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 copulationsdirectly in the NorthernRookeryat Cape Bird, RossIsland,
for food or for accessto food resources(Lack 1940, Antarctica(77ø13'S,166ø28'E).Observations of cop-
Brown 1967). For example, Wolf (1975) found that ulationbehaviorweremadeduringtheprelayingpe-
male 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 involving at leastfive different females,seenover the
more likely to copulateif the male givesher food four seasonsof study.In eachcase,a femalejoined a
duringcourtship. Weareunawareof anydescription single,unpairedmaleat hisnestsite;courtship(side-
of copulationsbeingdirectlyexchangedfor anyma- ways-stareand bow; Spurr 1975a)was followed by
terial item other than food. Furthermore, this behav- the 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 unsuc-
celisadeliae)acquiringnest material from extrapair cessfulcopulationattempt, the male producedan
malesafter engagingin copulationswith them.This ejaculatethat missedthe female'scloaca.In the re-
material 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,sug-
caninundatethebreedingcolony.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 thesefe-
smallneststo fail asa resultof floodingby meltwa- malesreturnedto her partnerimmediatelyafter the
ter. Moreno et al. (1995) concluded that stone col-
EPC 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: fiona@zoo.cam.ac.uk In addition, as previouslyreported by Derksen
526
April 1998] ShortCommunications 527

(1975),femaleswere observedacquiringstonesfrom if the male is unaware of the female's status as a

maleswithoutengagingin copulations. In eachcase, pairedindividual,he mayview thecopulationasthe
this behaviorwasinitiatedby the femalejoiningan initiationof a long-termpartnership,
in whichthefe-
unpairedmale at his site and engaginghim in mu- male rearrangingneststones(althoughnot taking
tual courtshipbehavior.Shethensimplytooka stone them awayfrom the nestsite)would constitutenor-
and left the site.Again, the malewasnot aggressive mal behavior.Because manylong-termpairingsare
toward the female, suggestingthat females may initiatedby a femalecomingto a male'ssite,courting
avoidaggression by solicitingcourtship.Tenfemales with him and engagingin copulation,any male ig-
wereobservedto engagein thisbehavior:onefemale noringsucha solicitation, or actingaggressively to-
was observedto take at least62 stonesfrom a single
ward a femalemanipulatinghis stones,might miss
male over a period of approximatelyone hour; an-
other female took one stone from one male and three a genuineopportunityto form a pair.
It is harder to seewhat a femalewould gain from
stonesfrom anothermale four dayslater;a third fe-
maletookstonesfrom a singlemaleon two separate tradingan EPCfor oneor two stones.A straightex-
occasions(fourdaysapart).Theincidenceof thisbe- changewould suggestthat to the female,eitherthe
havior would have been underestimated because it two wereequallyvaluable,or theEPCwaslessvalu-
was recordedlate in the 1996seasonby FMH only, able.This seemsunlikelywhen an EPC hasthe po-
andin 1997.In addition,thisbehaviormayhavebeen tentialto alterthepaternityof heroffspring,whereas
overlookedduring periodsof peak copulationactiv- a singlestonedoeslittle to increasethe likelihoodof
ity becausethe focusof observations wascopulation a successful breedingattempt.It is possiblethat the
behaviorrather than courtshipbehavior.In these exchange of oneEPCopensthe way to the femaleto
cases,it wouldappearthatthemalewascheatedinto collectmultiplestones,whichmightindeedincrease
allowingthe femaleto take a stonewithout gaining thechances of heroffspringsurviving.If so,thepair
anythinghimself. malemightbe predictedto respondto hisfemaleen-
On a few occasions(n = 7), in responseto a female gagingin extrapaircopulations by attemptingto col-
attemptingto steala stonefrom a male'snestsite,the lect enoughstonesto preventhis femalefrom need-
male, insteadof defendinghis stones,attemptedto ing to stealthem.Alternatively,a femalemayengage
mount the female. In each of these cases, the female
in an EPC for someotherreason(e.g.fertility assur-
immediatelymovedawayfrom the maleanddid not ance,increasingthe qualityof her offspring,gaining
allowhim to mount.In onlythreeof thesevencases a potentialfuture partner;Westneatet al. 1990)but
did the femaleleavewith a stone.It is possiblethat then exploit the male'sloweredguard by taking a
the male misinterpretedthe female'shead-down
stoneafter shehas engagedin the EPC. In this sce-
postureduringthe processof choosinga stoneand
nario,the femalegainsboth an EPCand someeasily
took it to be the head-bowcourtshipdisplaythat
usuallyprecedescopulation,althoughin no casedid obtainednest material. In addition, by returning to
the femalelie proneat the site,a necessary precursor her pair male with a stone,shemay be supplying
to successfulmounting. him with a reasonfor her absence.This trickery
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) femaleschoseun- In conclusion, it appearsthat femaleAd•lie Pen-
pairedmaleswith whomto engagein EPCs(females guins sometimesacquirenest material from extra-
of 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 Antarc-
copulations.
tica New Zealand for providingexcellentlogistical
The male clearlybenefitsby gainingan EPC that
couldresultin offspringfatheredby him but raised supportin all fieldseasons. Wewouldlike to thank
by anothermale(McKinneyet al. 1984,Birkheadand Corey Bradshaw, Rob Harcourt, Sue Heath, Gary
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 po-
tential benefit.The male alsomay gain if allowing a for helpful commentson the manuscript.The re-
femaleto take a stonemeansthat sheis morelikely searchwas fundedby the Natural EnvironmentRe-
to returnfor additionalcopulations, whichcouldin- searchCouncil,UK (FMH), and the University of
creasehischances of fertilizinghereggs.In addition, Otago,New Zealand (LSD).
528 ShortCommunications [Auk, Vol. 115

LITERATURE CITED strapPenguin(Pygoscelis

antarctica)1. Sexroles
and effectson fitness.Polar Biology 15:533-540.
BIRKHEAD,t. R., AND A. P. MOLLER.1992. Sperm SLADEN,W. J. L. 1958.The pygoscelidpenguins.II.
competitionin birds: Causesand consequences. The Ad•lie Penguin.Falkland Islands Depen-
Academic Press, London.
denciesSurveyScientificReports17:23-97.
BROWN,R. G. B. 1967. Courtship behavior in the SPURR,E. B. 1975a. Communication in the Ad•lie
LesserBlack-backedGull, Larusfuscus.Behav- Penguin.Pages449-501 in The biologyof pen-
iour 29:122-153.
guins(B. Stonehouse, Ed.). Macmillan,London.
DERKSEN, D. V. 1975. Unreportedmethod of stone SPURR,
E. B. 1975b.Breedingof the Ad•lie Penguin
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adeliaeat Cape Bird. Ibis 117:324-338.
TASKER,C. R., AND J. g. MILLS. 1981. A functional
HUNTER, E M., L. S. DAVIS, AND G. D. MILLER. 1996.
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Sperm transfer in the Ad61iePenguin. Condor
98:410-413. Gull (Larus novaehollandiae).
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241.
HUNTER, E M., G. D. MILLER, AND L. S. DAVIS. 1995.
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MCKINNEY, E, K. M. CHENG, AND D. J. BRUGGERS. copulationsin birds. Current Ornithology 7:
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Nest maintenance and stone theft in the Chin- 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,
Queensland4072,Australia;and
2Departmentof Ecology,
MasseyUniversity,Palmerston
North,NewZealand

In many cooperativelybreeding speciesof birds, 1972,Emlen1984,Curry and Grant 1989,Reyer1990,

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,
Brown 1987). The occurrenceof male-biased sex ra-
tios in somepopulationsof specieswith helpers-at-
the-nesthas led to the hypothesis(the differential
mortality model of Emlen et al. [1986]) that a short-
age of femalescouldexplain--at leastin part--de-
layeddispersal,helpingbehavior,andmate-sharing
by males(Rowley1965,Maynard Smith and Ridpath
E-mail: agoldizen@zoology.uq.edu.
au
Davies 1992). A shortage of females might result
from a higher rate of mortality comparedwith
males, perhaps associatedwith female-biaseddis-
persal.An experimentaltest on SuperbFairy-Wrens
(Maluruscyaneus)provided support for this model
(Pruett-Jonesand Lewis 1990).
A classicexample in the debate on the link be-
tweensexratiosand cooperativebreedingis the Tas-
manian 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-
vidualscollectednearhis study area and sexedby
dissection.Maynard Smith and Ridpath (1972)used