The Auk 115(2):526-528, 1998
FemaleAd•lie PenguinsAcquireNest Material from ExtrapairMales after Engaging
in Extrapair Copulations
E M. HUNTER •'3 AND L. S. DAVIS 2
•Department
ofZoology,
DowningStreet,University
of Cambridge,
Cambridge
CB23EJ,UnitedKingdom;
and
2Department
of Zoology,Universityof Otago,P.O.Box56, Dunedin,NewZealand
Femalesof a numberof bird speciesoccasionally November(Spurr 1975b).Our study site is situated
havebeenrecordedexchanging
copulations
directly in the NorthernRookeryat Cape Bird, RossIsland,
for food or for accessto food resources(Lack 1940, Antarctica(77ø13'S,166ø28'E).Observations
of copBrown 1967). For example, Wolf (1975) found that ulationbehaviorweremadeduringtheprelayingpemale Purple-throatedCaribs(Eulampis
jugularis)de- riods in 1993,1994,1996,and 1997.Full descriptions
fend groupsof flowersfrom conspecifics
but allow of thestudysiteandmethodsare availablein Hunter
femalesaccess
in exchangefor copulations.
Similarly, et al. (1995, 1996).
in monogamousRed-billed Gulls (Larusnovaehollan- The followingaccountis basedon 10observations
diae),Taskerand Mills (1981)showedthat a femaleis
more likely to copulateif the male givesher food
involving at leastfive different females,seenover the
four seasonsof study.In eachcase,a femalejoined a
duringcourtship.
Weareunawareof anydescription single,unpairedmaleat hisnestsite;courtship(sideof copulationsbeingdirectlyexchangedfor anyma- ways-stareand bow; Spurr 1975a)was followed by
terial item other than food. Furthermore, this behavthe femalelying prone at the male'ssite.The male
ior seemsto be limited in monogamousspeciesto then mounted and copulatedwith the female (see
within-pair interactions,with no recordsof females Hunter et al. [1995, 1996] for a full descriptionof
of any speciestrading food or any other immediate copulationbehavior).In 8 of the 10 casesobserved,
material benefit for extrapair copulations(EPCs; copulation resulted in successfulinsemination of an
Birkheadand Moller 1992).
ejaculate,determined by observationof the male's
Here, we describefemaleAd61iePenguins(Pygos- ejaculateenteringthe female'scloaca.In one unsuccelisadeliae)acquiringnest material from extrapair cessfulcopulationattempt, the male producedan
malesafter engagingin copulationswith them.This ejaculatethat missedthe female'scloaca.In the rematerial is in the form of small stones used to create
maining copulationattempt,the pair wasdisrupted
a platformon whichthe femalelaysher two eggs. by a neighboringindividual prior to cloacalcontact,
Stonesare in greatdemandin the colonyandarecol- andthemaleterminatedtheattempt.Followingeach
lectedby bothmalesandfemalesfromthe groundin copulation,the male dismountedfrom the female,
the area surroundingthe breedinggroup (Sladen and shepickedup a stonefrom his nestsiteand left
1958).In addition, individuals regularly stealstones immediately.In 5 of the 10 cases,the femalereturned
from thenestsitesof otherindividuals(Sladen1958). to the extrapair male forthwith to take a second
Any individual approachinga male at his nest site stoneandleft againwithoutcopulating.Oneof these
and taking a stoneis met with an aggressivere- femalesreturned a total of 10 times, taking a stone
sponsefrom the site-holder(Spurr1975a).Site-hold- from the extrapairmaleon eachoccasion.
At no time
ers will peck, "flipper-bash,"and chasestone-steal- was there any aggressive
responseby the male;he
ers.The benefitof collectingand defendinga large madeno moveto stopthe femalefromtakinga stone
pile of stonesis realized under particular weather from his site. Sevenof the 10 femalesthat gained
conditions,usually in springtime,when meltwater stonesfollowing copulationswere unbanded,sugcaninundatethebreedingcolony.Floodingby melt- gestingthattheycamefromoutsidethestudygroup
water canresultin nestdesertionand eggloss(Tay- in which most of the birds were banded. This was
lor 1962).Morenoet al. (1995)foundthat in the close- supportedby the fact that on four occasions,these
ly related ChinstrapPenguin(Pygoscelis
antarctica), femaleswere followed after copulationand were
which displayssimilarstone-collecting
behaviorto found to have partnersand nest sitesin breeding
the Ad61iePenguin,largenestswerelesslikelythan groupsadjacentto thestudygroup.Eachof thesefesmallneststo fail asa resultof floodingby meltwa- malesreturnedto her partnerimmediatelyafter the
ter. Moreno et al. (1995) concluded that stone colEPC and depositedthe stoneat their nest site. The
lectingand nestmaintenance
improvednestquality remainingthreefemales,eachof whichwasbanded,
and increasedreproductivesuccess.
copulated and took stones from males within the
Ad61iePenguinsare monogamousand breed in studygroupandthenreturnedto theirpartners,also
large coloniesin Antarctica.They engagein court- in the study group.Despitea numberof malesen-
shipand copulation
behaviorduringthe prelaying gagingin EPCsat females'nest sites,in n,ocasedid
period,whichspansfrom mid-Octoberto the end of
a maletakea stonefrom a female'ssitefollowingan
EPC.
E-mail:
[email protected]
In addition, as previouslyreported by Derksen
526
April 1998]
ShortCommunications
527
(1975),femaleswere observedacquiringstonesfrom
if the male is unaware
maleswithoutengagingin copulations.
In eachcase,
this behaviorwasinitiatedby the femalejoiningan
unpairedmale at his site and engaginghim in mutual courtshipbehavior.Shethensimplytooka stone
and left the site.Again, the malewasnot aggressive
toward the female, suggestingthat females may
avoidaggression
by solicitingcourtship.Tenfemales
wereobservedto engagein thisbehavior:onefemale
pairedindividual,he mayview thecopulationasthe
initiationof a long-termpartnership,
in whichthefemale rearrangingneststones(althoughnot taking
them awayfrom the nestsite)would constitutenormal behavior.Because
manylong-termpairingsare
was observedto take at least62 stonesfrom a single
male over a period of approximatelyone hour; another female took one stone from one male and three
stonesfrom anothermale four dayslater;a third femaletookstonesfrom a singlemaleon two separate
occasions
(fourdaysapart).Theincidenceof thisbehavior would have been underestimated
because it
was recordedlate in the 1996seasonby FMH only,
andin 1997.In addition,thisbehaviormayhavebeen
overlookedduring periodsof peak copulationactivity becausethe focusof observations
wascopulation
behaviorrather than courtshipbehavior.In these
cases,
it wouldappearthatthemalewascheatedinto
allowingthe femaleto take a stonewithout gaining
anythinghimself.
On a few occasions(n = 7), in responseto a female
attemptingto steala stonefrom a male'snestsite,the
male, insteadof defendinghis stones,attemptedto
mount the female. In each of these cases, the female
immediatelymovedawayfrom the maleanddid not
allowhim to mount.In onlythreeof thesevencases
did the femaleleavewith a stone.It is possiblethat
the male misinterpretedthe female'shead-down
postureduringthe processof choosinga stoneand
took it to be the head-bowcourtshipdisplaythat
of the female's status as a
initiatedby a femalecomingto a male'ssite,courting
with him and engagingin copulation,any male ignoringsucha solicitation,
or actingaggressively
toward a femalemanipulatinghis stones,might miss
a genuineopportunityto form a pair.
It is harder to seewhat a femalewould gain from
tradingan EPCfor oneor two stones.A straightexchangewould suggestthat to the female,eitherthe
two wereequallyvaluable,or theEPCwaslessvaluable.This seemsunlikelywhen an EPC hasthe potentialto alterthepaternityof heroffspring,whereas
a singlestonedoeslittle to increasethe likelihoodof
a successful
breedingattempt.It is possiblethat the
exchange
of oneEPCopensthe way to the femaleto
collectmultiplestones,whichmightindeedincrease
thechances
of heroffspringsurviving.If so,thepair
malemightbe predictedto respondto hisfemaleengagingin extrapaircopulations
by attemptingto collect enoughstonesto preventhis femalefrom needing to stealthem.Alternatively,a femalemayengage
in an EPC for someotherreason(e.g.fertility assurance,increasingthe qualityof her offspring,gaining
a potentialfuture partner;Westneatet al. 1990)but
then exploit the male'sloweredguard by taking a
stoneafter shehas engagedin the EPC. In this scenario,the femalegainsboth an EPCand someeasily
obtainednest material. In addition, by returning to
usuallyprecedescopulation,althoughin no casedid
the femalelie proneat the site,a necessary
precursor her pair male with a stone,shemay be supplying
him with a reasonfor her absence.This trickery
to successfulmounting.
It appearsthat femaleAd•lie Penguinswill some- wouldbenefitboththefemaleandtheextrapairmale
times acquirenest stonesfrom extrapair malesafter if it reducedthe chancesof the pair maleattempting
engagingin EPCs.Variouspoints of interestcan be a retaliatorycopulation(Birkheadand Mailer 1992).
noted from theseobservations:(1) femaleschoseunIn conclusion,
it appearsthat femaleAd•lie Penpairedmaleswith whomto engagein EPCs(females guins sometimesacquirenest material from extraof mostspecieschoosepairedmales;McKinneyet al. pair malesafter engagingin an extrapair copulation,
1984,Birkheadand Mailer 1992);(2) a high propor- and that both femaleand extrapairmale gain from
tion of the EPC attemptswas successful
(compared this behavior.Even the female'spair male gains a
with 59%,n = 35 pairs,of pair copulations
success- stonein his nest,althoughthis particularstoneand
ful; Hunteret al. 1995);(3) thecurrencyinvolvedwas the othersin his nestultimatelymay help to protect
nest materialratherthan food;and (4) the material the life of an offspringthat is not his own.
benefitwasgainedfollowingEPCsratherthan pair
Acknowledgments.--We
arevery gratefulto Antarccopulations.
tica New Zealand for providingexcellentlogistical
The male clearlybenefitsby gainingan EPC that
Wewouldlike to thank
couldresultin offspringfatheredby him but raised supportin all fieldseasons.
Corey
Bradshaw,
Rob
Harcourt,
Sue Heath, Gary
by anothermale(McKinneyet al. 1984,Birkheadand
Mailer 1992).The costof one or two stoneswould Miller, Cristian PerezMufioz, and Marj Wright for
field assistance and Tim Birkhead and Nick Davies
appear to be a small price to pay for so large a potential benefit.The male alsomay gain if allowing a for helpful commentson the manuscript.The refemaleto take a stonemeansthat sheis morelikely searchwas fundedby the Natural EnvironmentReto returnfor additionalcopulations,
whichcouldin- searchCouncil,UK (FMH), and the University of
creasehischances
of fertilizinghereggs.In addition, Otago,New Zealand (LSD).
528
ShortCommunications
LITERATURE
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Received
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AssociateEditor: J. Ekman
TheAuk 115(2):528-532,1998
"Wife-sharing" in the TasmanianNative Hen (Gallinula mortierii): Is it Caused by a
Male-biased
Sex Ratio?
ANNE W. GOLDIZEN?3 ALAN R. GOLDIZEN,• DAVID A. PUTLAND,• DAVID M. LAMBERT?CRAIG D. MILLAR,2
AND JASONC. BUCHAN•
•Department
of Zoology,Universityof Queensland,
Brisbane,
Queensland
4072,Australia;and
2Department
of Ecology,
MasseyUniversity,Palmerston
North,NewZealand
In many cooperativelybreeding speciesof birds,
adult males are thoughtto outnumberadult females
(e.g. Red-cockadedWoodpecker[Picoidesborealis],
Gowaty and Lennartz 1985; Splendid Fairy-Wren
[Malurussplendens],
Rowley and Russell 1990;Pied
Kingfisher[Cerylerudis],Reyer1990;seeEmlen1984,
1972,Emlen1984,Curry and Grant 1989,Reyer1990,
Davies 1992). A shortage of females might result
Brown 1987). The occurrenceof male-biased sex ra-
(Pruett-Jonesand Lewis 1990).
tios in somepopulationsof specieswith helpers-atthe-nesthas led to the hypothesis(the differential
mortality model of Emlen et al. [1986]) that a shortage of femalescouldexplain--at leastin part--delayeddispersal,helpingbehavior,andmate-sharing
by males(Rowley1965,Maynard Smith and Ridpath
A classicexample in the debate on the link betweensexratiosand cooperativebreedingis the Tasmanian Native Hen (Gallinula mortierii). Ridpath
(1972b)reportedmale-biasedsexratiosamongboth
adults(1.5 malesper female)and chicks(2.8 males
per female)in his study population,and an overall
sex ratio of 1.22 malesper femaleamong489 indi-
from a higher rate of mortality comparedwith
males, perhaps associatedwith female-biaseddispersal.An experimentaltest on SuperbFairy-Wrens
(Maluruscyaneus)
provided support for this model
vidualscollectednearhis study area and sexedby
E-mail: [email protected].
au
dissection.Maynard Smith and Ridpath (1972)used