October1999]
ShortCommunications
1141
pendence.Annalsof Mathematicsand Statistics RONALD, K., M. E. FOSTER,AND M. I. DYER. 1968.
15:546-557.
Physicalpropertiesof the blood in the RedHOGSTAD,
O. 1986.Socialrank and anti-predatorbewinged Blackbird(Agelaiusphoeniceus).
Canadihavior of Willow Tits, Parusmontanus,in winter
an Journalof Zoology46:157-164.
flocks. Ibis 130:45-56.
$A$ INSTITUTE.
1994.SASproceduresguide,version
KETTERSON,
E.D. 1979.Aggressivebehaviorin win6, 3rd ed. SASInstitute,Inc., Cary,North CaroteringDark-eyedJuncos:
Determinantsof domlina.
inanceand theirpossiblerelationto geographic SCHNEIDER,
K. J. 1984. Dominance,predation,and
•,ariation
in sex ratio.
Wilson
Bulletin
91:371-
optimal foraging in White-throatedSparrow
flocks.Ecology65:1820-1827.
KOIVULA, K., K. LAHTI, $. RYTK•NEN, AND M. ORELL.
$TURKIE,
P. D. 1986.Bodyfluids:Blood.Pages1021994.Do subordinates
exposethemselves
to pre129 in Avian physiology,4th ed. (P.D. Sturkie,
dation?Field experimentson feedingsiteselecEd.). Springer-Verlag,New York.
tionby WillowTits.Journalof AvianBiology25:
WILSON,
G. g., ANDL. P.WILSON.1978.Hematology,
178-183.
weightandconditionof captiveRedGrouse(LaPIPER,
W. H. 1995.Socialdominance
in youngWhitegopus lagopusscoticus)infected with cecal
throatedSparrows:Effectsof early socialexpethreadworm(Trichostrongylus
tenois
). Research
rienceand the unstableperiod. Auk 112:878383.
in VeterinaryScience25:331-336.
889.
PIPER, W. H. 1997. Social dominance in birds. Cur-
rentOrnithology14:125-187.
PRAVOSUDOV,V. V., AND t. C. GRUBB,JR. 1997. En-
ergy managementin passerinebirds duringthe
nonbreedingseason.A review. Current Orni-
ZANETTE,L., AND L. M. RATCLIFFE.1994. Social rank
influences conspicuousbehavior of Blackcapped Chickadees,Parusatricapillus.
Animal
Behaviour
48:119-127.
thology14:189-234.
goItt,
I., J. BROSTOFF,AND D. MALE. 1993. Immu-
nology,3rd ed. Mosby,London.
Received
2 April 1998,accepted
27 January1999.
AssociateEditor: L. J. Petit
TheAuk 116(4):1141-1144,1999
Male House SparrowsBehave as if a Fertilization Window Exists
MISTY D. HANKINSON •
Department
ofZoology,
Universityof Oklahoma,
Norman,Oklahoma
73019,USA
Spermcompetitioncan occurwhen a femalecopulateswith more than one male during the period
whenher eggscanbe fertilized(Parker1970).In monogamous
species,
wherethemaletypicallycontributes valuable parental care, intrasexual selection
shouldactonmalesto producetraitsthatminimize
spermcompetition,thus helpingensurethat the investingmale'sown spermfertilizesmostor all of his
energyexpenditureand/or time (opportunitycost),
somalescanbe expectedto confinethesebehaviors
to timeswhentheywouldbe mostbeneficial,if such
mate'seggs(Kempenaerset al. 1995).In birds, two of
secondovum (Bakst and Bird 1987, Birkhead and
times can be detected.
As layingcommences,
the presence
of the firstdevelopingovumin the oviductapparentlydecreases
the interval during which additionalspermcan be
introducedand have any chanceof fertilizingthe
the main waysa male avoidscuckoldryare mate Moller 1993,Bakstet al. 1994).Thismay reducethe
guarding and frequent copulation(Birkhead and hypothetical
"fertilizationwindow"("insemination
Moller 1992, Briskie 1992). However, both of these
behaviorsmaybe very costlyfor malesin termsof
window" of Chenget al. 1983)to aslittle as10 to 60
min afterthe layingof the precedingegg,while the
next ovum is in the infundibulum (Bobret al. 1964).
Thereafter,the secondegg, fertilized or not, begins
1Addresscorrespondence
to DouglasW. Mock, accumulating
layersof albumenandmembranes
that
Departmentof Zoology,Universityof Oklahoma, trap spermand actcollectivelyasa barrier to fertilNorman, Oklahoma 73019, USA. E-mail: dmock@ ization of a third ovum (Bakstet al. 1994).Furtherou.edu
more,the contractions
that propeleachegg through
1142
ShortCommunications
[Auk,Vol. 116
theoviductopposethemovements
of sperm,andthe
Oklahoma(35ø20'N,97ø40'W).Numberedplywood
fluid of the uterine mucosa also acts as a barrier to
nest boxeswere mounted on posts, fences,or old
the infundibulumwhere fertilization takes place buildings,with considerable
variationin thedistances
(Bakst et al. 1994). As evidence of this limitation, betweennearestneighbors.A sampleof nearestChenget al. (1983)reportedthat femaleMallards neighbordistances
takenfromthispopulation
in 1996
(Anasplatyrhynchos)
inseminatedafter the fertiliza- averaged28.6 _+SD of 16.4m (R. R. Whitekilleruntion window was estimatedto be closedproduced
only one fertileeggout of 179that were laid.
The idea that a fertilization window exists has be-
publ. data).Formy study,boxesneardensetreeswere
avoided to facilitate observationof mate-guarding
movementsby males.From mid-May to early July
comeincreasinglycontroversialin recentyears.Ad-
1996,activitiesaroundthe boxesof 16 pairs (eight
kins-Regan
(1995)showedthattimeof dayofmating duringlayingand eightduringincubation)
wereobdoes not affect the fertilization
success of the next
served from a car at a distance of 20 to 25 m. Ten of
eggin Japanese
Quail (Coturnixjaponica),
and obser- the16pairshaduniquecombinations
of colorbands.
vationsof copulationbehaviorhave provided eviFemale House Sparrowstypically entered their
dence both consistent with and counter to the "ferboxesto lay eggsbetween0615 and 0645 EST.On a
tilization-window" hypothesis (Birkhead et al. typical morning, I checkedthat day's focal nest at
1996).Forexample,in diurnallymatingbirdssuchas about 0550 to verify that a new egg had not apLesserKestrels(Falconaumanni;Negro et al. 1992) peared.The meannumberof eggsin the nestwhen
and Smith's Longspurs(Calcariuspictus;Briskie I arrivedwas2.09 _+0.42;oneor two eggsweresub1992),onepeakin copulationandmate-guardingac- sequentlyaddedto all focalnests.When the female
tivity occursin the morning,aswouldbe expected firstenteredthebox,sheusuallyremainedinsidefor
if a fertilizationwindow exists(i.e. when the oviduct 15to 45 rain, afterwhicha neweggwaslaid (thepreis free of a developingeggthat couldblockthe ovi- cisetime of laying was unknown).My first hour of
duct),but a secondpeaktakesplacein theafternoon, observationbeganassoonasthe femaleenteredthe
whichwouldnotbe predictedaccording
to the fer- boxin caseshelaid an eggimmediatelyuponentertilization-window
hypothesis.
Because
mateguard- ing. I interruptedobservations
brieflyafter30 min to
ing is often easier to observeunder field conditions
checkwhetheran egghad beenlaid; if the female
thanare copulations
per se,Pinxtenand Eens(1997)
foundit surprisingthat very few studiesusedmate
guardingasa behavioralclueto helpshedlight on
whethersuchwindowsare importantacrossdifferent species.In their observations
of free-livingEuropean Starlings (Sturnus vulgaris) in Belgium,
paired malesincreasedtheir mate-guardingattentivenessduring the late morning,which is an odd
time for passerines
to lay eggs(seeMace1989,Sheldon 1994)but whichis thetimethat femalestarlings
typicallylay their eggs.
Thepurposeofthisstudywastodetermine
whether maleHouseSparrows(Passer
domesticus)
behaveas
if exploitinga fertilizationwindow. Basedon DNA
fingerprinting,the frequencyper nestof extrapair
offspringin the populationthat I studiedis about
16%(R.R. Whitekillerunpubl.data),sothethreatof
spermcompetitionis very real. As in the starling
study mentionedabove,the questionwas whether
pairedmalesincreasetheir mate-guarding
behavior
duringtheputativefertilizationwindow(i.e.justafter theirmateshavelaid an egg),whenthehypoth-
had not left the box, I waited until she exited. After
a quickcountof eggs,I resumedrecordingto getthe
secondhalf of the first hour, which would be within
thefertilizationwindowif thefemalelaid an eggtoward the end of her time in the box. Therefore, the
first hourof observation
sampleda largeportionof
the presumedfertilizationwindow.After this first
sample,I waited30 _+0.5min beforestartingthesecond 1-h observation
period,whichwasintendedto
representa baselinemeasureof pair behaviorduring
the layingperiodbut outsideof the putativefertilization window. During observationperiods, I recorded the times when either mate entered or exited
the nestor vanishedfrom my view.
To controlfor possibletime-of-dayeffectsin the
aforementionedfertilization-periodsamples,a second setof sampleswas takenduring the incubation
period, involving pairs not used previously.These
samplesdifferedfromtheaboveprotocolin onlyone
respect:to minimizetherisk of desertionthatmight
accompanydisturbance(Seel 1968)during incubation, and becausethe female spendsa great deal
esispredictsthat suchactsshouldbe the mosteffec- moretime on the eggsoncelaying is complete,the
tive, relative to a secondhour-longsampletaken nestbox was not openedinitially to checkthe eggs.
slightlylateron the samemorning(whenanysuch Instead,I stoodbeneaththe nest briefly beforerewindow wouldhaveclosed).Similarly,differences
in turning to the car, thus causingdisturbancecommate-guardingfrequencyshouldbe greaterbetween parableto checkinga nestbut not enoughto cause
thetwo sampledhoursduringdaysin themiddleof desertion.
When a male was outside of the nest box and withthe layingperiod(whenfertility is at stake)thanfor
comparablesamplestakenon daysoutsideof thefer- in 10m of thefemale,hewasconsidered
to beguardtile period.
ing her (seeBurkeet al. 1989,Kempenaers
et al.
Methods.--Istudied House Sparrowsat Norman, 1995).The total time the malespentguardingwas
October 1999]
ShortCommunications
30-
1143
30-
early
late
LayingPhase
early
late
Incubation Phase
FIG.1. Incidenceofmateguardingby maleHouseSparrowsin earlyandlatemorningobservation
periods
during layingand incubation.Valuesare œ_+SD.
summedfor each 1-h observationperiod. Paired-t pothesisis that its durationcanonlybe approximated. Tobe conservative,
I usedthe highestestimateof
the firstversusthe secondobservation
periods.The the window's duration (60 min), but other estimates
testswere usedto comparemate attendancetimesin
difference
in mate attendance
between the first and
range as low as 10 min (e.g.Wetton and Parkin 1991).
secondsampleswas calculatedfor both the laying In somespeciesof open-cupnesters,the start of the
and the incubationperiods.Because
thesedatawere window(whichcoincides
with the layingof theprenot normally distributed,I used a Mann-Whitney viousegg)maybedetectedaccurately,
andin theory
testto comparedifferences
by period(i.e. layingvs. males could use this as a cue to determine when the
incubation). All tests were two-tailed.
window is open.Alternatively,malesmay haveto
Results
anddiscussion.--No
temporaleffectonmate rely on a simplebehavioralrule, suchascopulating
guarding occurred during the incubationperiod in the morning. If so, that might help explain the
(pairedt = 0.45,df = 7, P = 0.67;Fig. 1), somales morningpeaksin copulationobservedin manybirds
did not simply reducethe amountof time spentat that also lay in the morning (e.g. Tree Swallows
the nestor with the femaleasthe morningpassed. [Tachycineta
bicolor],Lifjeld and Robertson1993;ZeIn contrast,the samecomparison
duringthe laying braFinches[Taeniopygia
guttata],Birkheadet al. 1989;
periodshowedthat malesspentmuchmoretime at- and Smith'sLongspurs,
Briskie1992).
tending the female during the first sampleperiod
Behavioralpatternsconsistent
with exploitationof
thanduringthe secondsampleperiodfor themorn- a fertilization window have been noted in other
ing (paired t = 5.03, df = 7, P = 0.002;Fig. 1). The birds. For example,female Mallards are more "atdifferencesin mate guarding betweenfirst versus tractive"to malesand experiencemore attemptsat
secondobservation
periodsweremuchhigherdur- forcedcopulationjustaftereachlayingeventthanat
ing laying(14.38_+8.09min) than duringincubation anyothertime(Chenget al. 1983).Thishasbeenpro(0.95_+6.06min; Mann-WhitneyU = 4.0, P = 0.003). posedto occurbecauseunlike the female'smate, an
As predicted,male HouseSparrowsspentmore extrapairmaleprobablyis not copulatingrepeatedly,
time closeto their matesduring the laying period so it would benefit him to choose the best moment to
than during the subsequent
incubationperiod,and attemptan extrapaircopulation(i.e. during the puon laying days they tended to be near the female tative fertilizationwindow).Anotherexamplemay
more during the putative fertilization window than be the Aquatic Warbler (Acrocephalus
paludicola),
laterin the morning,a patternwhollyabsentduring whichhasveryintensespermcompetition(multiple
the corresponding
hoursof the incubationperiod. paternityin at least50%of broods;Schulze-Hagen
et
Takentogether,theseresultsare consistentwith the al. 1995).During the female'sprelayingfertile periview thatpairedmalesbehaveasthougha verybrief od, mostcopulationsoccurlate in the day,but once
opportunityfor the successful
introductionof ejac- layingbegins,copulationsoccurmostfrequentlyin
ulate exists,and that paired males adjusttheir be- themorningandusuallydirectlyaftera layingevent
haviorto this circumstance
in waysthat minimize (within the presumedfertilizationwindow).Finally,
therisksof spermcompetition
frompotentialextra- althoughCommonChaffinches(Fringillacoelebs)
repair copulations.
ducecopulationafterthe startof layingandshowno
One difficultywith the fertilization-window
hy- increasein copulationsduring the presumedfertil-
1144
ShortCommunications
ization window, males seemto guard their mates
more intenselyduring this period (Sheldon1994,
[Auk, Vol. 116
competitionin the polygynandrousSmith's
Longspur.Auk 109:563-575.
SheldonandBurke1994),muchlike thesparrowsin BURKE,T., N. B. DAVIES, M. W. BRUFORD,AND B. J.
the presentstudy.
HATCHWELL.
1989.Parentalcareand matingbeIn contrast,malesof someother speciesdo not
haviourof polyandrousDunnocksPrunellamodguardor copulatemoreduringtheputativefertilizaularisrelatedto paternityby DNA fingerprinttion window. For example,male WesternBluebirds
ing. Nature 338:249-251.
(Sialiamexicana)
do not increasetheircopulationrate CHENG, K. M., J. T. BURNS, AND E McKINNEY. 1983.
duringthe presumedfertilizationwindow (DickinForcedcopulationin captiveMallardsIII. Sperm
competition.Auk 100:302-310.
sonandLeonard1996).Instead,mateguardandcopulation increaseduring a generalfertile period (de-
DICKINSON, J. L., AND M. L. LEONARD.1996. Mate at-
finedas 10 daysbeforeclutchinitiationthroughthe
tendanceand copulatorybehaviourin Western
completionof laying).This optionmay be the best
Bluebirds:Evidenceof mate guarding.Animal
Behaviour 52:981-992.
availablefor speciesin which malescannotdetect
KEMPENAERS,B., G. R. VERHEYEN, AND g. g.
wheneggsarelaid by theirmates.
Acknowledgments.--I
thank D. W. Mock and P. L.
DHONDT.1995. Mate guarding and copulation
Schwagmeyer
for allowingme to usetheir research
behaviourin monogamous
andpolygynous
Blue
Tits: Do males follow a best-of-a-bad-jobstratpopulation,for theirhelpwith research
design,and
for editorial feedback. I also thank R. R. Whitekiller
egy?BehavioralEcologyand Sociobiology
36:
33-42.
for encouragement
and permissionto cite her un1992. Female conpublisheddata.Thisworkwassupported
by Nation- LIFJELD,J. T., AND R. J. ROBERTSON.
al ScienceFoundationgrant BNS 9408148and NSF
trol of extra-pairfertilizationin Tree Swallows.
Research
Experience
for Undergraduate
Supplement
Behavioral
EcologyandSociobiology
31:89-96.
to P. L. Schwagmeyer
and D. W. Mock,and alsoby MACE, R. 1989. Great Tits choosebetween food and
the University of OklahomaUndergraduateReproximityto a mate.The effectof time of day.
searchOpportunitiesProgram.
BehavioralEcologyand Sociobiology24:285290.
NEGRO, J. J., J. A. DONAZAR, AND E HIRALDO. 1992.
LITERATURE CITED
ADKINS-REGAN, E. 1995. Predictors of fertilization in
the JapaneseQuail, Coturnixjaponica.Animal
Behaviour 50:1405-1415.
BAKST, M. R., AND D. M. BIRD. 1987. Localization of
oviductalsperm-storagetubulesin the American Kestrel (Falcosparverius).Auk 104:321-324.
Copulatorybehaviourin a colonyof LesserKestrels: Spermcompetitionand mixed reproductive strategies.Animal Behaviour43:921-930.
PARKER,
G.A. 1970. Sperm competitionand its evolutionaryconsequences
in the insects.Biological
Reviewsof theCambridgePhilosophical
Society
45:525-567.
BAKST,M. R., G. WISHART,AND J.P. BRILLARD.1994. PINXTEN,R., AND M. LENS. 1997. Copulation and
mate-guardingpatternsin polygynousEuropeOviductalspermselection,
transport,andstorage
in poultry.PoultryScience
Review5:117-143.
BIRKHEAD,t. g., E. J. A. CUNNINGHAM, AND K. M.
CHENG.1996. The inseminationwindow providesa distortedview of spermcompetitionin
birds.Proceedings
of theRoyalSocietyof London Series B 263:1187-1192
an Starlings.Animal Behaviour54:45-58.
SCHULZE-HAGEN,K., B. LEISLER,T. R. BIRKHEAD,AND
A. DYRCZ.1995. Prolonged copulation,sperm
reservesand spermcompetitionin the Aquatic
Warbler,Acrocephalus
paludicola.
Ibis 137:85-91.
SELL,D.C. 1968. Clutch-size, incubation, and hatch-
ing success
in theHouseSparrowandTreeSparrow. Ibis 110:270-282.
1989.Spermcompetition
in theZebraFinch,TaeB.C. 1994. Timing and use of paternity
niopygia
guttata.Animal Behaviour38:935-950. SHELDON,
guardsby male Chaffinches.
Behaviour129:79BIRKHEAD,t. R., AND A. P. MOLLHR.1992. Sperm
97.
competitionin birds: Evolutionarycausesand
SHELDON,
B.C., ANDT. BURKE.1994.Copulationbeconsequences.
AcademicPress,London.
haviorand paternityin the Chaffinch.BehaviorBIRKHEAD,
T. g., ANDA. P. MOLLHR.
1993.Why do
al Ecologyand Sociobiology
34:149-156.
malebirds stopcopulatingwhile their partners
BIRKHEAD,t. R., E M. HUNTER, AND J. E. PELLATT.
are still fertile? Animal
Behaviour
45:105-118.
WETTON,J. H., AND D. t. PARKIN. 1991. An association
betweenfertility and cuckoldryin the House
Sparrow,Passerdomest&us.
Proceedingsof the
1964.Distributionof spermatozoa
in the oviduct
RoyalSocietyof LondonSeriesB 245:227-233.
and fertilityin domesticbirds.Journalof Reproductionand Fertility 8:49-58.
Received
13 March 1998,accepted
10 February1999.
BRISKIE,
J. V. 1992. Copulationpatternsand sperm AssociateEditor: ]. Ekman
BOBR,L. W., E X. OGASAWARA,AND E W. LORENZ.