.org/10.1016/j.fishres.2016.12.
010.
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