Rev Colomb Cienc Pecu 2017; 30:30-38

30

Revista Colombiana de Ciencias Pecuarias

Original articles

Effect of nursing behaviour, sex of the calf, and parity order on milk production of buffaloes¤

Efecto del ccomportamiento de amamantamiento, sexo del becerro y orden del parto sobre la producción de leche en búfalos

Efeito do comportamento de amamentação, sexo do bezerro e ordem de parto sobre a produção de leite em bubalinos

Aparecida de FM Oliveira1, PhD; Celia R Quirino2, PhD; Rosemary Bastos2*, PhD.

1Instituto Federal de Educação, Ciência e Tecnologia do Espírito Santo, Alegre, Espírito Santo, Brasil.

2Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense “Darcy Ribeiro”, Campos dos Goytacazes, Rio de janeiro, Brasil.

(Received: September 18, 2015; accepted: September 9, 2016)

doi: 10.17533/udea.rccp.v30n1a04

¤ Tocitethisarticle:OliveiraAFM,QuirinoCR,BastosR.Effectofnursingbehavior,sexofthecalf,andparityorderonmilkproductionofbuffaloes.RevColombCiencPecu2017;30:30-38.

* Correspondingauthor:RosemaryBastos.LaboratóriodeReproduçãoeMelhoramentoGenéticoAnimal,CentrodeCiênciaseTecnologiasAgropecuárias,UniversidadeEstadualdoNorteFluminense“DarcyRibeiro”,Av.AlbertoLamego,2000,CCTA–P4–laboratório01térreo-ParqueCalifórnia,CamposdosGoytacazes,RJ,Brasil,Cep:28016-812.Tel.:+55-2227397196.E-mail:rosebast@gmail.com

Abstract

Background: theallonursingeffectondailymilkproduction(DMP)and totalmilkproduction(TMP)hasbeenlittleexplored. Objective:toevaluatetheeffectofnursingbehaviour,sexofthecalfandparityorder(PO)onDMPandTMPofbuffalocows.Methods:thirty-fivebuffalocowsandtheircalveswereevaluated.Observationswereperformedmonthly(threeconsecutivedays)fromMaytoNovember.Thenursingbehaviorwascharacterizedas:1)isolatedfilialnursing(IFN);2)collectivefilialnursing(CFN),and3)non-filialnursing(NFN). CowsweregroupedintofourcategoriestostudytheeffectsofnursingbehavioronDMPandTMP:1)non-permissive(NP);2)filialpermissive(FP);3)filialandcollectivefilialpermissive(FCFP);and4)filial,collectivefilialandnon-filialpermissive(FCFNFP).DMPwasrecordedthreedayspermonthandTMPwascalculatedasDMP*270daysoflactation.Results:sexofthecalfandsecondandthirdPOhadaneffectonnursingbehavior(p<0.05).DMPandTMPweresignificantlyaffectedbycalfsexandnursingbehaviour(p<0.05).PO hadnoeffectonDMPandTMP.Conclusion:our resultssuggest thatnursingbehaviour isassociatedwithmilkproductioninbuffalocows.BuffalocowsthatacceptalltypesofnursingbehaviourhadthehighestDMPandTMP.Sexofthecalfinfluencednursingbehaviour,DMP,andTMP,sothatbuffalocowswithmalecalvesdisplayedmorefrequentallonursingbehaviourandyieldedmoremilk.

Keywords: allonursing, alloparental care, Bubalus bubalis, suckling.

31

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

Resumen

Antecedentes:elcomportamientodelalo-amamantamientosobrelaproduccióndiariadeleche(DMP)yproduccióntotaldeleche(TMP)hasidopocoexplorado.Objetivo:evaluarelefectodelcomportamientodeamamantamiento,elsexodelbecerroyelordendeparto(PO)enlaDMPyTMPdebúfalas.Métodos: seevaluaron35hembrasbufalinasysuscrías.Lasobservacionesserealizaronmensualmente(durantetresdíasconsecutivos)entremayoynoviembre.Elcomportamientodeamamantamientosecaracterizócomo:1)amamantamientofilialaislado(IFN);2)amamantamientofilialcolectivo(CFN)y,3)amamantamientonofilial(NFN).ParaevaluarlosefectosdelcomportamientodeamamantamientoenlaDMPyTMP,lasvacasfueronagrupadasen4categorías:1)nopermisivas(NP);2)permisivafilial(FP);3)permisivafilialycolectivafilial(FCFP)y4)permisivafilial,colectivafilialynocolectiva(FCFNFP).LaDMPseregistrótresdíaspormes,ylaTMPfuecalculadacomoDMP*270díasdelactancia.Resultados:elsexodelbecerro,elsegundoytercerPOtuvieronefectosobreelcomportamientodeamamantamiento(p<0.05).LaDMPylaTMPseafectaronsignificativamenteporelsexodelbecerroyelcomportamientodeamamantamiento(p<0.05).ElPOnotuvoefectosobrelaDMPylaTMP.Conclusión: nuestrosresultadossugierenqueelcomportamientodeamamantamientoestáasociadoalaproduccióndelecheenvacasbubalinas.LasbúfalaspermisivasatodotipodeamamantamientopresentaronmayorDMPyTMP.Elsexodelbecerroinfluyóenelcomportamientodeamamantamiento,enlaDMPyenlaTMP.Lasbúfalasconbecerromachopresentaroncomportamientodealo-amamantamientomásfrecuenteyprodujeronmayorcantidaddeleche.

Palabras clave: aloamamantación, Bubalus bubalis, cuidado aloparental, lactación.

Resumo

Antecedentes:ocomportamentodealo-amamentaçãosobreaproduçãodeleitediária(DMP)eproduçãodeleitetotal(TMP)temsidopoucoexplorado.Objetivo:avaliaroefeitodocomportamentodeamamentação,sexodosbezerroseordemdeparto(PO)naDMPeTMPemvacasbubalinas.Métodos:trintaecincofêmeasesuascriasforamavaliadasnoestudo.Asobservaçõesforamrealizadasmensalmente(trêsdiasconsecutivos)demaioanovembro.Ocomportamentodeamamentaçãofoicaracterizadocomo1)amamentaçãofilialisolada(IFN);2)amamentaçãocoletivafilial(CFN)e3)amamentaçãonãofilial(NFN).ParaavaliarosefeitosdocomportamentodaamamentaçãonaDMPeTMP,asvacasbubalinasforamagrupadasem4categorias:1)nãopermissiva(NP);2)permissivafilial(FP);3)permissivafilialecoletivafilial(FCFP)e4)permissivafilial,coletivafilialenãofilial(FCFNFP).ADMPfoiregistradatrêsdiasparacadamêseaTMPfoicalculadacomoDMP*270diasdelactação.Resultados:osexodosbezerros,asegundaeterceiraPOtiveramefeitosnocomportamentodeamamentação(p<0.05).ADMPeTMPforamsignificativamenteafetadaspelosexodosbezerrosecomportamentodeamamentação(p<0.05).APOnãoteveefeitonaDMPeTMP.Conclusão: nossosresultadossugeremqueocomportamentodeamamentaçãoestãoassociadosaproduçãodeleiteemvacasbubalinas.AsvacasbubalinasquesãopermissíveisatodosostiposdeamamentaçõesforamaquelascommaiorDMPeTMP.Osexodosbezerrosinfluenciouocomportamentodeamamentação,DMPeTMP,sendoqueasvacasbubalinasquepossuembezerrosmachosapresentaramfrequentecomportamentodealo-amamentaçãoeproduzirammaioresquantidadesdeleite.

Palavras chave: aloamamentação, Bubalus bubalis, cuidado aloparental, mamada.

Introduction

In some species, during the nursing periodlactatingfemalesoccasionallynurseoffspringthatarenottheirown,abehaviourreferredtoasallonursing(Riedman,1982;Hooglandet al.,1989).Allonursingcancontributetomaternalwelfare,udderhealthandmilkqualitybyreducingpainfulmilkpressureandudderinfections,whichmaximizesmilkproduction(Roulin,2002).

Oneof thegreat benefits for allosucklers is thecompensationofsomeimportantdeficienciesatbirth,suchaslowbirthweightormaternalmilkinsufficiency(VíchováandBartos, 2005).Allosucklersmayalsogain immunologicalbenefitsbysuckling frommorethanonenursingmother,thusobtainingvariousspecificimmunologicalcompounds,whichimproveresistanceagainstpathogens(RoulinandHeeb,1999).Besidesthis,allosucklerscanalsoingurgitateextramilkandtherebyobtainadditionalenergy(Packeret al.,1992).

32

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

However,allonursingmayimplycosts,becauselactationisthemostenergeticallyexpensivestageinmammals(Clutton-Brocket al.,1989).Inaddition,milk transfercould reduce theamountofnutrientsavailable to the current calf (Mendl, 1988) andallonursing can spread pathogens to a number ofcalvessimultaneously(RoulinandHeeb,1999).

Somenon-mutually exclusive hypotheses havebeenproposedtoexplainwhylactatingfemalesnursealienoffspring:misdirectedparentalcare(Packeret al.,1992),reciprocity(Ekvall,1998;Engelhardtet al., 2015;Glonekovet al., 2016), kin selection (PuseyandPacker,1994;Ekvall,1998;EberleandKappeler,2006;Engelhardtet al., 2016),evacuationofleftovermilk(RiedmanandLeBoeuf,1982;Wilkinson,1992),inexperienceoffemales(Murpheyet al.,1991;1995),andmilktheft(Murpheyet al.,1995;Maniscalcoet al.,2007;Zapataet al.,2009;Engelhardtet al.,2014;Glonekovet al.,2016).

Inbuffaloes,theallonursingbehaviourwasfirstobservedinaferalherdofCarabaobuffalos(Tulloch,1979)andwassubsequentlyreportedbyMurpheyet al. (1991;1995),ParanhosdaCostaet al.(2000),Andrioloet al.(2001)andMadella-Oliveiraet al.(2010).Theeffects of calf sex andbirthorder inbuffaloes candecisivelyinfluencesocialinteractionsduringsucking,promoting differential development among calves(ParanhosdaCostaet al.,2000).IntheIberianreddeer(Cervus elaphus hispanicus),thecomparisonbetweenhindmilkproduction(MP)andallosuckingfrequencyshowsthatthepercentageofallosuckingboutsincreasesastheMPofthenursingmothersdecreases(Landete-Castillejoset al.,2000).

Theobjectiveof this studywas to evaluate thepotentialeffectsofthecalfsexandparityorder(PO)onnursingbehaviour,DMP,andTMPofbuffalocows.

Materials and methods

Ethical considerations

The experimental protocolwas reviewed andapprovedbytheEthicsCommitteeonAnimalUseofUniversidadeEstadualdoNorteFluminenseDarcyRibeiro,Brazil(approvalnumber:262/2014)

Location and animals

ThestudywasconductedatCataiafarminSãoFrancisco do Itabapoana, Rio de Janeiro, Brazil(21º18’07”S and40º57’41”W, at an altitudeof 8m.a.s.l.).Inthisstudy,outbredMurrah,JaffarabadiandMediterraneanfemales(n=35;aged3to12yearsold) and their calveswere investigated.Thegroupincludedprimiparous(n=2)andmultiparousfemales(n=33).Calves(15malesand20females)includedinthestudywereallborninMarch(n=14),April(n=9),andMay(n=12).

Damsandcalveswereindividuallyidentifiedwithyellowoilpaint,withordinarynumberspaintedonthehindquarters.Matchingnumberswereassignedtothecowandcalf;sotheycouldbeidentifiedfromadistance.Plasticearringswereputontheanimals,sothattheywerepermanentlyidentified.Theanimalswere habituated to the horseback observer insidepasture for at least 15 days before beginningdatacollection.Duringthisperiod,theobserverconductedthe training using a protocol. Following the farmroutine,eachcowandhercalfwereallocatedfor15daysinamaternitypasturesystem(separatedfromotherfemales).Milkingbeganat4:00h,whenfemalesweremanuallymilkedinthepresenceoftheircalves.Aftermilking,around6:00h,theherdwascarriedtothepasture(measuring60hectares),whereallfemalesremainedwiththeircalvesuntil12:00h.Thestockingrateusedwas0.73AU/ha.Theherdwasremovedat12:00handthemotherswerethenplacedinapastureawayfromtheircalves.

Datawere collected during three days at thebeginning of eachmonth (May to November).Observationswere direct and continuous between6:00and12:00h(MartinandBateson,1986).Theobserverwasinadistanceofaround10mfromtheanimals.Abinocularwasusedfor identificationofnumbersatadistance,toavoidinterferencewiththebehaviouroftheanimals.Allanimalswereinsightatalltimes.Atimerwasusedtoregisternursingtime,followedbyidentificationofthecowandcalf.Thetimingofthestartandendofnursingwasregisteredinanaudiorecorder.Nursingwasconsideredtobeginfromthemomentthecalfattachedtotheteatwithasucklingmovement.

33

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

Nursing behaviorwas characterized into threetypes:1)isolatedfilialnursing(IFN):whenthefemalewasnursingitsowncalf;2)collectivefilialnursing(CFN):whenafemalebegannursingitsowncalfaswell asoneormore alien calves; and3)non-filialnursing(NFN),whenafemalewasnursingoneormorecalvesthatwerenothers.

Tostudytheeffectofnursingbehaviorondailymilk production (DMP) and totalmilk production(TMP),femalesweregroupedintofourcategories:1)non-permissive(NP):femalesthatdidnotallowanykindofnursing;2)filialpermissive(FP):femalesthatallowedIFN;3)filialandcollectivefilialpermissive(FCFP):femalesthatallowedtwotypesofnursingbehaviour: IFN andCFN; and 4) filial, collectivefilial andnon-filial permissive (FCFNFP): femalesthatallowedthreetypesofnursingbehaviour:IFN,CFN,andNFN.

Milkwascollectedfromeachcowandquantifiedduring thesame threedayspermonthwhennursingbehaviorwasobserved.DMPwas registered inKgs.TMPwasdefinedastheamountofmilk(Kg)producedthroughoutthelactationperiod(270days).

Statistical analysis

ThedatawereanalyzedusingSAS(SASInstituteInc,Cary,NC,USA). Frequencyof behaviorwasanalyzedwith the chi-square test (PROCFREQ).Forotherdata,weusedPROCMIXEDtofitalinearmodel for repeatedmeasures.Animalwas used asthe randomeffect,whilenursingbehaviour, sexofcalf,month of observation and parity orderwerefixed effects.Results are reported as least squaremeans(LSMEANS)withstandarderror(SE)givenbythePROCMIXED.Weusedp≤0.05asthelevelof statistical significance forall tests.Theanalysismodelwasasfollows:

Yijklm=m+TMi +Sj +MOk +POl +an+eijklm

Where:

Yijklm = dailymilk production and totalmilkproduction.

m=generalaverage.

TMi =effectofithnursingbehavior.

Sj =effectofsexofthejthcalf.

MOk =effectofkthmonthofobservation.

POl =effectoflth parity order.

an=randomeffectofanimal.

e ijklm = random error associated with eachobservation(N~0.1).

Results

Nursing behaviour

ResultsinTable1shownodifferenceindurationofnursingbetweenbuffalocowswithmaleorfemalecalves.FrequencyanddurationofnursingbehaviourfortheIFNweresignificantlygreaterinrelationtoCFNandNFN(p<0.05).TherewasalsosignificantdifferenceinrelationtofrequencyanddurationforCFNandNFN(p<0.05).Frequencyofnursingwasgreater in buffalo cowswithmale calves (p<0.05)thancowswithfemalecalves(Table1).

Differencesinfrequencyanddurationofnursingbehaviorwereobserved(p<0.05).InMay,frequencyofnursingbehaviorwassignificantlygreatercomparedwithJune,September,andNovember,anddurationof nursing behavior was higher comparedwithJune,September,October,andNovember(p<0.05).A significant difference for frequency of nursingbehaviorwasobservedbetweenNovemberandJuly,August,October (p<0.05).Regarding duration ofnursingbehavior,adifferencewasobservedbetweenNovemberandtheothermonths(p<0.05).

For the PO among buffalo cows there werestatisticallysignificantdifferencesinfrequencyanddurationofnursingbehavior(p<0.05).Buffalocowsin 2nd and3rd POhadgreater frequency values ofnursingbehaviorcomparedwithcowsin1stand4th PO.Regardingdurationofnursingbehavior,cowsin2ndand3rdPOhadgreatervaluescomparedwiththeotherPOs(p<0.05).

34

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

Table 1. Least square means and standard errors (SE) for frequency (episode/day) and duration (sec/day) of nursing type allowed by buffalo cows, calf sex, month, and parity order (PO).

Factors N Frequency(episode/day)

Duration (sec/day)

Nursing behaviour

IFN 226 0.38 ± 0.02a 181.1 ± 13.6a

CFN 226 0.08 ± 0.02b 29.6 ± 13.6b

NFN 226 0.002 ± 0.00c 2.5 ± 13.6c

Sex of calve

Male 294 0.20 ± 0.2a 71.8 ± 12.0a

Female 384 0.12 ± 0.02b 70.3 ± 11.0a

Observation month

May 90 0.30 ± 0.04a 122.2 ± 20.9a

June 105 0.12 ± 0.02bc 27.0 ± 19.4b

July 105 0.23 ± 0.04ab 78.1 ± 19.4a

August 105 0.19 ± 0.04ab 68.5 ± 19.4a

September 105 0.12 ± 0.04bc 28.7 ± 19.4b

October 93 0.16 ± 0.04ab 35.0 ± 20.4b

November 75 0 ± 0c 0 ± 0c

Parity

1st 39 0.07 ± 0.06b 25.9 ± 29.1a

2nd 96 0.29 ± 0.04a 102.4 ± 19.6b

3rd 39 0.29 ± 0.06a 157.6 ± 27.8b

4th 60 0.03 ± 0.05b 22.3 ± 22.8a

5th 192 0.13 ± 0.03ab 56.7 ± 13.7a

6th 108 0.14 ± 0.04ab 77.5 ± 17.0a

≥7th 144 0.17 ± 0.03ab 55.0 ± 14.5 a

IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non-filial nursing. N: number of observations. Means followed by different superscript letters (a, b, c) within the same column are significantly different (p<0.05).

Nursing behavior in relation to calf sex and PO

Figure1showsthatfrequency(A)andduration(B)of IFNwere significantlygreater in relation toCFNandNFN forbothcowswithmaleor femalecalves(p<0.05).Asignificantdifferencewasfoundinrelationtoduration(B)forCFNandNFNforbothcowswithmaleandfemalecalves(p<0.05),butnotforfrequency.

Resultsshowthatfrequency(A)ofIFNwashigherfor cowswithmale than thosewith female calveswere (p<0.05) for each nursing type.Cowswithfemalecalvesshowedhighervaluesforduration(B)ofIFNthanthosewithmalecalves(p<0.05).Besides,

frequency(A)andduration(B)ofnursingbehaviourforCFNweresignificantlygreaterinrelationtoNFNwhen comparing cowswithmale versus femalecalves(p<0.05).

Figure 1. Least square means and standard errors (SE) of the (A) frequency (episode/day) and (B) duration (sec/day) of each nursing type in relation to sex of the calf. IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non-filial nursing. Means with different superscript lowercase letters (a, b, c) show significant difference between nursing types (p<0.05) and means with different superscript uppercase letters (A, B) show significant difference between calf sex with regards to nursing type (p<0.05).

Figure2showsthefrequency(A)andduration(B)oftypesofnursingbehaviorinrelationtoPO.Exceptfor thesecondPO,whichshowednodifference infrequencybetweenIFNandCFN,thefrequencyanddurationof IFNwere statistically significantwhencomparedwithCFNandNFNforallPOs(p<0.05).

Factors affecting DMP and TMP: nursing behavior, calf sex, month of observation, and PO.

Theaveragelactationlengthfortheseanimalswas213.42days,withastandarddeviationof66.11days.TheDMPandTMPinrelationtonursingbehavior,calfsex,month,andPOincowsareshowninTable2.

Thenursingbehavioramongthe35buffalocowswasdistributedasfollows:3wereNP,18FP,7FCFP,

35

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

Figure 2. Least square means and standard errors (SE) of (A) frequency (episode/day) and (B) duration (sec/day) of each nursing type in relation to PO. IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non-filial nursing. PO: parity order. Means followed by different superscript letters (a, b) are significantly different within each PO (p<0.05).

and7FCFNFP.Asshown,DMPandTMPforcowswithFCFNFPweresignificantlyhighercomparedtothosewithNP,FPandFCFP(p<0.05).

TheDMPandTMPincowswithmalecalfweresignificantlygreater than thatof cowswith femalecalf(P<0.05). Duringtheobservedmonths,thepeakofDMPandTMPoccurred inMay.Adecrease inDMPandTMPwasobservedfromJunetoNovember(Table2).ThePOamongcowsdidnothaveaneffectonDMPnoronTMP(Table2).

Discussion

Our results show that collective nursing occurin buffalo cows, in agreementwith other studies(Murpheyet al.,1991;1995;ParanhosdaCostaet al., 2000;Andriolo et al., 2001).The IFNvaluesfor frequency anddurationwere higher thanCFNandNFN,differentthanreportedbyAndrioloet al.

Table 2. Least square means and standard errors (SE) of daily milk production (DMP) and total milk production (TMP) in relation to nursing behavior, sex of calves, month of observation, and parity order (PO) in buffalo cows.

Factors N DMP ± SE(Kg/day)

TMP ± SE(Kg)

Nursing behavior

NP 65 3.2 ± 1.2b 861.9 ± 310.0b

FP 334 3.0 ± 1.2b 818.1 ± 321.0b

FCFP 134 3.1 ± 1.3b 838.2 ± 337.3b

FCFNFP 135 3.5 ± 1.3a 945.0 ± 347.5a

Sex of calves

Male 387 4.4 ± 0.2a 1171.1 ± 53.2a

Female 381 3.7 ± 0.2b 1110.5 ± 50.6b

Observation month

May 90 6.9 ± 0.3a 1853.0 ± 76.2a

June 104 5.2 ± 0.3b 1418.6 ± 71.0b

July 105 4.4 ± 0.3c 1178.7 ± 71.0c

August 102 3.5 ± 0.3d 947.4 ± 71.9d

September 105 2.8 ± 0.3e 766.8 ± 71.0e

October 87 2.7 ± 0.3e 731.1 ± 76.5e

November 75 2.7 ± 0.3e 739.9 ± 80.8e

Parity

1st 39 4.3 ± 0.4a 1198.0 ± 118.1a

2nd 92 3.9 ± 0,3a 1105.5 ± 86.4a

3rd 39 4.0 ± 0.4a 1067.5 ± 112.9a

4th 60 4.5 ± 0.4ab 1123.8 ± 98.0ab

5th 189 3.9 ± 0.2a 1065.3 ± 65.5a

6th 105 3.5 ± 0.3b 918.8 ± 76.4ab

≥7th 144 4.4 ± 0.2ab 1156.5 ± 59.3ab

Nursing behavior: NP: non-permissive; FP: filial permissive; FCFP: filial and collective filial permissive and FCFNFP: filial, collective filial and non-filial permissive. N: number of observations. Means followed by the different superscript letters (a, b, c, d, e) within the same column are significantly different (p<0.05).

(2001),whoobservedlowervaluesforoccurrenceanddurationofIFNcomparedtoCFN.Thelowvaluesforcollectivenursingsuggestthatfarmmanagementinterfereswiththisbehavior.

The sex of the calf had an effect on nursingbehaviour;cowswithmalecalvesdisplayedgreaternursingfrequencythantheoneswithfemalecalves,andthefrequencyanddurationofIFNforbothweremore evident comparedwith other nursing types(CFNandNFN). Paranhos daCostaet al. (2000)

36

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

demonstratedthatmalecalvesspendgreatertimeinindividualfilialandincommunalnon-filialsucklingthanfemalecalves,whichshowsgreatercommunalfilialsuckling,suggestingthatthesexoftheoffspringdeterminesdifferences in allonursing strategies. Inbovinecattle,calfsexhadnoeffectonallosuckingfrequencyandgrowthgainof the calves (VíchováandBartŏs,2005).Zapataet al.(2010)demonstratedthat the relationship between allosuckling and theoffspring sexwas not evident in guanacos (Lama guanicoe).

Nursingbehaviourwasmoreprevalent inMay,JulyandAugust.Andrioloet al.(2001)showedthatsuckling behavior varied according to the periodof observation.Therewere increased suckling anddecreasedfilialsucklingduringthefirstfourmonths,while a decrease following the gradual process ofweaningwas observed after the fourthmonth ofnursing.

Our results showed differences in duration ofnursing behaviour for cows in 2nd and 3rd PO. ThefrequencyandthedurationofIFNwerehigherwhencomparedwithCFN andNFN in all POs, exceptforthesecondPO.Thisindicatestheimportanceoffilialnursing toensurecalfnutrition.According toGlonekováet al.(2016),notonlyfemaleparityaffectsthe probability of successful suckling involvingnon-filialcalves,butalsotheorderofcalfsuckling(whichcalfcametosucklefirst,second,etc.).Thus,othervariablesshouldbeevaluated,suchasageofthecalf,ageofthenursingfemale,andhierarchyrankdifferencesbetweenthenursingfemaleandtheownmotherofthecalf.

Ourresultsshowthatcowsthatwerepermissibleto all types of nursing behaviour (filial, collectivefilialandnon-filial)presentedhigherDMPandTMP.We thus infer that cowspermittingmore thanonenursingbehaviour aremore stimulated to producemoremilk.The cow-calf interaction is importanttoreleaseoxytocin,ahormonethatstimulatesmilkejection(PollackandHurnik,1978).Inbovinecows,Silveiraet al. (1993)demonstratedthatthefrequencyofoxytocin release followingsucklingwasgreaterintheowngroupwhencomparedtothealiengroup,thusthereleaseofoxytocinwasaffectedbymother-youngbonds.

IntheIberianreddeer,thepercentageofallonursingboutsincreasedwithincreasingmilkproductionbythenursinghind,butthepercentageofallosucklingbouts increased asmilk production of themotherdecreased (Landete-Castillejoset al.,2000),whichshowsadifferencebetweennursingbehaviorofthefemaleandsucklingbehaviorofthecalfinrelationtomilkproduction.

Furthermore, cowswithmale comparedwithfemalecalvesshowedhigherDMPandTMP.ThisisinagreementwithLandete-Castillejoset al.(2005),who showed that for Iberian red deer calvesmilkyieldwasgreaterindamswithmalesthanindamswith females.However, Paranhos daCosta et al. (2000)whodidnotobserveasignificantrelationshipbetweenmilkproductionandsexofthecalfdescribeddifferentresults.

ThepeakofDMPandTMPoccurredinMay.FromJunetoNovember,DMPandTMPdecreased.DMPwas6.9±0.3Kg/dayinMay,butatthebeginningofJune,productionbegan todeclineuntilNovember,reaching2.7±0.3Kg/day.Cerón-Muñozet al.(2002)showedthatproductioninthefirstmonthoflactationwas 6.87Kg, declining until the ninthmonth oflactation,with3.83Kg.Hurtado-Lugoet al.(2005)obtained high values at the beginning of lactation(4.64Kgto3.04±1.17Kg).WeobservedthatTMPranged from1853.0±76.2 (May) to 739.9±80.8(November)Kg.SampaioNetoet al.(2001)reportedtotalmilkproductionof2130.80±535.60Kg,andJunioret al.(2014)foundavalueof2218.03Kg.

OurresultsdidnotshowadefinitepropensityforachangeinthepatternofDMPandTMPrelatedtoPO.TheseresultsarenotinagreementwithSampaioNetoet al.(2001),Afzalet al.(2007)andPawaret al.(2012),becausethesestudiesshowedDMPwasaffectedbyfemaleparity.ThefactthatwedidnotfindadifferencebetweenPOandDMPandTMPmayberelated to thequalityof thepasture, sincepasturesarenative,withlownutritionalquality,andnoothersupplementaryfeedwasprovidedtotheanimals.

Inaddition,geneticandnon-genetictraitsshouldbe taken into consideration formilk productionparameters. Genetic improvement is related toselection, while non-genetic factors involve

37

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

management,quantityandqualityoffeed,andseason(Afzalet al.,2007).

In conclusion, our results suggest that nursingbehaviour is associatedwithmilk production inbuffalocows.FemalesthatarepermissibletoalltypesofnursingbehaviourhadthehighestDMPandTMP.Thesexofcalvesinfluencednursingbehaviour,DMPandTMP,socowswithmalecalvesdisplayedmorefrequentallonursingbehaviourandproducedhigheramountsofmilk.Femalescanpresentdifferenttypesofnursingbehaviour,independentfromPO,butIFNwasmoreevidentinallPOs.TheDMPandTMPwerenotaffectedbyPO.

Acknowledgements

ToMr.AloísioSiqueiradeAlmeida,farmowner,and his assistants, for allowing us to conduct theexperiment,andFAPERJforfinancialsupport(grantNo.E-26/170.645).

Conflicts of interest

The authors declare they have no conflicts ofinterestwith regard to thework presented in thisreport.

ReferencesAfzalM,AnwarM,MirzaMA.SomefactorsaffectingmilkyieldandlactationlengthinNiliRavibuffaloes.PakistanVetJ2007;27(3):113-117.

AndrioloA,ParanhosdaCostaMJR,SchmidekWR.Sucklingbehaviourinwaterbuffalo(Bubalus bubalis):developementandindividualdifferences.RevistEtol2001;3(2):129-136.

Cerón-MuñozM,TonhatiH,Duarte J.Munõz-BerrocalM,Jurado-GámezH.Factorsaffectingsomaticcellcountsandtheirrelationswithmilkandmilkconstituentyieldinbuffaloes.JDairySci2002;85:2885-2889.

Clutton-BrockTH,Albon,SD,GuinnessFE.Fitnesscostofgestationandlactationinwildmammals.Nature1989;337:260-262.

Eberle,M,Kappeler,PM.Familyinsurance:kinselectionandcooperativebreedinginasolitaryprimate(Microcebus murinus).BehavEcolSociobiol2006;60:582-588.

EkvallK.Effects of social organization, age and aggressivebehavioronallosucklinginwildfallowdeer.AnimBehav1998;56:695-703.

EngelhardtSC,WeladjiRB,HolandO,RiojaCM,EhmannRK,NieminenM.Allosuckling in reindeer (Rangifer tarandus):milk-theft,mismothering or kin selection?Behav Processes2014;107:133-141.

EngelhardtSC,WeladjiRB,HolandO,RoedKH,NieminenM.Evidenceofreciprocalallonursinginreindeer,Rangifer tarandus. Ethology2015;121:245–259.

EngelhardtSC,WeladjiRB,HolandO,NieminenM.Allosucklinginreindeer(Rangifer tarandus):atestoftheimprovednutritionandcompensationhypotheses.MammBiol2016;81:146-152.

GlonekováM,BrandlováK,PluhácekJ.Stealingmilkbyyoungandreciprocalmothers:highincidenceofallonursingingiraffes.Giraffa cameloparalis.AnimBehav2016;113:113-123.

Hoogland JL,TamarimRH,LevyCK.Communal nursing inprairiedogs.BehavEcolSociobiol1989;24(2):91-95.

Hurtado-LugoN,Cerón-MuñozM,TonhatiHGutierrez-ValenciaA,HenaoA.ProduccióndelecheembúfalasdelaCostaAtlánticaColombiana.LivestResRuralDevelop2005;17:12.

Junior JSB, FragaAB,CoutoAG,BarrosCC, SilvaRMO.Produçãodeleite,duraçãodalactaçãoeintervalodepartosembúfalasmestiçasMurrah.RevCaatinga2014;27(2):184-191.

Landete-CastillejosT,GarciaA,GardeJ,GallegoL.Milkintakeandproduction curves and allosuckling in captive Iberian reddeer, Cervus elaphus hispanicus.AnimBehav2000;60:679-687.

Landete-CastillejosT,GarciaA,López-SerranoFR,GallegoL.Maternal quality and differences inmilk production andcompositionformaleandfemaleIberianreddeercalves(Cervus elaphus hispanicus).BehavEcolSociobiol2005;57:267–274.

Madella-oliveiraAF,BastosR,QuirinoCR.Comportamentode amamentação emamada embubalinos, suas relações comperíododelactação,idadeesexodosbezerros.RevCeres2010;57(2):211-217.

ManiscalcoJM,HarrisKR,AtkinsonS,ParkerP.AlloparentinginStellersealions(Eumetopias jubatus):Correlationswithmisdirectedcareandotherobservations.JEthol2007;25(2):125-131.

MartinPandBatesonPBATESON,P.Measuringbehaviourand introductory guide. Cambridge: CambridgeUniversityPress,1986.

MendlM,1988.Theeffectsoflittersizevariationonmother-offspringrelationshipsandbehaviouralandphysicaldevelopmentinseveralmammalianspecies(principallyrodents).JZool(Lond)1988;215:15-34.

MurpheyRM,ParanhosdaCostaMJR,LimaLOS,DuarteFAM.Communalsuckinginwaterbuffalo(Bubalus bubalis).ApplAnimBehavSci1991;28:341-352.

MurpheyRM,ParanhosdaCostaMJR,GomesdaSilvaR,SouzaRC.Allonursing in river buffalo,Bubalus bubalis: nepotism,incompetence,orthievery?AnimBehav1995;49(6):1611-1616.

PackerC,LewisS,PuseyA. Acomparative analysis of non-offspringnursing.AnimBehav1992;43(2):265-281.

38

Rev Colomb Cienc Pecu 2017; 30:30-38

Oliveira AFM et al. Nursing, calf sex, and parity on milk yield of buffaloes

ParanhosdaCostaMJR,AndriolloA,OliveiraJFS,SchimidekWR.Suckling and allosuckling in riverbuffalo calves and itsrelationwithweightgain.ApplAnimBehavSci2000;66(1):1-10.

PawarHN,RaviKumarGVPPS,NarangR.Effectofyear,seasonandparityonmilkProductiontraitsinMurrahbuffaloes. JBuffaloSci2012;1:122-125.

PollackWE,HurnikJF.Effectofcalfcallsonrateofmilkreleaseofdairycows.JDairySci1978;61:1624-1626.

PuseyAE,PackerC.Non-offspringnursinginsocialcarnivores:minimizingthecosts.BehavEcol1994;5(4):362-374.

RiedmanML,LeBoeufBJ.Mother–pupseparationandadoptioninnorthernelephantseals.BehavEcoSociol1982;11(3):203-215.

RoulinA,HeebP.Theimmunologicalfunctionofallosuckling. EcolLett1999;2(5):319-324

RoulinA.Whydo lactating females nurse alien offspring?Areviewofhypothesesandempiricalevidence.AnimBehav2002;63(2):201-208.

SampaioNeto, JC,MartinsFilho,R,Lôbo,RNB,Tonhati,H.Avaliação dos desempenhos produtivos e reprodutivos de umrebanho bubalino noEstado doCeará.RBrasZootec 2001;30(2):368-373.

SAS–InstituteInc.StatisticalAnalysisSystemuser’sguide.Version9.3ed.SASInstituteInc.Cary,NorthCarolina,USA,2012.

SilveiraPA,SpoonRA,RyanDP,WilliamsGL.Evidence formaternal behavior as a requisite link in suckling-mediatedanovulationincows.1993;49(6):1338-1346.

TullochDG.Thewaterbuffalo,Bubalus bubalis, inAustralia:Reproductiveandparent-offspringbehaviour.AustWildlifeRes1979;6(3):265-287.

VíchováL,BartošL.Allossucklingincattle:gainorcompensation?ApplAnimBehavSci2005;94:223-235.

WilkinsonGS.Communalnursingintheeveningbat,Nycticeius humeralis,BehavEcolSociobiol1992;31:225-235.

ZapataB,CorreaL, Soto-GamboaM,LatorreE,González,BA,EbenspergerLA.Allosucklingallowsgrowingoffspringtocompensate for insufficientmaternalmilk in farmedguanacos(Lama guanicoe).ApplAnimBehavSci2010;122:119-126.

ZapataB,González,BA,EbenspergerLA.Allonursingincaptiveguanacos,Lama guanicoe:milktheftormisdirectedparentalcare?Ethology2009;115:731-737.