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Influence of energy balance and body condition on estrus and estrous cycles in Holstein heifers

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The objective was to determine effects of energy balance and body condition on estrous behavior and estrous cycles in Holstein heifers. Before the experiment heifers were fed so body condition remained moderate or they became fat. During the 2 x 2
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  Influence of EnergyBalanceandBodyConditiononEstrusandEstrousCyclesinHolsteinHeifers 1 A.VILLA GODOY 2T.L.HUGHES 3  S EMERY 3E.P.STANISIEWSKI 4  n L. FOGWELL3MichiganStateUniversity EastLansing 48824 1225 ABSTRACT The objectivewas to detennineeffects of energybalanceandbodyconditiononestrousbehaviorandestrouscyclesinHolsteinheifers.Beforetheexperimentheiferswerefedsobodyconditionremainedmoderate or theybecamefat.Duringthe2x2factorialexperiment,moderateandfatheiferswereinpositive or negativeenergybalance.Heiferswerefedindividuallytwicedaily,andenergybalancewascalculateddaily.Heiferswereobservedfor30 min every3 b and all standingandmountingeventswererecordedfor three consecutiveestrouscycles.Whenprogesteroneinserumwas <1 ng/ml,standingandmountingactivitywereprofiled.Area,peak,andduration of activityprofileswereexaminedamonggroups of heifers.Negativeenergybalance or fatbodyconditiondidnotreduce peak or duration of estrousbehavior and thusdidnotreducedetectability of estrus.Onset of diestruswasdelayedinheifersthatwerefatandinnegativeenergybalancerelative to otherheifers. We suggestthatfatbodycondition,coincidentwithnegativeenergybalance,mayreduceaccuracy of timingartificialinseminationrelativetoovulationandmayconsequentlyreducefertilityincattle. Key words: energybalance, body condition,estrus) Received February I,1990. Accepted May 22,1990.lMichiganAgriculturalExperimentStationJournal  - dcleNumber12414.2NationalInstitutionforForestry,Crop and LivestocltResearch.Department of Physiology.Apdo.Postal 29-A; Queretaro, Qro 76020 Mexico.30ePartment of Animal Science.ReprintrequeststoR. L. Fogwen.  The UpjobnCompany,Kalamazoo,MI49001. INTRODUCTION Estrusisdetectedwithonly 5 to 60 of ovulationswhen dairy cowsareobservedtwo 13,23) or three timesdaily 21).Whensurveillance of cowsiscontinuous,estrusisdetectedwithatleast95 of secondandthirdpostpartumovulations 12).Rigor of informedobservationsispresumedto be amajorsource of variationindetection of estrus.Duration of estrus in dairycattlerangesfrom1to 21 h 7,12);thus,cowsarealsoanimportantsource of variation in detection of estrus. At least80 of dairycowshavenegativeenergybalance  NEB) duringearlylactation 19,21).   feedpresentedtocowsisadequate,ingestion of calories,notyield of milk,isthemajordeterminant of energybalance EB)inpostpartumcows 21).Thus,factorssuchasexcessbodyfat 9)thatreduceintake of feedmayincreasemagnitude or incidence of NEB.DuringNEB,homeorheticeventssustainmetabolicsupport of lactation 1).DuringNEB,mammaryfunctionapparentlyhasmetabolicpriorityoverovarianfunction.Evidenceshowsthatsecretion of progesteroneduringsecondand third postpartumdiestrusisassociatednegativelywithNEB 21).Alteredovarianfunctiondue to NEBcouldaffectexpression of estrus in cattle.OverallhypothesisisthathomeorheticeventscoincidentwithNEBreduceexpression of estrus.Postpartuminterval,number of postpartumovulations,parityandNEBareconfoundedinpostpartumlactatingcowsbutnotinnulligravidheifers.Asinlactatingcows 21),NEBreducedsecretion of progesterone in nulligravidheifers 22).Thus,heiferswereause ful model to examineeffects of NEBonlutealfunction 22).Theobjective of thisexperimentwas to determineeffects of energybalanceandbodyconditiononbehavioratestrusandduration of estrouscyclesinnulligravidheifers. MATERIALSANDMETHODS TwentynulligravidpostpubertalHolsteinheiferswereblockedby BW andwereassigned 1990JDairySci73:2759-2765 2759  2760 VllLA-GODOYET AL. EstrousBehavior TABLE   Composition of totalmixedrations  TMR . Dietl ergyingested(16).Amounts of CP ingestedsatisfiedrequirementssoallheiferswereinpositivenitrogenbalance.Inalternateweeks, BCof heiferswasscoredasdescribedbyMulvanny(15).Unlessotherwisestated,BCmeasuredatonset of experimentalphasewasusedonlytoclassifyotherdataandwasnotexamined as data or usedasanindependentvariable.Heiferswerehousedintwoadjacentpens,andallheiferscouldbeobservedsimultaneouslyfromonelocation.AllPEBheiferswere in onepen,andallNEBheiferswereintheother pen. Duringthreeconsecutiveperiods of estrus(experimentalphase),heiferswereobserveddailyfor30-minperiodsat3-hintervals.Behavioraleventsrecordedwerestandingtobemounted   s andmounting.Jugularbloodwassampleddailybyvenipuncture. Pro gesteroneinserumwasquantifiedbyradioimmunoassay(21)andwasusedtodefmeestrusanddiestrus.Aheiferwasconsideredinestrus Ctem Phases used Conditioning   Adaptation   Experimental   Ingredients,   Alfalfahaylage24.94.422.4 Com silage53.416.948.9 High moisture ear com 16.273.112.0Proteinsupplement(44 )5.0 5.1 16.2Vitamin premix   ChemicalanaIysis2  3 Dry matter,  40.050.946.4Energy, Mcal/kg4 1.5 1.61.4Crudeprotein, 13.613.317.7Aciddetergentfiber, 21.714.315.5IDry matter basis.2Metbodsforchemicalanalysis in Villa-Godoy et al.(22).3Concentration of minerals in totalmixedrationswere:   (.71 ),P(.39 ),K(1.1 ), Mg (.26 ),S(.21 ), Na (.13 ), Mn (57 ppm), Fe (228ppm),Cu(8ppm),and Zn  48 ppm). ~ energyformaintenance  NEm calculatedfromchemicalanalysis of TMR. BodyWeight,ConditionScore,andEnergyBalance Bodyweight of heiferswasmeasuredat1500hon2consecutivedeachweek.Intakeoffeedwasrecordeddailyandenergybalance(EB)wasestimateddailyforindividualheifers as differencebetweenenergyrequiredanden-withinblock to a2x2factorialexperiment.Maineffectswere: 1 bodycondition(moderateorfat)and2)energybalance(positiveornegative).Heiferswereinafree-stallbarnequippedforindividualfeeding.Heiferswerefedtotalmixedrations (TMR) (Table 1 andhadfreeaccesstowaterandtrace-mineralizedsalt.Thestudyconsisted of threephases:conditioning,adaptation,andexperimental.Conditioningphasewas' 6moandstartedwithtwogroups of heifers of similarage(' 10mo)andbodyweight(277 ± 5kg).DuringconditioningheiferswerefeddietsAorB(Table1)oncedaily,andthisphaseendedwhenrange of bodycondition(BC)formoderate(MBC)andfat(FBC)heifersdidnotoverlap(22).Duringadaptation(20d)heifersweremeal-fedindividuallyduringtwo90-minperiodsdaily.Allheiferswereoffered1.6 kg ofOMof diet Nl00 kgbodyweight(Table1).Ovaries of heiferswereexaminedrectallyatleasttwiceandpresence of acorpusluteumdesignatedaheiferaspostpubertal.Estruswassynchronizedwithtwoinjections of prostaglandinF2atohomogenizestage of estrouscycleamongheifersatonset of experimentalphase.Duringexperimentalphase(3periods of estrusperheifer)heiferswerefedindividuallytwomealsdaily.OietsAandC(Table1)wereoffered(22)butamounts of dietary OM andCPoffered/l00kg BW weresameforpositiveenergybalance(pEB)andNEBheifers.Caloricdensity of dietAwasgreaterthanthat of diet C. DietAsupportedPEBanddailygain of BW ( '.8kg).HeifersfeddietCexperiencedNEBandlost BW andcondition(22).Thus,fourtreatmentcombinations(number of heifers)wereestablishedfortheexperimentalphase:MBC-PEB(5),FBC-PEB(6),MBC-NEB(5),andFBC-NEB(4).Independent of BW change,dietarycaloriesandkgOM/IOOkg BW remainedconstantwithenergystatus.Thus,totalfeedoffereddailytoeachheiferwasadjustedweeklyforchangesin BWof thatindividual. Journal of DairyScienceVol.73,No.10,1990  DmT,BODY CONDmON AND ESlRUS INHEIFERS 2761whenstandingbehaviorcoincidedwithbasalconcentrationsofprogesterone  ::;I ng/mI). On- set of estruswasthefirststandingeventduringbasalprogesterone.Duringeachperiod of observation,ambienttemperatureandnumberofheifersthatweremountingorthatstoodtobemountedwererecorded. Duration of EstrousCycles  n estrouscyclewastheintervalbetweenonset of twoconsecutiveperiods of estrus.Meanconcentration of progesterone(basal)duringestrus ±1 dwas.125ng/mI.Diestrus was theperiodwithinanestrouscyclewhenprogesteroneinserumexceededbasalprogesteronebytwostandarddeviations.Estrusandmetestruswerecombinedtorepresentintervalfromonset of estrustoonsetofdiestrus. StatisticalAnalysis Frequencydistributions of standingandmountingactivitywereconstructedandareaoftheseprofileswasconsideredtoindicatetotalactivityduringestrus.Keycomponents of area,peak,anddurationwerealsoexamined.Peakwasmaximalstandingormountingactivityperhourduringestrusandindicatedmaximalintensity of behaviorindependent of phase of estrus.Durationwastheintervalbetweenfirstandlaststandingormountingactivityduringbasalprogesterone.Thedatadescribedwereexaminedbytwo-factoranalysis of variancewithperiod of estrus as subplots(10).Bonferroni   statistics(10)wereusedtocontrastwithinmaineffect(EBand Be orwithin-treatmentcombinationamongperiods of estrus.Contrastsamongtreatmentcombinationswithinperiod of estruswerebyDunnett stest(10),andMBC-PEBheiferswereconsideredcontrols.  n all analysesofEBandBCeffectsonstandingormountingactivity,thenumber of heifersconcurrentlyinestrusandambienttemperaturewereincluded as covariates.Thus,covariancewasusedtoreducepotentialbiasduetonumber of heifersinestrus(11, 12 orambienttemperature(6, 8 . RESULTSANDDISCUSSION AllheiferswithadequatedietwereinPEB,gainedBW,andsustainedBC.Afterfirstestrus,heifersfedreduceddietaryenergywerein NEB andlostBW.For all NEBheifers,BCdeclinedbelowMBC(52.25)atthirdestrus.Thus,allfourdesignedtreatmentcombinationswereachieved(22)soitwaspossibletodetermineindependentandassociativeeffects of EBandBConbehaviorduringestrus.Insomepreviousreports(7,14),asign of estruswaswhenanimalsweremountedbutdidnotstand,butinthisstudy,only64 of thisactivitycoincidedwithbasalprogesterone.Incontrast,moststanding(98.2 )andmounting(91.7 )activitycoincidedwithbasalprogesterone,andthus,wasconfinedlargely to theperiovulatoryperiod.Thus,onlystandingandmountingactivityduringbasalprogesteroneareincludedinthisreport.Totaland peak ofstandingactivitywerenotinfluencedbyEB,BC,orinteractions(Figure1),but,inFBC-NEBheifers,duration of standinginfirstestruswaslonger  P<.OI thaninsecondandthirdestrus(Figure 1 . Duration of estrusdeclined as FBC-NEBheiferslostBC.DurationofstandingactivityinsecondandthirdestrusforFBC-NEBheifersdidnotdifferfromMBC-PEBheifers;thusFBCincreaseddurationofstandingactivity.Whydifferencesinduration of standingactivitydidnotcausedetecteddifferencesintotalstandingactivityarenotexplained.Insufficientnumberofheifersisnotalikelyexplanationbecauselesserdifferencesweredetectedforothervariables.Alternatively,similartotalactivitywasdistributeddifferentlyamonggroups.Specifically,inMBC-PEBandFBC-NEBheifers,95to100 of standingactivityoccurredwithin12h of onset.InMBC-NEBandFBC-PEB,only50to70 of standingactivityoccurredwithin 12 h of onset.Thus,frequency of activitythroughoutestruswaslesswithincreasedduration,sototalactivitydidnotdiffer.Total, pe k andduration of mountingactivity(Figure2)didnotdifferamongperiods of estrus,so data wereaveragedamongperiodswithintreatment.Contrastsweretodetermineinfluence of maineffectsandtreatmentcombinationsonmountingactivity.Totalactivityandpeak of mountingbehavior(Figure2)wereincreased  P<.OI byNEBbutnotaffectedby Be AsalientresultofthisexperimentisthatEBorBCdidnotaffecttotal,peak,orduration of standingactivity.Dietaryrestriction[65 of NRC(16)requirements]didnotaffectsecretion 10urnal of DairyScienceVol.73,No. 10 1990  vnLA-GODOY ET AL. o ~-- ----- ------ r--- a b MBC-MBC- FBC- FBC- PEB NEB PEB NEB TREATMENTCOMBINATIONS   > i=u e:{ -.J e:{  ::   0 0   > e:t  t I <J - c  l m >  l < 9   Z e:{ w   Cl. Z  >  t 0 Z ~ 0 l e:{  :: ::J 0 23 ESTRUS a   b ab   ~ab _ b -:-..--  b .- bb o ...J... . r 10 20 20 40 FigureI.Effects of energybalanceand body condition on standingbehavior of heifersduringthree periods of estrus.Heifers had moderate  MBC e orfat FBC)  0 body conditionandwere in positive  PEB - or negativeenergybalance  NEB -- . Estrus, total activity, and peak and duration of standingactivityaredefined in text.Treatmentcombinations and number of heiferswere:MBC-PEB n = 5),FBC-PEB n = 6),MBC-NEB n = 5), and FBCNEB  n = 4).a.b,cporeachvariable area, peak, orduration)meansamongorwithinestruswithdifferentsuperscriptdiffer  P<.05 . Pooled standarderrorsare:4.7for total activity, 1 5 for peak, and1.9forduration.Figure2.Effects of energybalance and body condition on monntingbehavior of heiferspooledamongthreesuccessive periods of estrus.Treatmentcombinationsandnumber of heifersweremoderate body condition  MBC  positiveenergy balance  n = 5),fat body condition FBC)PEB n = 6),MBC-negative energy balance  NEB n = 5), and FBC-NEB n = 4).a.bporeachvariable  area, peak or duration)meanswithdifferentsuperscriptsdiffer  P<.Ol . Pooledstandarderrorsare:6.0forarea,1.3 for peak, and8.6forduration. of estradiolfromdominantovulatoryfollicles of nonlactatingbeefcows 20);thus,noeffect of NEBonbehavioratestrusmight be expected.Four-foldgreaterjugularserumconcentrations of estradioldidnotaffectdurationorintensity of estrusinheifers 5). In addition,activityatestruswasnotaffectedinheifersfed80 NRCrequirementsforenergy,protein,andDM 14).Cattleinpreviousreports 14,20)werehousedingroups,NEBonthemwasnotdocumented,andBCwasnotcontrolled or tested. In FBCheifers,NEBreducedduration of standingasBCdeclinedandasduration of NEBincreased.Thus,EBandBCinteractedtoinfluencevariation of standingbehavior at estrus.Atthirdestrus,duration of standingactivityinFBC-NEBheifersdidnotdifferfromMBC-PEBheifers.Itisnotlikelythatreducedduration of standingactivityinFBC-NEBheifersactuallyreducesdetection of estrus. Area, peak, andduration of estrousactivityarecontinuousvariables,butdetection of estrusisadiscretevariable.Relativetosomepreviousreportsthatexaminedestrusdiscretely,weenhancedsensitivitytotesteffects of NEBandFBConbehavioratestrus in heifers.Fromthesedatainheifers,itispossiblethat EB orBCmaynotaffectdetectability of estrusinpostpartum dairy cows.Alternatively,heifers Journal of Dairy ScienceVol.73,No.10,1990  DIET,BODY CONDmON, AND ESTRUS IN HEIFERS 2763 TABLE2.Effects of energy balance aDd bodycoDdition on duration of estrouscycles in beifers.lTABLE3.Effects of energybalance and body condition on duration of diestrus in beifers.   TreatmentNumber of combination 2 heifers Estrous cycle  d 3 FlISt Second TreatmentNumber of combination 2 beifers Estrous cycle  f FlI St Second X SE X SE X SE X SE MBC PEB 521.3 .8 21.3.8 M C PIm 514.2.514.7.8 mC PEe 6 20.7.920.7.7 FBC PEB 6 13.7.813.5.9 M C NE 521.2 .5 22.7.9 M C NE 513.8 1.1 15.61.0 mC NE 4 24.3- .7 27 d 2.1 mC NE 417.0-1.320.0b2.1  Mean differs  P<.OS fromotherswithincolumn aDd row. ~ n differs P<.OI fromotherswithincolumn.lEstrouscycleswerenumberedaccordingtoperiods of precedingestrusandweredefinedasintervalbetweentwoconsecutiveonsets of estrus.2 Main effect of bodycoDdition BC was moderate MBC or fat  FBC). Main effect of energy ba1aDce was positive  PEB) or negative  NEB). Jay design third estrouscycleended in middiestrussoduration of estrouscycleafter third estrus was notmeasured. may be animperfectmodelforcowsbecausemagnitude of spontaneousNEB in lactatingcows 21 was5-to100foldgreaterthaninducedNEBinheifersinthisstudy. In fact,atfirstpostpartumovulation,NEB of cowsdetectedinestruswasless than EB or cowsnot detected inestrus 2 .Magnitude of EB forlactatingcowsnotdetectedinestrus 2 was two tothreefoldmorenegative than heifersinpresentexperiment 22 .Associations of magnitude of NEBandexpression of estrus at secondandthirdpostpartumovulations  breed ingperiod havenot been tested.Duringtheadaptationphase,duration of estrouscyclesforheifersdidnotdifferamongfourtreatmentcombinationsandaveraged20.4 ± .7d.During the experimentalphase, EB andBC, as maineffects,didnotaffectduration of estrouscycles 22.4 ± .7dinTable2 ,duration of diestrus 15.3 ± 1.1 d Table3 , or intervalsfromonset of estrustoonset of diestrus 5.2 ±   d in Table4 ,butNEBandFBCinteracted to prolongestrouscycles.Widevariation in length of bovineestrouscycleshasbeen re- ported 17,18 and is assumedtobeduelargelytoinefficientobservationsforestrus. In contrast,whennutritionisadequate,variationinintervalfromestrustoonset of diestruswasminimal in heifers 3 .Metabolicstatus of heif-  Mean diffrn fromolbers  P<.OS withincolumn.  Mean differsfrom others  P<.OI withincolumn.lDiestrus was intervalwithin an estrouscyclewhenprogesteronein serum exceeded mean atestrus ± 1 d by two standarddeviations.2 Main effect of bodycoDdition BC was moderate MBC orfat FBC . Main effect of energy balance was positive  PEB) or negative  NEB). ~st us cycles  periods of diestrus were numberedaccording to periods of precedingestrusandweredefined as intervalsbetweenconsecutiveonsets of estrus. By designthirdestrouscycleended in mid-diestrussoduration of diestrusafterthirdestrus was not measured.Valuesaremean ± standarderror. ersinthepresentstudyinfluencedduration of estrouscycles.ProlongedestrouscyclesinFBC-NEBheiferscouldbedue to extendeddiestrus,delayedonset of diestrusafterovulation. or reducedlutealdevelopment In thepresentstudy,onset of diestruswasdelayedinFBC-NEBheifers.Fastingdelayedovulation,andprolongedestrouscyclesinmice 4 ,soNEBmaydelayovulationincattle. In addition,reducedlutealweightandreducedslope of ascendingprogesteroneprofiles (1 to10dpostestrus supportthatlutealdevelopmentwasreducedinFBC-NEBheifers 22 .Thus,delayedonset of diestrusinFBC-NEBheifersisduepartiallytoimpairedlutealdevelopment. CONCLUSION No evidence of adverseindependentorassociativeeffects of EBand BC onstanding or mountingactivity of heifersinestruswas found SustainedFBCprolongedstandingbutreducedmountingactivity.The primary conclusionisthatneitherNEBnorFBCreduceexpression or detectability of estrusinheifers;thus,opportunitiesforinseminationshouldnotbeaffectedbyNEBorFBC.Twoissuesthatwarrantfurtherinvestigation:1 whethergreater Journal of DairyScienceVol.73,No.10,1990
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