factor affect gonadal development of fish

Muchlisin, Z.A. - Factors Affect Gonadal Development and Egg Quality ofF emale Broodfish

INTRODUCTION

Aquacultureis fanning of aquaticorganisms not only fishes but alsomollusks,crustaceans,andaquaticplants.It has been practiced in various part oftheworldforas longas 4,000yearsago.De Silvaand~derson (1995)reportedthat aquaculture was first practiced inmainland China since most ofthe firstdocumentationonaquaculturewasfoundin China. In addition, more than 2000years ago the Japanese reared fishes inirrigationditches(Ackeforsetal.,1994).

Recently,fishlandingsfromnaturalresourceshavereduceddramaticallyasdevelopmentinseafishingtechnologies,methods of seafood preservation andtransportationimprovementof. On theother hand, market demands haveincreasedovertheyearsashumanpopu-lationintheworldandawarenesson the

nutritional advantages offish proteinincreased.In 2020 forexample,humanpopulation in the world is expected toreach8.5billioncomparedto 6.0billionat present.Therefore,as countriesseekfor alternatives to meet the marketdemand,aquacultureandmarineculturehave been identified as possible solu-tions to this problem. For example, in1998aquaculture provided about 25%ofthe world's fish supply compared to8% in 1984(Kalyani, 2002).However,oneofthemainproblemin aquacultureishigh mortalityoflarvae thatresulted in

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lowproductionof fishculture.Applica-tion of a good broodstock and larvalmanagementprogramsarewaysthat canbe used to overcome these problemsand increaseproductionoffish. A goodmanagementofbroodstockwill resultedin high qualityof egg, spermandlarvaeaswell.

There are many factorshave beenidentifiedasfactorsinfluencingeggqualityand reproductive performance offishfemale broodstock,such as nutrition interm of proteins, lipids, carbohydrates,vitamins and minerals; broodfish andenvironmentalcondition.Nutritionis a

mainfactorthatinfluenceeggqualityandreproductiveperformanceoffishdirectlyor indirectly.

Like terrestrialanimals,fishneedsprotein,lipid,carbohydrate,mineralsandvitaminforgrowingandmaintainingtheirbody. It has also been well known thatthegrowthrateofbroodfishislowerthanthat oflarvae due to the fact that adult

fish requires more energy for gonadal.development(Steffens,1989).

Since the 1980s,increasing atten-tionhasbeenpaidtotheroleofindividualnutrient components in the diet ofbroodstock. The major group of feedcomponents,includingprotein,fattyacid,andvitaminhavebeenexamined(Furuitaet al., 2001).

Besidesthenutritionalcomponents,ratio sizeofbroodstock can alsoaffect

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egg and fry quality. In rainbow trout(Salmogairdneri)forexample,theeggsandfryproducedbybroodstockgivenahalfdailyration(0.35%bodyweightperday)weresignificantlysrnaller(eggweightof63.7 mg, and fryweight of94.6 mg)thanthoseofthefull-rationof0.7%bodyweightperday(82.9mgeggweightand105.1 mg fry weight) respectively,althoughbroodstockration sizehad noeffectupon theaminoacid compositionof egg produced (Knox et al.,1988).Similarly, Ali and Wootton (1999)reported that female three-spinedsticklebass Gasterosteusaculatus, fedwith high rations(16% ofBW per day)showed an increase inbatch fecundity,and low ration (4% ofBW per day)resulted inan increaseinthe numberofdays until the next spawning. Indeed,daily and seasonal rates of feeding ofbroodstockdietscanaffectto fecundityandeggsizeof fish(Carrilloetal.,2000).

PROTEIN

Proteinisanessentialcomponentofthe cell nucleus, internal organs,brain,nerves andskin.Proteinislargeorganicmoleculethatcontaincarbon,hydrogen,oxygen,nitrogenandoftensulphur.Thebasic compositionof most proteins aresimilar; C = 50-55%, H = 6-8%, 0 =20-23%,N=15-18%,S=0-4%. Thefim-damentalstructural unit of the proteinmoleculeisaminoacid,whichcomprises

Biologi, Vol.4, No.6, Desember 2005

of20 naturallyoccurringtypes (Jobling,1995).Tacon(1987)citedthatenzymeswhichareproteins,playa criticalrole incellularmetabolismsinceallbiochemicalreactiondependsonenzymes.Enzymesare essential for carbohydrateand lipidmetabolism, for synthesis of tissueproteinsandmanyimportantcompounds,and protein can also form a source ofenergyforfish.

Ingeneral,aminoacidcanbeclassi-fiedinto two groups; the indispensableamino acids (arginine, histidine, isoleucine,

leucine, lysine, methionine, phenylalanine,

threonine, tryptophan, valine, and thedispensableaminoacids(glycine,alanine,serine, tyrosine, cysteine, proline,hydroxyproline,asparticacid,glutamicacid,andornithine).

Indispensable amino acids areamino acids that cannotbe synthesizedwithin the animal body or at a rateinsufficient to meet the physiologicalneeds of the growing animal,andmustthereforebe supplied fromthe diet. Onthe otherhand, dispensableaminoacidsare those that can be synthesized in thebody from a suitablecarbonsourceandotheraminoacidsor simplecompoundssuchas diammoniumcitrate,andconse-quently may not be supplied in readymade form in the diet (De Silva andAnderson, 1995).

Proteinis averyexpensivecompo-nentinfishdietsandaccountsforasmuch

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Muchlisin, Z.A. - Factors Affect Gonadal Development and Egg Quality of Female Broodfish

as40-70%oftheaquacultureoperationalcost. Therefore, information of theoptimum dietaIyproteinrequirementforthedifferentfishspeciesatdifferentstagesofgrowthisessential.

In broodstock, Eskalinen (1989)reportedthat the relative fecundity(thenumber of eggs produced per bodyweightoffemaIe)andeggsizeofAtlanticsalmonwas higherwhen they were fed31% dietaryprotein levelof semimoistfeed. Similarly,Alhafedh et al. (1999)reportedthattherelativefecundityofNiletilapia increased with increasing thedietary protein levels, and was signifi-cantlyhigherat 25-35%dietaryproteinthan those fish fed40-45%protein,butdietaIyproteinlevelsbetweenof25% to45%hadnosignificantinfluenceon eggsize and weight. A similar result wasreportedby Cisse(1988),whoreportedthatthehighestspawningfrequencyandegg production were obtained fromfemalesfedwith30%proteincomparedto those of 20%, 25%, 35%, 40% or50%dietaryprotein.Reducedfecundityhavebeenreportedinseveralfishspecies,where the cause could either be theinfluenceof a nutrientimbalanceon the

brain-pituitary-gonadendocrinesystemor by therestrictionin theavailabilityofbiochemicalcomponentforegg forma-tion (Izquierdoet al., 2001).

Dietary protein level influencespuberty,oocytedevelopment,spawningperformance, and egg quality of Nile

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tilapia, Oreachromisni/oticus.Nile tilapiafed a low protein diet «17%) did notshow oocyte maturation,while femalesfed 25% protein showed sloweroocytegrowth, and females fed> 32% proteinlevels had early oocyte growth andmaturation (Gunasekera et al., 1995).Furthermore,Gunasekeraetal. (1996b)laterreportedthatNiletilapiabroodstockfed 20 and 35% protein dietproducedahighernumber of eggsper spawn(totalfecundity) than those fed 10%protein,buteggsizeandrelativefecunditydidnotdiffersignificantlybetweenthetreatments.In sea bass, Dicentrarchus labrax thefecundityandreproductiveperformancewere better at a higher dietary proteinlevel of 51% (Cerda et al.,1994).

Wee and Tuan (1988) reported thatthe optimum dietary protein level forspawning Oreochromis ni/oticus was35%. Broodstock fedwithdietscontaining20% protein were spawned lately, whileother groups fed with higher dietaryprotein level of27.5%, 35%,42.5% and50% spawned earlier. Moreover, theabsolute and relative fecundities were

found to be significantlyhigher in the fishfed with a 27.5% and 35% dietaryprotein than those fed with higher proteinlevels of 42.5 and 50%. However, high

protein diets produced heavier and largereggs at shorter spawning interval.

Proteins areultimately degraded intoamino acids that are utilized either as an

energy source or for somatic protein

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synthesis. However, very little infonnation

is knownaboutthe specificamino acidrequirements of the broodfish (Luquetand Watanabe, 1986). DietaIy tryptophan,a precursor of the neurotransmitter

serotonin, has been reported to positivelyaffectgonad maturation in both males andfemales. Supplementation of 0.1 %

tryptophan in the dietof ayu (Plecoglossuallivelis) resulted in a significant increase

in the serum testosterone level advancingthe time of spermiation in males andinduced maturation offemales (Akiyamaet al., 1996).

LIPID

Lipidisanimportantenergysourceinfishbutwithotherimportantroles,suchas beingthetransportmediumfor lipid-solublecompounds(e.g.somevitaminssuch as A, D, E, and K), as structuralelements in cell membranes, and asprecursors for a number of importantbiologicallyactivecompound(e.g.somehormone,pigmentsandgrowthfactors)(Jobling, 1995).

Phospholipidespeciallydeterminescell membrane structure and fluidity(Zonneveldetal., 1991;Jobling,1995),and dietary phospholipids are alsoreported to improve egg quality(Watanabe et al., 1991). In addition,lipids inparticularfattyacidshavebeenshownto affect teleostspituitarygland,which regulate gonadal hormone, andsteroids sexlevels(Cerdaetal., 1994a;

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1994band Bruce et al., 1999).Indeed,Pustowka et al., (2000) reported that a12%tallow oil (a highly saturatedfattyacid) diet increased cholesterol andmonounsaturatedfattyacidslevelsignifi-cantly in the spermatozoa plasmamembranescomparedtodietscontaining12% herring, 12% menhaden or 12%safflower oils (highn-3, n-6fattyacid),high level of cholesterol and mono-unsaturated fatty acids respectively inspermatozoaplasmamembraneswhichin turn increased resistance to

cryopreservation damage in rainbowtrout.

Several researchers have empha-sizedtheimportanceoflipidinbroodfishnutrition. For example, Duray et al.(1994)reportedthat the elevationof di-etary lipid level from 12% to 18% inbroodstock diet of rabbitfish (Siganusguttatus) resulted in an increase infecundity and hatching rate. Similarly,fecundity ingiltheadseabream(Sparusaurata) was found to increase signifi-cantly with an increase in dietary n-3HUFA level up to 1.6% (Femandez-Palacios et al., 1995).

In addition,polyunsaturated fattyacid can also regulate eicosanoidproduction,particularlyprostaglandins,whichareinvolvedinseveralreproductionprocesses, including the production ofsteroid hormoneand gonadaldevelop-ment such as ovulation (Moore, 1995;

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Muchlisin. Z.A. - Factors Affect Gonadal Development and Egg Quality of Female BroodflSh

Mercure and VanDer Kraak. 1996).SantiagoandRayes(1993)studied

the effectof dietary lipid source on thereproductive performance and tissuelipids ofNile tilapiaby feedingexperi-mental diets containing 5% oil fromdifferent sourcesnamely, cod liver oil,cornoil, soybeanoil, coconutoil-basedcookingoil,andcombinationofcodliveroilandcornoil.Theyfoundthatcodliveroil (a sourcesn-3 fatty acid) resulted inpoor reproductiveperformance,but thehighest weight gain. Overall, seedproductionwas foundto be remarkablyhighforfishfedwithsoybeanoilasourceof 18:2,n-6 fatty acid.

CARBOHYDRATE

Carbohydratesare another impor-tantenergysourcesforterrestrialanimals,but is not a primary energy source foraquaticanimalssincefishcannotdigestiteffectively(Steffens, 1989).However,there are no publications in the role ofcarbohydrateon thereproductiondevel-opmentofthe fish.

VITAMIN AND MINERALVitaminsareessentialforthemain-

tenanceofhealthandgrowthof fish,andact as cofactors or substrate in some

metabolicreaction,andtheyarerequiredin relativesmallanlounts(De SilvaandAnderson,1995).Elevenwater-soluble(ascorbic acid, myo-inositol, choline,thiamin, nooflavin, pyridoxine, pantothenic

416

acid, biotin, niacin, folic acid, and cyano-cobalamin)and four lipid-solublevitamins(A, D, E, and K) are known to berequired by fish (Jobling, 1995).

Vitamins A, C, and E are known to

affect fecundity offish. The quality of thefeed, especially the vitamin content,becomes more important as the femalesget older. For example, a-tocopherol orvitamin E is an essential substance for

growth and reproduction of fish (Tokudaet aI., 2000). A deficiency of tocopherolleads to an inferior state of developmentof carp ovaries, resulting in increasedmoisture content, and reduced fat and

protein content of the ovaries (Steffens,1989),which in turn has a negative effecton the quality of the larvae produced. Inayu (Plecoglossus altevelis) for example,a reduced alpha-tocopherol level in thebroodstock diet caused low survival rates

of egg to eyed stage and hatching(Takeuchi, et al., 1981), and causedreduced sexual coloration and reproduc-tive activity in Nile tilapia (Schimittou,1993).

Vitamin E (a-tocopherol) has beentransported and preserved more positivelyin the gonad during the reproduction pe-riod. During maturity serum a-tocopherolhad partlycombinedwith the vitellogenin-likeparts thatdiminished afterthe spawn-ing period of Japanese flounder (Tokudaet al., 2000). In addition, Izquierdo etal., (200 1)also have reported an increasein dietary a-tocopherol level up to 125

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mglkgresultedinan improvementinfe-cundity of gill-head seabream as ex-pressedby thetotalnumberofeggspro-duced/femaleandeggviability.

A dietary supplement of ascorbicacidor vitaminC haspositiveeffectsonthereproductiveperformanceinvariousfishspecies(Eskalinen,1989).Ithasbeensuggested that supplementation ofascorbicacid(1250mgof ascorbicacidper kg of dry diet) improves the hatch-ability of egg, and the condition andsurvivalrateoffiy (Solimanetat.,1986).AlthoughFuruitaetaI.,(2001)reportedthat feeding broodstock with a higherlevelof vitaminA increasesthevitamin

A contentineggsbutdoesnotaffecteggquality of Japanese flounder,Paralichthysolivaceus,becauseexcessdietaryvitamin A was storedmainly inthe broodstockliver.

Theothercomponentinfishdiet ismineral.Mineralsareneededbyanimalsto maintain many of their metabolicprocesses and provide materials formajor structural elements such as theskeleton. Mineralsrequiredfornormalmetabolism can be divided into twogroups,majorandtraceminerals.Majormineralsarerequiredinlargequantitiesand these includecalcium,phosphorus,magnesium,sodium,potassium,chlorine,and sulphur. Trace minerals are thoserequiredsmallquantitiesandincludeiron,iodine,manganese,copper,cobalt,zinc,selenium, molybdenum, fluorine,


alumanium,nickel,vanadium,silicon,tinand chromium(De SilvaandAnderson,1995).

Calciwnandphosphorusareimportantconstituentsofskeletalmaterial.Copper,manganese, cobalt, zinc, and seleniumhavearoleinmetabolicfunctions,ironisa componentof the respiratorypigmenthaemoglobin,and iodineis requiredforthe production ofthe thyroid hormone(Jobling,1995).

Fishcan absorbpartof therequiredmineralsdirectlyffomthewaterthroughtheirgillsoreventhroughtheirentirebodysurface,andtherateofmineralabsorptionvaries among fish species and withvariationsinenvironmentalfactorssuchasthemineralconcentrationinthewater,water temperature, pH etc. (Hepher,1988).To date, the effects of mineralson the reproductiveperformanceof fishhavenotbeen studied.Howevertherole

of mineralsonreproductionofterrestrialanimal have been evaluatedby Nurhanet ai., (2002) and reported that supplemental

chromiumof400 J.1g1kgofdiet,andzincono mg/kg or combinationsof 400 J.1gofCrplusandCror30mgofZn/kg ofhen diets increased egg productionand eggweightcomparedto control.

BROODFISHThe conditionof femalebroodfish

is another factoraffectingthereproduc-tiveperformance,eggsand larvaequal-ityoffishes.Generally,fishfecundityand

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eggsizeincreaseby increasingbroodfishsize (Buckleyetal., 1991andBromageet al., 1990),but the egg sizemay varyfrom one spawning to another, and thenumber of eggs contained in a specificvolumemayalsobe different(Carrilloetal., 2000; Jonsson and Jonsson, 1999).This result is supported by Kazakov(1981), and Morita and Takashima,(1998) who reported that egg size ofrainbow trout, Atlantic salmon andwhite-spotted charr (Salvelinusleucomaenis)increasedby increasingtheage andsizeof females.A similarresultwas found in the Nile tilapia,Oreochromisniloticus (Gunasekera etal., 1996b),Tilapiazilla, (Coward andBromage, 1999),and in white-spottedcharr (Morita and Takashima,1998).Morita,et al., (1999) also reportedthategg size was strongly associated withbroodfish growth history, however itsassociation with egg number was notestablished. .

In addition,Bromageet al.,(1990)reportedthatfecundity,eggsize,totaleggvolume of rainbow trout increased byincreasing fish size, whereas relativefecunditydecreasedas fishget larger.Apositiverelationshipbetweenbroodfishsize, eggs and larval viability wasalsofound in Australian bass (Harris, 1986) and

Iceland cod (Marteinsdottir andSteinarsson, 1998). However, the re-lationshipbetweenthe sizeof ripe eggs

418

and fishsize remains unknown.In had-

dock, Melanogrammusaeglefinuseforexample, a significant relationship be-tweenthelengthoffemalebroodfishandeggdiameterwasobservedforthesmaller2-3 years old broodfish, but not for thelarger fish (4-8 years old) (Hislop,1988). .

Lastly, it is a fact that femalesproducing large eggs were limited toproducingfewereggs.Bigeggsgenerally,producelargerlarvaeathatching,whichmay have a positive influence on theindividual fish in terms of resistanceto

stnvationorotherenvironmental challenges.

ENVIRONMENTALFACTORSMultipleenvironmentalfactorsare

oftenassociatedwithgonadmaturationand eggqualityof the fish,especiallyinegg sizes (Cnamber, 1997). Environmental

factorsregulatethe hormoneactivityofthe fish, thus affecting egg quality(Asturianoet aI.,2000), indicating thatthe environmentandhormonesactboth

indirectly and directly, respective. Acorrelationbetweenthe annualbreedingand testicular androgens have beenreviewed by Lileyand Stacey(1983)innumerous species of teleost such asstickleback,Atlanticsalmon,gold fish,plaice, brown and rainbow trout, andstriped mullet, and they found at leastthree environmental factors; season,temperatureandsalinitythatinfluenceeggsizeoffish.

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In teleosts,temperatezone,highlypredictablecOlrelationisoftenobservedfor seasonaland reproductivecycle. Intropical zones, seasonal changes ofenvironmentarelessextreme,andmanyfishes exhibit extended or continuous

reproductive pattern (Redding andPatino, 1993). In temperate marinefishes,spawningoccursthroughouttheyears.Ithasbeenfoundthatwaterqualityparameterssuchasdissolvedoxygen,pH,salinity, temperature, nitrite are majorfactors affecting seed production oftilapias (Littleet al., 2000).

Watertemperatureandsalinityvaryseasonally, annually and spatially intemperate marine habitat. Watertemperature and photoperiod are thedominant physical variable definingseasonally in these systems,and watertemperature also varies stronglyalong latitudinal and depth gradients.Seasonalvariationinsalinitycanalsobesubstantial in near shore and estuarine

habitats, reflecting seasonal fluxes infreshwater inflow, but the dominantsalinity gradient is associated.with thetransitionbetween freshwaterand salt-water in estuaries (Chamber, 1997).InAtlantic cod Godus marhua for ex-

ample, reductionin day lengthintermsof photoperiodsis avitalenvironmentalsignal regulating the maturation andspawning,andsexualmaturationdelayed(Hemre et aI.,2002).


Water temperature which variessignificantlythroughouttheyearintluencestherelativefecundityinBalticcod(Kraus,et al., 2000). Temperature has beenknownas a factoraffectingreproductionandmetabolismoffish.Furthermore,tem-peratureandphotoperiod.alsoaffectthedaily cycle ofGtH in female gold fish(Hontela and Peter reviewed by Peter,1983).

Generally,reproductionandmeta-bolic rates of fish are slower at low

temperatures, though it varies fromone species to others.Forexample,Niletilapia reproductionis slowat tempera-tures of 21 to 24°C and increases in

frequency above 25°C up to 30°C(popmaandLovshin,1996),andinfemaleseabass,oocytedevelopmentis abortedanddidnotreachfullmaturationat tem-

peratures below 10°Cduring the mainperiod of gonad development (Pawsonet al., 2000).

However,it isreportedthatsalinityratherthantemperatureplaysa vitalrolein the reproduction performance inmarinefishsuchasAtlanticcod,wherebythe egg quality of captive Atlantic codvaries even at constant temperature(Kjesbu et al., 1992).

Most ofthe studies suggest thatsalinityandtemperatureaffectoneggsizemostduringoogenesis(Chamber,1997).As fortemperature,theoptimumlevelofsalinitydiffersrom onespeciestoanother.

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Forexample, Oreochromiss mossambicus

can reproduce at 35-49 ppt whileOreochromissaureusandTilapiazillidonot reproduce at all in sea water whileOreochromissni/oticusceasereproduc-tionaltogetheratsalinitieshigherthat30ppt (Watanabe, 1985). Studies byYeheskelandAvtalion,(1986) showedthat fertilityof Oreochromissni/oticusdecreased from 94% to 26% by increasing

salinities from 0.00 to 1.00 ppt, butfertility increased from 17% to 91%when pH increased from 4.5 to 9.0,whilethespawningandtotalhatchingrateof grey mullet, Mugi/ cephalus L washighestat30ppt (LeeandMenu, 1981).

EFFECT OF PROTEIN ON EGGSAND BODY COMPOSITIONS OFBROODSTOCK

Research on the dietary proteininfluenceoneggandbodycompositionoffish brood stock is still limited com-

pared to the information available ondietaIyproteinrequirementforlarvaeandgrow-out fish. Alhafedh et al. (1999)reportedthat the protein contentof dietsignificantlyinfluencedtheproteincontentof the fish body, in that high dietaryprotein levels (40 to 45%) resulted inhighermuscleproteincontentthanthefishfed low andmedium (25-35%) proteindiets. They also reported that lipidcontent decreasedby increasingdietaryproteinlevel.InadditiQn,Gunasekeraetal., (1996b)has also foundthat protein

420

content in eggs maintained on a 35%protein dietwassignificantlyhigherthanthose maintained on a 10% and 20%

dietaryproteinlevel.Incontrast,differentdietary protein levels did not appear toinfluenceeggproteincontentinEuropeansea bass (Cerda et al., 1994)and in redsea bream (Watanabeat al., 1985).

Robinson and Li (1999) reportedthat visceral and fillet fat of channel

catfish decreased by increasing thedietary protein level. Fish fed a 24%protein diet had highervisceral fat andfillet fat than those fed the 28% or 32%

proteindiet.Fattinessinchannelcatfishmay be related to a number of factors,including sex, size, strain and age.Generally,there is a direct correlationbetween the DEIPratio and fattiness in

catfish(RobinsonandRobinette,1994).Robinson andJackson (1991) reportedthat an increase in muscle fat wasobserved in channel catfish fed a feed

containing26%protein (11.lkcal DE/gprotein) as compared to fish fed a 32%protein feed but with a lower energycontent (9.0 kcal DE/g protein) or fishfed a 28% protein feed(10.4kcal DE/gprotein).SimilarresultswerefoundbyLiand Lovell (1992) that fish fed a lowprotein feed had a higher percentagemuscle fat. Carcass moisture and total

lipidafterthe feedingtrialdidnotdiffer,andbodyproteinincreasedwithincreasingdietary protein,but body protein ofthecontrol larvae was similar to that of

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larvae given the 600,10protein diet (Eguia,

et al., 2000).

CONCLUSIONS

There are many factorshave beenidentifiedasfactorinfluencingeggqualityand reproductive performance of fishfemalebroodstocksuchas environment,broodfishconditionandnutritionintermof protein, lipid,carbohydrate,vitaminandmineral.Although,nutritionespeciallyprotein, vitamin A, C and E are mainfactorsthat influencingeggqualityandreproductiveperformanceoffishdirectlyand indirectly.In term of environmentfactor,temperatmeandsalinityplayavitalrole in gonadaldevelopmentoffish. Inaddition,bodycompositionoffish andegg composition were influenced bycompositionof thediet.

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