Effect of dietary inclusion of Atlantic snow crab, Chionoecetes opilio and Northern pink shrimp, Pandalis borealis processing by-products on nutrient digestibility by juvenile haddock, Melanogrammus aeglefinus L.

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Effect of dietary inclusion of Atlantic snow crab, Chionoecetes opilio

and Northern pink shrimp, Pandalis borealis processing by-products

on nutrient digestibility by juvenile haddock, Melanogrammus

aeglefinus L.

Tibbetts, Sean M.; Lall, Santosh P.

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Pleasecitethisarticleinpressas:Tibbetts,S.M.,Lall,S.P.,EffectofdietaryinclusionofAtlanticsnowcrab,Chionoecetes

xxx (2013) xxx–xxx

ContentslistsavailableatSciVerseScienceDirect

Animal

Feed

Science

and

Technology

journalhomepage:www.elsevier.com/locate/anifeedsci

Short

communication

Effect

of

dietary

inclusion

of

Atlantic

snow

crab,

Chionoecetes

opilio

and

Northern

pink

shrimp,

Pandalis

borealis

processing

by-products

on

nutrient

digestibility

by

juvenile

haddock,

Melanogrammus

aeglefinus

L. Sean

M. Tibbetts

∗

_,

_Santosh

_P.

_Lall

NationalResearchCouncilofCanada,AquaticandCropResourceDevelopment,1411OxfordStreet,Halifax,NovaScotia,CanadaB3H3Z1

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received3May2012

Receivedinrevisedform16April2013

Accepted17April2013 Available online xxx Keywords: Haddock Gadoid Crab Shrimp Nutrientdigestibility

a

b

s

t

r

a

c

t

AstudywasconductedtoevaluatetheeffectofdietaryinclusionofAtlanticsnowcrab, Chionoecetesopilio(Crab)andNorthernpinkshrimp,Pandalisborealis(Shrimp)by-product mealsonnutrientdigestibilityinhaddock,Melanogrammusaeglefinus.Thestudyprovides coefficientsoftotaltractapparentdigestibility(CTTADs)essentialfordietformulations aimedatfurthergrowthperformanceandnutrientutilizationstudieswithgadoidsusing thesewastestreamsaspotentialreplacementsforhigh-costfishmealsandpoorlydigestible wheatby-products. Organicmatter(OM)CTTADwassignificantlyimproved(P=0.005) withShrimp150(0.82)relativetotheControl(0.79),whileShrimp300wassimilar(0.79) (P=1.000).NosignificantdifferenceinOMCTTADwasfoundbetweentheControland Crab150(P=0.110),Shrimp150(P=0.473)orShrimp300(P=0.144)atanaverageof0.80. However,OMCTTADwassignificantlyreduced(P<0.001)forCrab300(0.76).Inclusionof Shrimpat150g/kgsignificantlyimproved(P=0.003)grossenergy(GE)CTTAD(0.85on average)relativetotheControl(0.83),whileCrab150(P=0.081),Crab300(P=0.134)and Shrimp300(P=0.986)werestatisticallyequaltotheControl(average,0.82).Crudeprotein (CP)CTTADofCrab150(P=0.803)andShrimp150(P=0.980)weresimilartotheControlat anaverageof0.90whileCrab300(P<0.001)andShrimp300(P=0.005)weresignificantly reduced(average0.86).DietaryinclusionofeitherAtlanticsnowcraborNorthernpink shrimpprocessingby-productmealat150g/kg,concomitantwitha50%reductioninwheat middlingsand10%reductioninfishmeal,resultedinOM,GEandCPCTTADsequaltoor exceedingthatofthefishmeal-basedControldiet.

1. Introduction

To meet nutritional requirements, gadoid feeds contain 650–700g/kg fish meal, 80–100g/kg marine fish oil and 20–30g/kgvitaminsand traceelements(LallandNanton,2002;Lalletal.,2003).Theremaining150–250g/kgis typi-callycarbohydrate-richwheatby-productsthatarepoorlydigestedbycold-watergadoids(Tibbettsetal.,2005;NRC,2011). Therefore,inadditiontoloweringtherelianceoncostlyfishmeal,itisalsoimportanttoidentifylocalalternativeingredients withhigherdigestibilitythanwheatby-products.Traditionally,crustaceanby-productmealshavenotbeenusedindietsfor

Abbreviations: OM,organicmatter;GE,grossenergy;CP,crudeprotein;FCR,feedconversionratio;DP,digestibleprotein;DE,digestibleenergy;IFN,

internationalfeednumber;CTTAD,coefficientoftotaltractapparentdigestibility.

∗ Correspondingauthor.Tel.:+19028683005;fax:+19028682015.

E-mailaddresses:Sean.Tibbetts@nrc-cnrc.gc.ca(S.M.Tibbetts),Santosh.Lall@nrc-cnrc.gc.ca(S.P.Lall).

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farmedsalmonidslikeAtlanticsalmon,Salmosalarandrainbowtrout,Oncorhynchusmykiss.Unlikeotheranimalandplant proteinsources,themajorby-productofcrustaceanprocessingistheshellwhichcontainhighash(>25%)andchitin(>15%), bothofwhichcannegativelyaffectdigestibility,growthandskeletaldevelopmentinfarmedfish(Foxetal.,1994;NRC, 2011).Unlikesalmonids,gadoidshaveshownbetterutilizationofash-andchitin-richingredients(Danulat,1987;Danulat andKausch,1984;Toppeetal.,2006).Itisalsowellknownthatcrustaceanby-productmealsenhancedietpalatabilityfor fishduetotheirexcellentchemo-attractantproperties(HertrampfandPiedad-Pascual,2000).Crustaceanby-productsare abundantlyavailableandunder-utilizedinAtlanticCanada.CommerciallandingsofAtlanticsnowcrabandNorthernpink shrimpinAtlanticCanadawere76,726and121,600t,respectively,in2010.Sinceonly∼30%ofthecrabbodyand∼60%of theshrimpbodyissuitableforhumanconsumption(DeGroot,1995)withtheremaindercomposedofhead,shell,viscera andunextractablemeats,annualquantitiesoftheseprocessingby-productscouldexceed53,000and48,000t,respectively. TheprimaryobjectiveofthisstudyistodeterminetheCTTADsessentialfordietformulationsaimedatfurthergrowth performanceandnutrientutilizationstudieswithgadoidsusingthesevaluablewastestreamsaspotentialreplacementsfor high-costfishmealsandpoorlydigestiblewheatby-products.

2. Materialsandmethods

2.1. Crustaceanby-productmealsandexperimentaldiets

LiveAtlanticsnowcrabandNorthernpinkshrimpcaughtoffthecoastofNewfoundlandandLabrador(NL)inJanuarywas icedonboard,sizegradedonthewharfanddeliveredtotheprocessingplant(Quin-SeaFisheries,OldPerlican,NL).Crabwas immediatelycookedinfreshwater(100◦_C_for₁₁_min)_and_edible_meats_extracted_by_hand_while_shrimp_pre-soaked_in_sodium

metaphosphate-basedmaturingagentandthenmechanicallypeeledtoobtainediblemeats.Shellsandotherby-products weredriedinanindustrialdryer(140◦_C_for₂₀_min)_and_delivered_to_us_by_overnight_courier._Initial_moisture_content_was

higherthandesired(110–130g/kg)sowasfurtherdried(80◦_C_for₉₀_min)_to_reduce_moisture_content_to_<100_g/kg._Products

werefinelyground(500␮mscreen)usingalaboratoryhammermill(Model3100,PertenInstruments,Huddinge,Sweden). Analyzedproximatecomposition,grossenergyconcentrationandchitincontentareshowninTable1.Fiveisonitrogenous (530g/kgCP)experimentaldiets(Table2)wereformulatedaccordingtoDPandDEvaluesofpracticalfeedingredientsfor juvenilehaddock(Tibbettsetal.,2004).Dietsconsistedoffourtestdietscontainingeithercrabby-product(Crab)orshrimp by-product(Shrimp)ateither150or300g/kg(w/wbasis)andafishmeal-basedcontroldiet(Control).Alldiets(4.0mm pellets)werepreparedasdescribedinTibbettsetal.(2006).

2.2. Experimentalprocedures

FishwerecaredforinaccordancewiththeCanadianCouncilonAnimalCare’sGuidelinesontheCareandUseofFish inResearch,TeachingandTesting(CCAC,2005).Onehundredandninetyjuvenilehaddockwererandomlyallottedtoten 120Lcylindro-conicalfiberglasstanksequippedwithfecalcollectioncolumns(Tibbettsetal.,2006).Toensurepositive growth,fishwerebulk-weighedandcountedatthebeginningandendoftheexperimentandtheyhadaninitialmean weightof123.1±0.4g(range,122.5–123.6g)andafinalmeanweightof144.0±7.2g(range,130.3–153.6g).Fishwere acclimatedfor8dayspriortothedigestibilitytrialandeachof5dietswasfedtotankscontaining19fishfor25days.Filtered (30␮m)UV-treatedseawater(salinity,28–30ppt)wassuppliedat2L/minina flow-throughsystemandcontinuously aerated(11.0±0.3mg/Ldissolvedoxygen;99.2±2.3%saturation).Watertemperaturewasmaintainedthermostatically (11.6±0.1◦_C)_and_recorded_daily._Fish_were_hand-fed_to_apparent_satiety₃_times_daily_Monday_to_Friday_(09:00,_13:00,

16:00h)andtwicedailySaturdayandSunday(09:00,13:00h).Eachweek-day,afterthefinalfeedingoftheday(16:00h), thetanksandfecalcollectioncolumnswerethoroughlycleanedwithabrushtoremoveanyresidualparticulatematter(feces anduneatenfeed).Fecalsampleswerecollectedeachmorning(08:30h)into250mLplasticbottles,centrifuged(2750×g for35minat5◦_C)_and_the_supernatant_gently_decanted_and_discarded._A_minimum_of₆₀_g_of_wet_fecal_material_was_collected

from2replicatetanks,comprisedof30gateachof2sub-samplingperiodspertank,andeachsamplewasstoredinasealed

Table1

Proximatecomposition(g/kg),grossenergyconcentration(MJ/kg)andchitincontent(g/kg)ofAtlanticsnowcrab(Crab)andNorthernpinkshrimp(Shrimp)

by-productmeals(drymatterbasis).

Crab Shrimp Analysis CP 323 378 Lipid 7 28 Ash 463 431 GE 9.3 11.2 Carbohydratea ₁₂₃ ₁₀₁ Chitin 247 214

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Pleasecitethisarticleinpressas:Tibbetts,S.M.,Lall,S.P.,EffectofdietaryinclusionofAtlanticsnowcrab,Chionoecetes containerat−20◦_C._Fecal_samples_were_lyophilized_at_a_low_(<5◦_C)_shelf_temperature_(model_50-SRC-6,_The_Virtis_Company,

Gardiner,NY,USA),finelygroundandstoredat−20◦_C.

2.3. Analyticaltechniques

Crustaceanby-productmeals,experimentaldietsandlyophilizedfecalsampleswereanalyzedintriplicateforproximate composition,grossenergyconcentrationandchromicoxidecontentaccordingtoTibbettsetal.(2006).Chitincontentof CrabandShrimpwasdeterminedaccordingtoBlackandSchwartz(1950).Briefly,∼0.5gofsampleishydrolyzedfor1h inboilingHCl(1M)andtheresiduesretained(40–60␮m).Residuesarethendigestedfor2hinboilingNaOH(5%,w/v) andthenwashedwithboilingdH2Oandacetone.Residuesarethendried(110◦C)andincinerated(600◦C)andthenchitin

contentestimatedas:([dryresidueweight−incineratedresidueweight]/[sampleweight])×100%.

2.4. Statisticalprocedures

TheexperimentaldesignwasarandomizedblockandCTTADswerecalculatedfromtheaverageof2replicatetanks receivingeachexperimentaldietand2consecutivesub-samplingperiodsfromeachtank.Statisticalanalyseswereperformed usingANOVAandinthecaseofasignificantdifference,treatmentmeansweredifferentiatedusingtheTukey’smultiple rangetest (SigmaStat® _v._3.5)._Raw_data_was_confirmed_to_have_a _normal_distribution_and _constant_variance_using_the

Kolmogorov–Smirnovtest(SigmaStat®_v._3.5)._A_5%_level_of_probability_(P<0.05)_was_chosen_to_sufficiently_demonstrate_a

statisticallysignificantdifference.

3. Results

Proximatecomposition,GEconcentrationandchitincontentofCrabandShrimparepresentedinTable1.Lipidcontents were7and28g/kg,respectively.ChitincontentofCrab(247g/kg)washigherthanShrimp(214g/kg).AshcontentofCrab andShrimpwashigh(>400g/kg)withCrabhigher(463g/kg)thanShrimp(431g/kg).ThelargestdifferencebetweenCrab andShrimpwasCPcontent,whichwashigherforShrimp(378g/kg)thanforCrab(323g/kg).SincelipidcontentofCraband Shrimpwereverylow(<30g/kg)andCPcontentofShrimpwasmorethan50g/kghigherthanCrab,GEcontentinShrimp (11MJ/kg)washigherthanCrab(9MJ/kg).FormulationandcompositionofexperimentaldietsispresentedinTable2. Dietswereisonitrogenous(average,532g/kgCP)andrangedinash(114–221g/kg)andchitincontent(0–74g/kg).Lipid,

Table2

Formulationandcompositionoftheexperimentaldietsincludingcrustaceanby-productmeals.

Control Crab Crab Shrimp Shrimp

150 300 150 300 Ingredients(g/kgofdiet) Fishmeala ₅₁₅ ₄₇₀ ₄₅₅ ₄₆₀ ₄₁₄ Soybeanmeala ₈₀ ₈₀ ₄₉ ₈₀ ₈₀ Crabby-productb _- ₁₅₀ ₃₀₀ _– _– Shrimpby-productb _– _– _– ₁₅₀ ₃₀₀

Cornglutenmeala ₁₀₀ ₁₀₀ ₁₀₀ ₁₀₀ ₁₀₀

Wheatmiddlingsc ₂₀₄ ₁₀₄ ₀ ₁₀₄ ₀ Chromicoxided ₅ ₅ ₅ ₅ ₅ Cholinechloridee ₆ ₆ ₆ ₆ ₆ Vitaminmixturef ₁₀ ₁₀ ₁₀ ₁₀ ₁₀ Mineralmixturef ₁₀ ₁₀ ₁₀ ₁₀ ₁₀ Fishoila ₇₀ ₆₅ ₆₅ ₇₅ ₇₅

Analysis(g/kgorMJ/kgdrymatterbasis)

CP 534 526 531 534 533 Lipid 176 120 131 185 161 Ash 114 164 221 162 206 Carbohydrateg ₁₇₆ ₁₉₀ ₁₁₈ ₁₁₈ ₁₀₀ Chitin 0 37 74 32 64 GE 22.0 20.1 18.7 20.7 19.4 DPh ₄₈₅ ₄₇₂ ₄₅₇ ₄₈₃ ₄₆₃ DEi _18.3 _17.0 _15.3 _17.7 _16.1

a_Corey_Feed_Mills_Ltd.,_Fredericton,_NB,_Canada.

b_Quin-Sea_Fisheries_Ltd.,_Old_Perlican,_NL,_Canada.

c_Walker’s_Livestock_Feeds,_Dartmouth,_NS,_Canada.

d_EM_Science,_Gibbstown,_NJ,_USA.

e_United_States_Biochemical,_Cleveland,_OH,_USA.

f_Vitamin_and_mineral_mixtures_according_to_Tibbetts_et_al.₍₂₀₀₄₎_.

g_Carbohydrate_calculated_as₁₀₀₀

−(crudeprotein+lipid+ash).

h_Digestible_protein.

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Table3

Coefficientsoftotaltractapparentdigestibility(CTTADs)a_of_organic_matter_(OM),_gross_energy_(GE)_and_crude_protein_(CP)_of_experimental_diets_including

crustaceanby-productmeals.b

Diet OM GE CP Control 0.789±0.008b _0.831 ±0.002ab _0.909 ±0.004b Crab150 0.811±0.006bc _0.846 ±0.004bc _0.898 ±0.004b Crab300 0.764±0.004a _0.817 ±0.002a _0.861 ±0.010a Shrimp150 0.824±0.003c _0.855_±_0.004c _0.904_±_0.004b Shrimp300 0.790±0.006b _0.828_±_0.005ab _0.869_±_0.008a PooledSEM 0.005 0.004 0.006 Pvalue <0.001 <0.001 <0.001

a_Calculated_according_to_Tibbetts_et_al.₍₂₀₀₆₎_.

b _Mean_±_SEM_(n₌_2);_values_within_the_same_column_with_different_superscripts_are_{significantly}_different_(P<0.05).

carbohydrateandGErangedfrom120–185g/kg,100–190g/kgand19–22MJ/kg,respectively.Fishfedexperimentaldiets showedpositivegrowthwithaveragegrowthrateof3.13±0.03%/day(range,3.07–3.17%/day)andsurvivalwas100%.CTTAD ofOM,GEandCParepresentedinTable3.CTTADsofOMfortheControl,Crab150,Crab300,Shrimp150andShrimp300diets were0.79,0.81,0.76,0.82and0.79,respectively.CTTADsofGEwere0.83,0.85,0.82,0.86and0.83,respectively.CTTADsof CPwere0.91,0.90,0.86,0.90and0.87,respectively.

4. Discussion

Thevariousdietformulationsreducedfishmealuseby45–101g/kgandwheatmiddlingsby100g/kgtototalreplacement (Table2).BasedonCPandGECTTAD,inclusionofCraborShrimpat150g/kgweretheonlyformulationsthatmaintained dietaryDPandDElevelsclosetotheControlat472–485g/kgDPand17–18MJ/kgDE.OMCTTADforCrab300(0.76)was statisticallylowerthanallotherdietswhichranged0.79–0.82(average,0.80)andthisisconsistentwiththisdietcontaining thehighestash(221g/kg)andchitin(74g/kg).ThisOMCTTAD(0.80)agreeswithpreviousworkwithjuvenilehaddockfed similardiets(Tibbettsetal.,2005).OMCTTADofCrab150(P=0.110)andShrimp300(P=1.000)(0.79–0.81)werestatistically notdifferentfromtheControl(0.79),whileShrimp150wassignificantlyhigher(0.82;P=0.005).Thisindicatesthatreplacing fishmealandwheatmiddlingswithCrab(upto150g/kg)andShrimp(upto300g/kg)ispossiblewithoutcompromising OMCTTAD.Shrimpat150g/kgispreferableto300g/kgasOMCTTADwassignificantlyhigher(P=0.006)forShrimp150 (0.82)thanforShrimp300(0.79),whichwasnotdifferentfromtheControl(0.79).InclusionofCrabat150(P=0.081)and 300g/kg(P=0.134)andShrimpat300g/kg(P=0.986)hadnosignificantimpactonGECTTADrelativetotheControl(average, 0.83)whileShrimp150significantlyimproved(P=0.003)GECTTAD(0.86),whichisconsistentwithpreviousfindings(0.86) injuvenilehaddockfedsimilardiets(Tibbettsetal.,2005).Again,inclusionofShrimpat150g/kgispreferableto300g/kg asGECTTADwassignificantlyhigher(P=0.001)forShrimp150(0.86)thanShrimp300(0.83),whichwasnotdifferentfrom theControl(0.83).WithregardstosignificantlylowerOMandGECTTADsofShrimp300relativetoShrimp150,OMandGE portionsoffeedsarederivedfromCP,lipidandcarbohydrate.Sincecarbohydratedigestibilityincold-waterfishislow(NRC, 2011)anddifferencesinlipiddigestibilitybetweendietsisunlikely(havingidenticallevelsoffishoilandlittleoilcontribution fromShrimpitself),reducedOMandGECTTADsislikelyduetolowerCTTADofCPatthehigherShrimpinclusion(300g/kg) asaresultofhigherdietaryashandchitin.Indeed,CPCTTADwassignificantlylower(P=0.014)forShrimp300(0.87)thanfor Shrimp150(0.90).CPCTTADforCrabandShrimpwas,infact,significantlyreduced(P<0.05)at300g/kg(0.86–0.87)relative toCrab150(P=0.007),Shrimp150(P=0.014)andControl(0.90–0.91)whichwerestatisticallynotdifferent(P=0.803and0.980, respectively).CPCTTADrangeissimilarbutslightlylowerthanpreviouslyreportedforjuvenilehaddock(0.93)fedsimilar diets(Tibbettsetal.,2005).Differenceislikelyduetohigherashcontentofdietsusedinthisstudy(114–164g/kg)thanthe previousstudy(92–112g/kg)anddietsusedinthepreviousstudyhadamuchlowerinclusionofcrustaceanmeal(50g/kg). CPCTTADinthisstudyforCrab150,Shrimp150andControl(0.90–091)agreewellwiththoseofAtlanticcod(0.91),arelated gadoidfish(Joblingetal.,1991).SignificantimprovementsinOMandGECTTADofShrimp150(0.82and0.86,respectively) relativetoControl(0.79and0.83, respectively)mayberelatedtoefficientutilizationofchitinprovidedatamoderate level(32g/kg)inShrimp150.ThisissupportedbysimilarfindingswithAtlanticcodshowingefficientchitinutilizationat moderateinclusionlevels(Danulat,1986,1987).Unlikefishby-products,themajorby-productofcrustaceanprocessing istheshell,whichcontains150–300g/kgchitin(poly-␤-(1→4)-N-acetyl-glucosamine),representing500–800g/kgoftotal organiccomponentsoftheshell(Garzónetal.,1998).Althoughchitinaseenzymeactivityhasbeenfoundinthedigestive tracts,invivochitinCTTADinsalmonidsislow(<0.05)forrainbowtrout(Lindsayetal.,1984)andAtlanticsalmon(0.13–0.40) (Olsenetal.,2006).Danulat(1986,1987),whoalsoreportedsignificantchitinaseenzymeactivityinthedigestivetractsof Atlanticcod,foundhighinvivochitindigestibility(>0.90).Thesamemaybetrueofhaddocksincetheyarehighlyrelated, havesimilarfeedinghabitsandthedietofwildhaddockconsistsof48%echinodermsandcrustaceanswhicharehighly chitinous(Lalletal.,2003).

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Pleasecitethisarticleinpressas:Tibbetts,S.M.,Lall,S.P.,EffectofdietaryinclusionofAtlanticsnowcrab,Chionoecetes 5. Conclusion

DietaryinclusionofeitherAtlanticsnowcraborNorthernpinkshrimpprocessingby-productmealat150g/kg, concomi-tantwitha50%reductioninwheatmiddlingsand10%reductioninfishmeal,resultedinOM,GEandCPCTTADsequalto orexceedingthatofthefishmeal-basedControldiet.ThisstudyprovidedCTTADsessentialfordietformulationsaimedat furtherstudiesongrowthperformanceandnutrientutilizationefficiencyofgadoidsfeddietsincludingthesecrustacean by-productmeals.

Acknowledgements

WegratefullyacknowledgeMarcKiellyfromtheCanadianCenterforFisheriesInnovation(CCFI),St.John’s,NLandFred HopkinfromQuin-SeaFisheriesLtd.,OldPerlican,NLfordonatingtheAtlanticsnowcrabandNorthernpinkshrimp by-productsusedinthestudyandforprovidingdetailsontheprocessingprotocolsused.WethankShannonScott-Tibbetts fromtheFishermenandScientistsResearchSociety(FSRS),Dartmouth,NSforhelpingtocompilethecommercialcraband shrimplandingsdatafromFisheriesandOceansCanadareports.ThecriticalreviewandvaluablesuggestionsofDarrinReid duringthepreparationofthismanuscriptisgreatlyappreciated.

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