ContentslistsavailableatScienceDirect
Animal
Reproduction
Science
j o ur na l h o me p a g e:ww w . e l s e v i e r . c o m / l o c a t e / a n i re p r o s c i
Using
UHF
proximity
loggers
to
quantify
male–female
interactions:
A
scoping
study
of
estrous
activity
in
cattle
C.J.
O’Neill
a,b,∗,
G.J.
Bishop-Hurley
c,
P.J.
Williams
d,
D.J.
Reid
e,
D.L.
Swain
b aCSIRO,AgricultureFlagship,AustralianTropicalScienceandInnovationPrecinct,Building145,JamesCookDrive,Townsville, QLD4814,AustraliabSchoolofMedicalandAppliedSciences,CQUniversity,NorthRockhampton,QLD4701,Australia
cCSIRO,AgricultureFlagship,QueenslandBiosciencePrecinct,306CarmodyRoad,St.Lucia,QLD4067,Australia dTropicalBeefTechnologyServices,POBox809,Rockhampton,QLD4700,Australia
eAgri-ScienceQueensland,DAFF,NorthRockhampton,QLD4701,Australia
a
r
t
i
c
l
e
i
n
f
o
Articlehistory: Received6March2014 Receivedinrevisedform 17September2014 Accepted19September2014 Availableonline8October2014 Keywords: Biotelemetry Estrousdetection Behavior Ultrasonography Cattle
a
b
s
t
r
a
c
t
Reproductiveefficiencyisanimportantdeterminantofprofitablecattlebreedingsystems andthesuccessofassistedreproductivetechniques(ART)inwildlifeconservation pro-grams.Methodsofestrousdetectionusedinintensivebeefanddairycattlesystemslack accuracyandremainthesinglebiggestissueforimprovementofreproductiveratesand suchmethodsarenotpracticalforeitherlarge-scaleextensivebeefcattleenterprisesor free-livingmammalianspecies.RecentdevelopmentsinUHF(ultrahighfrequency) prox-imityloggertelemetrydeviceshavebeenusedtoprovideacontinuouspair-wisemeasure ofassociationsbetweenindividualanimalsforbothlivestockandwildlife.Theobjectiveof thisstudywastoexplorethepotentialofusingUHFtelemetrytoidentifythereproductive cyclephenotypeintermsofintensityanddurationofestrus.Thestudywasconductedusing BelmontRed(interbredAfricanderBrahmanHereford–Shorthorn)cattlegrazingirrigated pastureonBelmontResearchStation,northeasternAustralia.Thecow-bullassociations fromthreegroupsofcowseachwithonebullwererecordedovera7-weekbreeding sea-sonandthestageofestruswasidentifiedusingultrasonography.Telemetrydatafrom bullandcows,collectedover48-dayloggerdeployments,werelogtransformedand ana-lyzedbyANOVA.Boththenumberanddurationofbull-cowaffiliationsweresignificantly (P<0.001)greaterinestrouscowscomparedtoanestruscows.Theseresultssupportthe developmentoftheUHFtechnologyasahands-offandnoninvasivemeansofgathering socio-sexualinformationonbothwildlifeandlivestockforreproductivemanagement.
CrownCopyright©2014PublishedbyElsevierB.V.Thisisanopenaccessarticleunder theCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/3.0/).
1. Introduction
Reproductiveefficiencyisanimportantdeterminantof
profitabilityinboththedairyandbeef industries(Royal
etal.,2000;Burnsetal.,2010).Moreover,thelackofbasic
∗ Correspondingauthor.Tel.:+61749232063.
E-mailaddresses:[email protected],Christopher.O’[email protected] (C.J.O’Neill),[email protected](G.J.Bishop-Hurley), [email protected](P.J.Williams),[email protected] (D.J.Reid),[email protected](D.L.Swain).
reproductivedataisamajorimpedimenttothesuccessful
implementationofconservationprogramsforendangered
mammalian species (Andrabi and Maxwell, 2007). The
challenge in rangeland cattle breeding operations is to
assessreproductivecapacityoncattlerarelyhandledand
inremotelocations.Incontrasttoextensivecattlesystems,
theintensivecattle industry possesses a range of
tech-niquestomonitoracow’sreproductivestatus.Inintensive
systems, cow-mountingbehavior during sexually active
group(SAG)formation,increasedactivity,assaysofmilk
progesterone,vasectomizedbullsandeitherelectronicor
http://dx.doi.org/10.1016/j.anireprosci.2014.09.017
0378-4320/CrownCopyright©2014PublishedbyElsevierB.V.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/ licenses/by-nc-nd/3.0/).
non-electronicestrousdetectionaidshavebeenusedto
detectestrousin cattle (Diskin and Sreenan, 2000;Firk
etal.,2002).However,despitetheopportunityto
moni-torcowsmoreintensivelyinsuchsystemstheincidenceof
silentovulationissignificant(Ranasingheetal.,2010)and
undetectedestrusisincreasing(Dobsonetal.,2008;Walsh
etal.,2011).
The issue of poor estrous detection is compounded
bythelowheritabilityoftraitscurrentlyusedto
geneti-callyimprovefertility(Cammacketal.,2009;Burnsetal.,
2010),buttherelativelyhighheritabilityofendocrine
fer-tility traitssuggests theirinclusion ina selection index
toimprovefertility(Royaletal.,2002).Hence,the
accu-rateidentificationofthereproductivephenotypeincattle
willbenefitbothgeneticandARTstrategies thataimto
improvereproductive efficiency(Cushmanet al.,2007).
Genomicstudiesofestrousexpressionindairycows(Boer
et al., 2010;Homer et al., 2013) have identified alleles
associatedwithincreasedestrousactivitywhichsuggests
notonlypotentialgeneticmarkerstoimprove
reproduc-tion of cattle, but also expanding studies of thenexus
betweenincreasingmilkproduction withtraits
indicat-inga decline in both health and fertility of dairy cows
(Rauw etal.,1998;Lucy, 2001).Giventhebetweenand
withinbreedvariationinestrousintensityandduration,
a quantitativegeneticand genomic investigationof the
twotraitsiswarranted.Bosindicuscattleevolvedin
trop-ical regions and compared to B. taurus, have relatively
lowerreproductiverates (Frischet al.,1987), inherently
less estrousexpression (Orihuela, 2000)and lowerbull
libido(Galinaet al., 2007).Nevertheless, breedersof B.
taurusbeefcattlemustalsoensurethatselectionfor
pro-ductiontraits(e.g.steergrowthratesandcarcassandmeat
quality)do not compromise eitherbehavioral estrusor
pregnancytraitsofbeefcows(McClureetal.,2010).Estrous
detection is of particular concern in the dairy industry
wherethedecliningreproductiverates have been
asso-ciated with a reduction in estrous expression (Dobson
etal.,2008; vanEerdenburg,2008; Walshetal., 2011);
namely, estrous intensity and duration (Cutullic et al.,
2009).
However,intermsofmale-femalereproductive
inter-actions in cattle, we have at one extreme competition
betweenbullsinamulti-sirerangeland beefproduction
systemandtotheother,artificialinsemination(AI)
pro-gramsinanintensivedairyproductionsystem.Thelatter
systemdictatesthatfemaleshavenocontactwithmales
andthereforenoopportunitiesforanypositive
biostim-ulationaffectfrommales(Zaleskyetal.,1984;Fioletal.,
2010).
Inproductionsystemsthatincludebullsrunningwith
cows, a mating event will involve a close encounter
between a bull and a cow. Biotelemetry data from
UHF transceiver devices (contact or proximity loggers)
recording the frequency and duration of close
encoun-tersbetweencowsandcalveshavebeenusedtoidentify
maternalassociationinfreerangingbeefcattle(Swainand
Bishop-Hurley,2007).For cattlebreeding programs the
identificationof closeencounters duringestrous events
couldbeusedtodeterminethereproductiveperformance
ofindividualanimals.
ThispaperexploreswhetherUHFtelemetrythatrecord
thefrequencyanddurationofclose(<5m)bull-cow
inter-actions during a 7-week breeding period, can be used
toidentifyestrus.Theproximityloggerdataweretested
against data collected from both ovarian and uterine
ultrasonographyusingcattleinanintensivetropicalbeef
grazing system. UHFtelemetryas a meansto elucidate
issuesassociatedwithmale–femalereproductivebehavior
isdiscussed.
2. Materialsandmethods
2.1. Studysiteandanimals
Thestudywasconductedduringthe2005–2006
breed-ingseasonatBelmontResearchStation,a3260haproperty
locatedinnortheasternAustralia(150◦13E,23◦8S).
Forty-five,4-to12-yearoldBelmontRed(interbredAfricander,
BrahmanandHereford-Shorthorn–B.taurusxB.indicus)
lactatingcowswiththeircalf-at-footwereallocatedtoone
ofthreeadjacent7hapaddockssoineachpaddockthere
wasasimilarcowagestructure.A5-yearoldBelmontRed
bullwasplacedineach paddockforthedurationofthe
breedingseason:12December2005–27January2006.The
breedingseasonontheBelmontResearchStationwould
routinelycommenceonoraboutthisdayinDecember,
con-tinuefor12weekswithacorrespondingpeakinthecalving
seasonlateOctobertoearlyNovember.Howeverthebulls
inthepresentstudyjoinedtheirmatingfamiliesonthis
date,butwereremovedafter47days,coincidingwiththe
endofthestudy.Onceallocatedtotheirpaddockthebulls
andcowsremainedinthatpaddockforthedurationofthe
breedingseason.Itwasassumedthateachbullresponded
normallytocowestroussignalsasthebullshad
success-fullyperformedinpreviousbreedingseasons.Theforage
wasirrigatedRhodesgrass(Chlorisgayana)andeach
pad-dockcontainedshadetrees.Thecattlehadadlibitumaccess
towatersuppliedviaawatertrough.Ethicsapprovalwas
obtainedfromtheRockhamptonanimalethicscommittee:
RH209/05.
2.2. Deploymentofproximityloggers
Proximityloggers(modelE2C181CSirtrackLtd.,
Have-lock North, New Zealand) recorded contact between
animals by the transmission/reception of UHF signals
(Prange et al., 2006). Proximity loggers simultaneously
transmitsignalsto,andreceivesignalsfrom,other
prox-imityloggers withinapredeterminedread-range,which
wassettoamaximumof5minthisexperiment.Theexact
distance betweenthose contactslogged will vary since
radiowavescanbereflectedorblockedbyobjectssuch
asothercows. However,aninteractionthatis recorded
betweentwoindividualsthatarewithin5mrepresentsa
closeencounter.Amoredetailedexplanationofthe
oper-ationoftheproximityloggersusedinthisexperimentcan
befoundinSwainandBishop-Hurley(2007).
AswithPrangeetal.(2006)wealsousedaprototype
logger and wereconcernedwith relativelylimited data
storagecapacity(memorycapacityof16,384records)of
activitysuchasSAGformation.Hence,proximityloggers
weredeployedoncows,calvesandbullsfor1week,for4
deployments,witha1-weekgapbetween.The1-weekgap
allowedthecollarstoberemovedandthedatadownloaded
ensuringdatawerenotlostduetothedevicebeingatfull
datacapacity.The1-weekdelaybeforethenext
deploy-ment also allowed routinemaintenance of the devices,
namelyrepairofabatterywirepronetobreakingcausing
alossofdata.Bothtechnicalissueshavebeenaddressedin
laterversionsofthelogger.
Onday1ofadeployment,thecowsandcalveswere
broughtintotheyardsandrandomlyallocatedto
proxim-ityloggers.Theproximityloggercollarswerefittedtothe
neckoftheanimal andthegroupof15cowswiththeir
calveswastakentotheirassigned paddock.Therewere
nocasesofanimalsdisplayingdiscomforttothecollar.On
day8ofthedeploymenttheanimalswerebroughtback
totheyardsforcollarremovalandthenreturnedtotheir
assignedpaddock.Thetelemetrydataweredownloaded
fromtheproximityloggersandtheproximityloggersreset
forthenextdeployment.Eightdaysaftercollarremoval
theanimalsreturnedtotheyardsfortherandom
reallo-cationoftheproximityloggersforthenextdeployment.
Thedatesof thedeploymentswere:(1)9December–16
December2005;(2)23December–30December2005;(3)
6January–13January2006and(4)20January–27January
2006.Bullswerefittedwithaproximityloggerandtaken
totheirpaddockduringthefirstdeploymentofproximity
loggersandbecamepartofthereallocationofproximity
loggersatsubsequentdeployments.
2.3. Ultrasoundscanning
Estrus was assessed in cows by ovarian ultrasound
usingaRealTimeUltrasound(HondaHS2000V,HLV-457M
probeTokyo,Japan)withavariable-frequencytransducer
setat10MHz.Scanswereconductedbyanexperienced
ultrasonographeratthestartandendofeachweekly
prox-imityloggerdeployment.Morefrequentscanningwould
have betteralignedestrousstatuswiththe
correspond-ingtelemetrydata(i.e.lessdilutionofthetelemetrydata
for analysis), but for rangeland cows not used to
regu-larmusteringthiswouldhaveincreaseddisruptiontothe
established social, grazing, suckling and SAG formation
withinthematingfamily,andmaycontributetoincreased
levels of stress, which can detrimental to reproductive
behavior asshown byvon Borellet al.(2007).At
scan-ning,eachovarywasviewedbyultrasoundimagingand
thepresenceofacorpusluteum(CL)orthediameter(mm)
ofthelargestfolliclewasrecorded.ThepresenceofaCL
andthechangesinfollicularmeasurementsbetweenscans
wereusedtoestimatetimeofestrus.Thesameultrasound
devicewasusedtodeterminethepregnancystatus(either
pregnantornon-pregnant)ofthecowandestimatetheage
anddateofconceptionbymeasuringcrowntorumplength
ofthefetus.
2.4. Ovarianandconceptionscanclass
The ovarian ultrasonography data for each cow for
theweeklyproximityloggerdeployment,incombination
withauterinescan(10February2006),wereusedbythe
ultrasonographer to identify a cow’s estrous and
preg-nancy status for the week the collars were deployed
namely:(1)non-pregnantand anestrus/anovulatory;(2)
pregnant–diestruswithpregnancyconfirmedwithuterine
scan;(3)estrus–follicular growth,maturation,ovulation
and conception confirmed with uterine scan and (4)
estrus–folliculargrowth,maturation,ovulationbutno
con-ception.
2.5. Telemetrydataprocessing
Ofthe192proximityloggerdeploymentsonthecows
andbulls,therewere23occasionsthecowproximity
log-gersfailedtorecorddataforaperiodoftime.However,
bull-cowinteractionswererecordedonboththebulland
thecowproximityloggersandreciprocaldatafromtwo
proximityloggerscanbeusedtodetermineanassociation,
evenwhenoneoftheloggersfailstorecorddata(Swain
andBishop-Hurley,2007).Thecollarfittedtooneofthree
bulls(BullB)waslostatthestartoftheseconddeployment;
thus,therewerenotelemetrydatafromthisbullduringthis
deployment(treatedasmissingvalues).Thedeployment
ofproximityloggerscoincidedwiththeovarianscanning
scheduleofthecows(supplementaryTableS1).
2.6. Statisticalanalyses
Daily contact frequency and contact duration were
calculated for each deployment and assigned toone of
thefourweeklyovarian/conceptionclasses, namely:(1)
non-pregnantandanestrus/anovulatory;(2)pregnant;(3)
estruswithconceptionand(4)estruswithoutconception.
Aswithapreviousanalysisoftelemetryrecords(Swainand
Bishop-Hurley,2007),thedatawerelogtransformedprior
toanalysisduetolargedifferencesinvariance.Thedata
wereanalyzedbyANOVAusingGenStatRelease8.1(Payne
etal.,2005)andovarian-conceptionclasswereregarded
asfixedeffects. Asourfocus wastodocumentthe
con-tactdatageneratedfromUHFtelemetryduringanestrous
eventinastandardbreedingseason,thethreebullswere
notrotatedbetweenpaddocks.Again,tominimize
disrup-tiontoestrousevents,thematingfamilyremainedintheir
assignedareaforgrazingforthedurationofthebreeding
season.Hence,wemakenostatisticalinferenceasto
differ-encesinanimalreproductiveefficiency,libidoandpaddock
affects.
3. Results
Itwasassumedthattheultrasoundwasabletoindicate
theeventofestrusandofconceptionforallocationofcows
totherespectiveclasses.Thedatashownin
Supplemen-taryTableS1isofacowthatconceivedon15December
2005duringdeployment1andtheconceptioncoincided
with343bullcontactswithatotal duration ofcontacts
of11,734sonthatday.Thisrepresentsa17-foldincrease
incontactsanda43-foldincreaseindurationofcontacts
overthemeannumberanddurationofcow-bullcontacts
on a daily basis during deployment 2 (19.8±6.06 and
Table1
LeastsquaresmeansLog10(±SEm)ofnumberanddurationofhourlybull-cowcontactsforeachovarian/conceptionclasswithineachdeployment.
Ovarian/conceptionscanclass Numberofcontactsperh Durationofcontactsperh(s)
Anestrus/anovulatory–non-pregnant −0.21±0.047a(0.62)A 1.11±0.080a(12.8)
Diestrus–pregnant −0.25±0.063a(0.56) 1.03±0.107a(10.8) Estrus–conception 0.16±0.066b(1.45) 1.69±0.113b(49.1) Estrus–butnoconception 0.18±0.083b(1.51) 1.57±0.141b(37.3) abWithinacolumn,valueswithnocommonsuperscriptaresignificantlydifferent(P<0.001)
ABack-transformedvalueinparentheses.
Table2
Numberofcowsinestrusandthetotalnumberofcontactsanddurationofcontactsforeachdeploymentofproximityloggers.
Deploymentof proximityloggers
Totalnumberofcows inestrus
Overallnumberofcontacts (percowperday)
Overalldurationofcontacts(h) (percowperday)
1 18(4)A 24.9 0.22
2 18(10) 29.4 0.33
3 7(8) 13.1 0.14
4 1(0) 20.6 0.16
Note:thebullsweretakentotheirassignedpaddockmidwaythroughdeployment1.
ANumberofcowsdeterminedtohaveconceivedviaultrasonographyofthefetusshowninparentheses.
Basedontheovarian/uterineultrasoundeachcowfor
eachdeploymentwasallocatedtotheappropriate
ovar-ian/conceptionclass.Table1showsforeachovarianand
conceptionclassthelog10transformedvaluesforthe
num-berofbull-cowcontactsperhourandthecorresponding
durationofthosecontactsperdeployment.Thebull-cow
contacts,bothnumberanddurationofcontacts,were
sig-nificantly(P<0.001)higherduringdeploymentsinwhich
estrusoccurred(classes3and4)thanindeploymentsin
whichtherewerenoestrousevents(classes1and2).The
contactdataclearlyseparatedtheestrousfromanestrous
cows,buttherewerenosignificant(P>0.10)differences
withintheestrousfromanestrousclasses(Table1).The
increaseincontactactivityasanindicationofestruswas
alsoassociatedwithadisproportionalincreaseinthe
dura-tionofcontacts.Therewere2–3timesmorecontactsfor
estrouscowsthannon-estrouscows,withcontactsbeing
3–5timeslonger(Table1).
Theoverallaccumulationofconceptionsofthesecows
over the 7-week exposureto bullswas relatively high,
with 39 cows or 86.7% of cows conceiving during the
season.Ultrasonographyestablishedthatestrusand
con-ceptiondidnotoccuruniformlythroughoutthebreeding
season,butpredominately earlyinthebreedingseason;
indeployments1,2and3(Table2).Thepeakincontact
activitycoincidedwiththepeakinconceptions:29.4
con-tactsandanaveragedurationof0.33h(20min)percow
perdaywith10conceptionsduringdeployment2.Inthe
final deployment (deployment4)there was onlya
sin-gleestrouseventdetectedandzeroconceptions,butwith
over20bullcontactsof0.16h(10min)percowperday
(Table2).
Telemetry dataalso revealed individualanimal
vari-ationand probabledateof conception.Ultrasonography
of two cows (Cows 99–840 and 00–019) determined
theycycled andconceived duringdeployment2 (23–30
December2005).Thetelemetrydatasuggestthepeakin
estrusforCow99-840occurredon26December(390
con-tacts withaccumulatedduration of 11.4h, over 25 and
26 December2005), whilst for Cow00-019 estrusonly
occupied1day(317contactswithanaccumulatedduration
of5.4h,over25and26December2005)(Fig.1).
Althoughthethreematingbullsrecordedrelativelyhigh
accumulativeproportionpregnant–93.3,80.0and86.7%
forBullsA,BandCrespectively,therewasvariationinthe
durationofcontactofindividualbullswithcowsduringthe
estrousperiod.Table3showsthenumberofbull-cow
con-tactsforatleastonecloseproximitycontact(<5m)ofeach
cowoneachdayofthedeploymentoverthe4deployments.
Itwasonlyduringthedeploymentwiththelargestnumber
ofconceptions(deployment2),thebullsmadecontactwith
everycowintheirgroupeverydayofthedeployment(data
notshown).However,notallbullsmaintainedthisregime
throughoutthebreedingseason.Ononlyfiveoccasionsdid
Bull Anothavecontactwitheverycowinhisgroupon
everydayofthedeployment,whereas,thisoccurredon23,
oralmost10%oftheoccasionsforBullC(Table3).
4. Discussion
Theproximityloggeriscapableofdocumenting
animal-to-animal interactions associated with both wildlife
(Prange et al., 2006) and livestock (Swain and Bishop-Hurley,2007).We presentevidencethatthetechnology
was also able to record a change in contact behavior
betweenabulland acowsignifyingtheonsetofestrus
Table3
Thenumberofdaysinwhichthebullmadeatleastonecontactwithevery cowinthebreedinggroup(asrecordedbytheproximitylogger):potential daysforthebull-cowcontactandnumberofoccasionsinwhichacowwas missed.
Bull Possibledaysfora
bull-cowcontacttobe recorded
Numberofoccasions therewasnoclose contact
A 279 5(1.8%)A
B 204 14(6.9%)
C 242 23(9.5%)
ANumberofdaystherewasnobull-cowcontactasapercentageofthe totalpossibledaysshowninparentheses.
(A)
(B)
0 50 100 150 200 250 300 24th 25th 26th 27th 28th 29th 24th 25th 26th 27th 28th 29th Number of Contacts Cow 99-840 Cow 00-019Number of contacts with Bull A
during deployment 2
(24-29 December 2005) for cows 99-840 and 00-019
0 5000 10000 15000 20000 25000 30000 35000 24th 25th 26th 27th 28th 29th 24th 25th 26th 27th 28th 29th Duration of Contacts (s) Cow 99-840 Cow 00-019
Duration of contacts (s) with Bull A
during deployment 2
(24-29 December 2005) for cows 99-840 and 00-019
Fig.1.Dailycontacts(A)anddurationofcontacts(B)oftwocows(identities:99-840and00-019)withBullAwherethecowsweredeterminedby ultrasonographytobeinestrusandhaveconceivedduringdeployment2(23–30December2005).
inthecow.Estimatesofhowoften(numberofcontacts)
and for how long (duration of contacts) a bull comes
in close proximity (<5m) with a cow have been
pre-sented as reproductive behavior. From these contacts,
andinconjunctionwithovarianultrasonography,weare
drawing inferences as to the value of the technology
in identifyinga female’sreproductivestatus (i.e.estrus,
anestrus);asanadditionalaidtothedetectionofestrus
andrecordingmaleandfemalesexualactivity.UsingUHF
proximity loggers to record SAG activity, McNeill et al.
(2010)withathresholdalgorithmfromdairycowcontacts, and O’Neillet al.(2010a)withaPerl programthat
pre-dictedfutureestrouseventsfrompreviousestrousevents
inbeefheifers,concludedthetechnologywascapableof
detectingestrus.Fromourstudyofbull–cowaffiliations
we believe thescope for the technology is wider than
simpleestrousdetectionandhasadditionalimplications
forclearlyidentifyingreproductivedysfunction(repeated
estruswithoutconception),maleand femalelibido,
rel-ative importance of sociality and of biostimulation in
reproductiveinvestment,andthequantificationofestrous
intensityanddurationforbothgeneticandgenomic
stud-ies.
Thehighlysignificant(P<0.001)elevationinboth
num-beranddurationofbull-cowcontactsassociatedwiththe
changeinfollicularmeasurementsofestrouscows
(ovar-ian/conceptionclasses3and4)comparedwithnon-estrous
cows(ovarian/conceptionclasses1and2)(Table1),
sug-geststhetechnologyeffectivelyidentified differencesin
contactactivitybetweenestrusandanestrus.Theproblem
ofdetectionofestrusinbothB.indicusandhighmilk
pro-ducingB.taurusdairybreeds(GalinaandOrihuela,2007;
Roelofsetal.,2010)couldbeaddressedwithcontinued
developmentofUHFtelemetrytechnologyaloneorin
com-binationwithothertechnologiessuchasapedometer(Firk
etal.,2002)orawirelessaccelerometerand
magnetome-tersystemtosimultaneouslydetectestrousandsickness
behavior(Pastelletal.,2009;Swainetal.,2011).
Other telemetry systems are used commercially to
detectestrusactivity(DiskinandSreenan,2000),butthe
essenceoftheUHFproximityloggeristhesocialcontextof
estrousactivityandtheabilitytoseparatethecomponents
ofthatactivity–eachanimal’srelativecontributiontothe
estrousevent.Ithaslongbeenrecognizedthatthereisa
socialdimensiontoestrousbehavior(Hurniketal.,1975;
neglectedin bothbeef (Fordyce etal.,2002;Galinaand Orihuela,2007)anddairycattle(Ungerfeld,2007;Walsh
et al., 2011).Moreover, a wireless system combining a
device(e.g.anaccelerometer)torecordmounting
activ-itywitha UHFtelemetry devicetorecord bothestrous
intensityanddurationwouldprovideclaritytotheissue
ofenergeticcostand/ornegativegeneticcorrelations
asso-ciatedwith thereproductive cycle phenotype(Kotiaho,
2001;Blancetal.,2006).Giventhatthereisnoclearcause
forthediminishedexpressionofestrusbehaviorindairy
cattle(vanEerdenburg,2008;CornwallisandUller,2009)
webelievetheutilizationofUHFbiotelemetrytostudythe
socialcontextofthereproductionofallcattleiswarranted.
Moreover,suchatechnologywouldestablishrelationships
withinthecomponentsofestrousactivity(e.g.intensity
andduration ofsexualcontacts). Thetechnologywould
alsoenabletheinvestigationofthenexusbetween
repro-ductive investmentand measures of productivitywhen
nutritionislimited(Blancetal.,2006)aswithcowsinharsh
environmentsorwhenthefeedinglevelofthecowfalls
shortofitsproductionpotential.Continueddevelopment
ofUHFtechnology,incombinationwithotherbiotelemetry
technologies,togeneratesocial,reproductiveandsickness
behaviorinformationwillenableanimalbreederstoadopt
aholisticapproachtotheiranimalhusbandry.
Theoverallaccumulativeproportionpregnantof86.7%
forlactatingcowswitha7-weekbullexposurewasan
indi-cationoftheherd’srelativelyhighfertilityforthisregion
ofnorthernAustralia(Burnsetal.,2010).Thattheestrous
eventsand conceptions occurred early in the breeding
seasonratherthanthroughouttheseason(Table2)
sup-portsevidence(BurrisandPriode,1958;Frischetal.,1987;
Cushmanetal.,2013)ofthemorereproductiveefficient
femalecalvingearlyratherthanlaterinthecalvingseason.
Both the scanning and telemetry data also
demon-stratedallthreebullswerereproductivelysoundforthis
breedingseasonandtheblameforanynon-pregnantresult
couldbedirectedatthecow.Indeed,thebullsmaintained
apresence withthecows throughoutthebreeding
sea-son.Thenumbersofcontactspercowperdayforthefirst
andlastdeploymentswere24.9and20.6respectively,yet
thecorrespondingnumbersofcowsinestruswere18and
1(Table3).Thebullsdidnotcomeinclosecontactwith
allofthecowseachday,soitispossiblethatvisualand
olfactorysignalsallowedthemtodetectestrousfroma
dis-tance.However,thecontactactivityoverallsuggeststhe
bullsmaintainedasexualvigilanceofthecowsforsigns
of estrusand again demonstrated optimal reproductive
behavior(Orihuela,2000).
Cushmanetal.(2007)andCornwallisandUller(2009)
highlightthelackofstudiesquantifyingtherelationships
betweensexualtraits.Thepresentstudywasnotdesigned
toidentifystatisticaldifferencesinlibido,butto
demon-stratethe potentialrole of UHFtelemetry in the study
ofsexualtraitsandimportantly,theinteractionbetween
sexualandsocialtraitsinmammalianspecies.Theclose
proximitycontactsbetweenbullsandcowsnotedinthis
studymaynotnecessarilybeextrapolatedtoother
produc-tionsystems;forexample,tropicalrangelandsormultiple
sirebreedingprogramsaswiththeFordyceetal.(2002)
work. The data showing Bull A failed to make a close
contactwitheverycowoneverydayononly1.8%of
occa-sionscomparedwith9.5%ofoccasionsforBullC(Table3),
isoflittleconsequenceforaproductionsystemwherethe
paddocksallocatedtothebreedingprogramwereonly7ha
inarea.Theauthorsmakenoattempttodrawconclusions
astodifferencesinlibidobetweenthethreemales.
Never-theless,suchdifferencesinbullcontactactivityshownin
Table3mayhaveconsequencesifthepaddocksassignedto
thebreedingprogramaresubstantiallylargerandcontain
competingbulls.Largerpaddocksaremorerepresentative
of rangeland production environmentsand factors such
asthebull’swalkingability,olfactorysensors,
aggressive-ness,socialityandresponsetofemalemountingbehavior
becomemoreprominentforbullperformance(Orihuela,
2000;Fordyceetal.,2002).
Thedatafromthisstudysuggestthelengthofestrous
of Cow 99-840 was longer than Cow 00-019 (Fig. 1).
Giventwoothercowsfromthispaddockalsoconceived
duringthisperiod(23–30December2005),amore
con-clusivequantificationoflengthofestruscouldbebased
onthecontact information ofother cowsin thegroup:
thosecowsthatformaSAGandespeciallythosethatare
alsoinestrus(PhillipsandSchofield,1990).Anadditional
analysisoftheinteractionsbetweencowsmightbeused
to revealimportant female–female networks associated
withfemalesociality(Landaeta-Hernándezet al.,2002).
Ungerfeld(2007)highlightedthelackofinformationon
female-to-female relationship and the need to conduct
researchasameansofimprovingthereproductive
man-agementoffemalelivestock.WhileAcevedoetal.(2007)
foundthemostlikelycowtobeinvolvedinSAGformation
wasacowthatwasinestrus,notallcowsrespondsexually
tothegroupareinestrus(PhillipsandSchofield,1990).Is
itsocialityandconformingtogroup-typicalbehaviorthat
motivatesanon-estrousfemaletobeinvolvedinsexual
activity,oristhisanindicationofhighgeneticreproductive
potential?Proximityloggersmaybeausefultoolfor
quan-tifyingwhichcowsparticipateinSAGsandthedurationof
theestrousevent.However,utilizingdatafromallcow-cow
contactsmaynotbeappropriateforallproductionsystems.
In intensivedairysystems a‘teaser’or vasectomized
bullcouldbeincorporatedintoAIprograms(Diskinand
Sreenan,2000)andtelemetryrecordsfromonlybull–cow
contactsmaybesufficientforestrousdetectioninthis
sys-tem.Indeed,bullsmayuseolfactory/gustatorystimulito
predicttheonsetofestrusseveraldaysbeforetheestrous
event(Frenchetal.,1989).However,therewouldneedto
bescreeningofsuchbullsforlibidoandtemperamentprior
totheiruseandappropriatesupervisiononceintheherd.
Whilsttheneedforsexualstimulationpriortoservicehas
beendocumentedinthebull(PerryandLong,1992),the
roleofbiostimulationandtheimpactofthebull’sauditory,
visualandolfactorystimulistillneedstobeclearlydefined
forthecow(TauckandBerardinelli,2007;Ungerfeld,2007).
ThepositiveresultsfromNorton’s(2008)Canterburyteaser
bullstudyinvolving7farmsand1528dairycows,andthe
Rekwotetal.(2001)reviewofpheromonesand
biostimu-lationsuggestsapotentialroleforutilizingthe‘bulleffect’
inreproductivemanagementofcows inartificial
breed-ing systems.Aswiththeevolutionaryconsequences for
(Claussetal.,2010),theremayalsobeevolutionary
con-sequencesfortheendocrinologyandreproductivesignals
ofdairyfemalesthathavegonemanygenerationsdevoid
ofmalecontactandthereforelackofstimulationof
male-orientatedreceptorsassociatedwithestrousbehavior.
Justaslimitationswiththesatellite-basedglobal
posi-tioningsystems(GPS)technologyhavehadtobeaddressed
(Hebblewhiteand Haydon,2010; Swainetal.,2011),so
towith theemerging UHFtechnology. Ideally, theUHF
biotelemetry should generate data in real-time and at
intervals small enoughto closethe gapbetweensocial
contacts and the physiological process related to those
contacts (Krause et al., 2013). We conclude from the
present study that UHF proximity loggers are a viable
option for theaccuratedetection of estrusand there is
scopetousethetechnologytoexploresocio-sexual
sig-nals associated with sexualphysiology. However, given
thelargenumberoftelemetryrecordsgenerated(1.5
mil-lionrecordsinthecurrentstudy),itisessentialthedata
processing is automated to enable animal breeders to
usetheinformation toimprove reproductionefficiency.
Thisstudyrequiredtheproximityloggerstoberemoved
after a week of data collection toallow the recordsto
bedownloaded.If theproximity loggerdeviceswereto
beusedoncommercialcattleorrangelandherbivoresan
automated wireless data downloadcapability would be
required.
For cattle producers, the opportunitythen exists for
the data from a particular herd to be linked to other
herds in a central database for the genetic evaluation
of estrous intensity and duration. The quantification of
an estrous event has ramifications for improved
selec-tionindicesforbothgenetic(Weigel,2004)andgenomic
(Homer et al., 2013) options to improve poor
repro-ductive ratesincattleandidentificationofreproductive
dysfunction. Algorithms of UHF telemetry data,
com-bining male–female and female–female contacts, have
thepotentialtonot onlyprecisely identifyestrous
tim-ing, but also quantify the intensity and duration of
that estrous event. Such data enables the collection
of basic ART data in wildlife species and addressing
suboptimal fertility in cattle in a range of production
environments.Giventhecow’sbehavioraland
physiolog-icalresponsetotheproductionenvironment iscomplex
(Orihuela,2000;Ungerfeld,2007;vanEerdenburg,2008),
data from various telemetry systems (Handcock et al.,
2009) have the potential to provide additional
infor-mation on thereproductive axisin terms of important
animal-social-genetic-environment-management
interac-tions(Cornwallis and Uller, 2009;O’Neill et al., 2010b;
Walshetal.,2011).
Conflictsofinterest
Theauthorsdeclarethattherearenoconflictsof
inter-est.
Acknowledgements
ThisworkwasfundedthroughCSIROFoodFutures
Flag-ship. The authors would like to thank the staff at the
BelmontResearchStationforassistingintheconductofthe
experiment.UsefulcommentsonthemanuscriptfromDon
Menzies(CQUniversity)andthetwoanonymousjournal
reviewerswereappreciated.
AppendixA. Supplementarydata
Supplementarydataassociatedwiththisarticlecanbe
found,intheonlineversion,athttp://dx.doi.org/10.1016/
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