The Auk 116(2):504-512, 1999
WHY
DO APTENODYTES
PENGUINS
HAVE
HIGH
DIVORCE
RATES?
JOi•LBRIED,1 FRI2DI2RIC
JIGUET,AND PIERREJOUVENTIN
CentreNationaldela Recherche
Scientifique,
Centred'EtudesBiologiques
deChizd,
79360 Beauvoir sur Niort, France
ABSTRACT.--In
long-livedbirds,monogamyis thoughtto enablebreedersto retainthe
samematefrom year to year,but exceptionsoccur.Forexample,King Penguins(Aptenodytes
patagonicus)
andEmperorPenguins
(A.forsteri)havemuchlowermatefidelitythandosmaller species
ofpenguins,despitetheirhighratesof survival.Recently,
Olsson(1998)suggested
thatdivorcein King Penguins
couldbe adaptive.AlthoughOlssonwasthefirstto propose
an adaptivefunctionfor divorcein this species,
he wasunableto assess
the relationships
amongindividualquality,dateof arrival,matechoice,andbreedingsuccess.
Accordingly,
we studiedKingPenguins
andEmperorPenguins
to furtherexaminethedeterminants
and
consequences
of divorce.Mate retentionwasnot affectedby breedingperformance
in the
previousyearor by experience,
andneithermateretentionnor divorcehad significant
consequences
onchickproduction
thefollowingyear.KingPenguins
weremorelikelytodivorce
asarrivalasynchrony
of previous
partnersincreased.
In EmperorPenguins,
thistendency
to
divorceoccurredonlywhenfemalesreturnedearlierthantheirpreviousmates.MostEmperorPenguinpairsformedwithin 24 hoursafterthearrivalof males,whichwereoutnumberedby females.KingPenguins
thathadnestedsuccessfully
in theirnextto lastattempt
werefavoredasmatesfor onesthathadbeenunsuccessful,
andindividualsof bothspecies
probablychosethebestmatesavailable.
Mostof ourresultsfor KingPenguins
andEmperor
Penguins
supportedOlsson's
(1998)conclusions
in thatdivorceappearstobeadaptive.Mate
retentionin the absence
of a true nestingsite(neitherspecies
buildsa nest)wouldbe maladaptivefor thesespecies,
whichfacestrongtime constraints
for breeding.Therefore,divorceoccursbecause
costsof materetentionarehigh.Aptenodytes
penguinsappearto have
adoptedan optimaldivorcestrategyin orderto adaptto their longbreedingcyclein a demandingenvironment.Received
27 June1998,accepted
30 October1998.
SOCIAL
MONOGAMY
is the predominantmat- theirchickontopof theirfeet.Onlytwospecies
ing systemamongbirds(Lack1968),andmany occurin thisgenus,theKingPenguin(AptenoandtheEmperorPenguin(A.
long-livedspecies
havea longreproductive
life dytespatagonicus)
span(Stearns1992).High survivalmayenable forsteri).Beingthe largestspecies
of penguins,
monogamous
speciesto retainthe samemate theyhavea longbreedingcycle,part of which
between successivebreeding attempts more takesplaceduring the australwinter (Stonetheymustopfrequentlythando species
with highermortal- house1953,1960).Consequently,
ity (Rowley 1983). In addition, breeding suc- timize their reproductiveoutputduringsevere
cessoften is enhancedby mate retention(e.g. conditions that involve a decline in food availRowley 1983,Ens et al. 1996).
ability and a four-monthwinter fastfor chicks
High survivalrates and long reproductive of the subantarctic
King Penguin(Stonehouse
life spans are common in seabirds (Ricklefs 1960, Weimerskirchet al. 1992), and low tem1990),but mate fidelity varies amonggroups. peraturesand ice for the antarcticEmperor
For example,albatrosses
are very faithful to Penguin(Stonehouse
1953).In addition,both
their partners (Rowley 1983, Warham 1990), speciesfacestrongtime constraintsfor breedwhereasfrigatebirdsregularly divorce (see ing. Thus,layingaftertheendof Januaryat Iles
Black 1996) between successive
breeding at- Crozetor after 1 Januaryon SouthGeorgiaIstempts(Nelson1976).Thisvariabilityalsooc- land invariably resultsin breeding failure in
curswithin the samefamily,asis the casefor King Penguins(Weimerskirch
et al. 1992,Joupenguins(Williams1996).The genusApteno- ventinandLagarde1995,Olsson1996)because
dytesis unique in that adults do not build a late-hatched chicks have not been able to store
nest,incubatingtheirsingleeggandbrooding sufficient fat reserves before the austral winter
(Stonehouse1960, Van Heezik et al. 1994, JouE-mail: [email protected]
ventinandLagarde1995).In themoresynchro5O4
April 1999]
Divorce
in Penguins
505
nouslybreedingEmperorPenguin(Stonehouse posedthe "expensivefat-storing"hypothesis,
1953, 1960; Isenmann 1971; Weimerskirch et al. suggestingthat individualswould facea trade-
1992),only the earliest-hatched
chicks(i.e.be-
off between the costs of divorce and the costs
fore 10 August;Isenmann1971) are able to de-
of building up reserveswhile waiting for their
previouspartnerssothat materetentionwould
part to seawhen the ice breaksin December,
havingcompleted
theirmoltbut attainingonly
50% of adult body mass(Isenmann1971).
Aptenodytes
penguinsare long lived, with a
occur.AlthoughOlssonbelievedthat divorce
was adaptivein King Penguins,his studystill
neededto be supplementedin somerespects.
the
mean annual survival rate of 0.91 to 0.95 (Jou- In particular,he did not evaluateaccurately
ventin and Weimerskirch 1991, Weimerskirchet
al. 1992).Yet, they show low mate fidelity between years (15% in Emperor Penguin [Isenmann 1971,Jouventin1971];19 to 29% in King
Penguin[Barrat1976,Olsson1998])compared
eventual benefits (in terms of offspring production) of extensivedivorce, and he did not
analyze the relationshipsamong individual
quality,dateof arrival,matechoice,andbreeding success.Despite a lack of data on Emperor
thathis
with otherpenguins(œ= 84%;Williams1996). Penguins,Olsson(1998)alsosuspected
hypotheses
were
relevant
for
this
species;
like
For divorceto be adaptive,individualsthat divorce should obtain some benefit; i.e. it would the King Penguin,EmperorPenguinshave
be "optimal" for an individual to divorce if its part-time pair bonds,and fat reservesplay a
reproductivesuccess
frombreedingwith a pre- major role during courtshipand incubation
viouspartner in the nextyear is lower than its (Pr•vost 1961, Isenmann 1971). Here we proaveragefuture success(i.e. the averagefor all vide resultsfrom our long-termstudy of King
future breedingattemptsuntil the individual Penguins,supplementedwith data from Emperor Penguins,that enabledus to further asdies; McNamara and Forslund 1996).
Severalhypotheseshavebeenput forwardto sessthe adaptivevalueof divorcein thesespeexplain divorcein birds (e.g. Ens et al. 1993, cies.
Choudhury 1995), including penguins (WilSTUDY AREA AND METHODS
liams 1996).The "incompatibility"hypothesis
predictsthatpairshavinglowbreedingsuccess
From September1990to March 1994,we conductare morelikelyto divorce,andthateachof the
ed a demographicstudyof King Penguinsin a small
previouspartnersshouldbe more successful colony(750 pairs) on PossessionIsland, Crozet Arwith its new mate (Coulson 1966, Rowley chipelago(46ø25'S,51ø45'E).We attachedflipper
1983).In specieswith part-timepair bonds(i.e. bandsto 989birds and checkedfor their presenceevduring part of the year only), the main reason ery otherday.To assess
the influenceof previousrefor pairs to split might be asynchronous
re- productivesuccesson divorce,we consideredpairs
turns by previousmates (Coulson1972, Boe- to be successfulif at leastone mate was seenfeeding
kelheide and Ainley 1989, Davis and Speirs a chickafterSeptember,or wasmoltingafterNovem1990).In his study of King Penguins,Barrat ber If the eggdid not hatch,or if oneof the parents
(1976)alsohypothesizedthat divorceis caused was molting before Decemberor displaying in early
December,the pair wasassumedto havefailed (Jouby the asynchronous
return of previouspart- ventin and Lagarde 1995). At best, King Penguins
ners to the colony.However,his assumption can breed successfullyevery other year (Weimerwasbasedon a smallsample(threepairs),and skirchet al. 1992,Olsson1996).Therefore,individual
his study was conducted during only one quality at the onsetof breedingcyclen was defined
breeding season. Recently, Olsson (1998) from the reproductiveperformanceatbreedingcycle
showed that divorce rates in King Penguins n - 2 (Olsson 1996).
Data on EmperorPenguinswere from studiesconfrom South Georgia Island increasedas the
previousmatesreturnedmoreasynchronouslyducted in 1968by P. Isenmann(pers. comm.)and in
to the colony,confirmingBarrat's(1976) hy- 1969by P.Jouventin.Field work was carried out at a
colony(12,500pairs)on PointeG•ologie,TerreAd•pothesis.He alsoshowedthat King Penguins lie,
Antarctica (66ø40'S,140øE),where flipper tags
cameashoreat the onsetof the breedingcycle were attached to 855 individuals between 1965 and
with only half of their body reserves.Because 1967. From arrival until laying, daily observations
they fast when on land, their fat storeswere wereperformedon bandedbirdsthatwereknownto
closeto exhaustionat the end of their first stay have bred in 1967 and 1968. Thus, dates of arrival at
in the colony.Accordingly,Olsson(1998)pro- the colony(in 1968and 1969) and pair formation(in
506
BRIED,
JIGUET,
ANDJOUVENTIN
1969) were known accuratelyfor each individual.
Pairsin which onematewas seenfeedinga chickafter 15 November
were considered
[Auk, Vol. 116
lO
8
8
28
o-3
4-7
8-1o
>1o
lOO
successful.
80
Forbothspecies,
observations
lastedfor half a day
so that the same individual
could be observed sev-
60
eral timeswhile performingdifferentactivities.Sex
was determined
from measurements
and behavior
(Pr•vost1961,Jouventin
1982)wheneverpossible.
Individuals
that lost their band in the course of the
study,or that paired with an unbandedpartner
while their previous(banded)partnerwas not ob-
o
served(the rate of band lossis 22.3%in the first year
Asynchrony of returns (deys)
afterbandingfor KingPenguins;
Weimerskirch
et al.
1992),were excludedfrom our dataset.To assess
the
effectof the asynchrony
of returnsof previouspart1 oo
nerson matefidelityin King Penguins,we controlled
for the effectsof previousbreedingperformance .__.6o
(successfulvs. unsuccessful)and breeding experience,becausetheseparametersare known to influence mate retention in a number of species(Greenwood and Harvey1982,CoulsonandThomas1983).
We performedstepwiselogisticregressions
using
PROC CATMOD (maximum-likelihoodanalysis)of
•
6o
•
2o
SAS(1988).Only thebest-fitting(i.e.mostparsimonious)modelsarepresentedin theResults.It wasnot
possibleto control for previousbreeding performance in Emperor Penguinsbecausewe did not
know whether1967breedingpairs were successful
or failedprior to divorceor remating.Breedingsuccesswasknownfor somepairsthatbredin 1968,but
we did not take it into accountbecauseour sample
size was too small for reliableanalyses.When controlling for breedingexperience,
we consideredonly
theknownexperience
of individuals(i.e.thenumber
of breeding attempts since the beginning of our
study, not the number of breeding attemptsperformedby an individual sinceit recruitedinto the
10
10
10
0-5
6-15
>15
Asynchrony of returns (days)
FIG. 1.
Mate retentionand asynchronyof return
of partnersfromthepreviousyearin KingPenguins
(top) and EmperorPenguins(bottom).Successful
and unsuccessfulpairs were pooled. Blackbars =
mate-fidelityrates,graybars= divorcerates;sample
sizes indicated
above bars.
Potential
factorsin divorce.--AmongKing Penbreedingpopulation).If thesamebird wasobserved guin pairsfor whichreturndateswereknown
during severalconsecutiveyears,we avoidedpseu-
for both mates,matesof the 39 pairs that di-
doreplication
by calculating
themeanvaluefor each vorcedwere more asynchronous
in returning
parameterbefore conductingour analyses.G-tests to the colony(• = 15.3 +_SD of 9.8 days)than
were performedusingWilliams' correction.All tests werethoseof the 16pairsthatreunited(•?= 5.9
were consideredsignificantat P < 0.05.
RESULTS
Pair-bond
durationandmatefidelity.--Thedurationof pair bondsin King Penguinsneverex-
ceededtwo successive
years,and theprobability of divorcewas 78% (n = 76 pair years).Mate
fidelity (22%) tended to be higher than that
found in two consecutiveyears for Emperor
Penguins(15%) by Isenmann(1971;41 pairs)
and Jouventin(this study;21 pairs),although
the differencewasnot significant(G = 1.37,df
= 1, P > 0.2). Pair bondslastedup to four years
in Emperor Penguins.
- 5.0 days). Likewise, return asynchronyof
previouspartnerswas significantlyhigher in
unsuccessfulpairs (• = 13.6 -- 9.8 days,n = 48)
than in successful
pairs (•?= 5.3 - 6.0 days,n
= 6; Kolmogorov-Smirnovtest, D = 0.60, P =
0.04). However,preliminary modelsgiven by
the CATMODprocedurefailedto find a significant effect of previous reproductiveperformance and breeding experienceof pairs on
mate retention,which decreasedsignificantly
as the secondpartnerreturnedto the colony
later (best-fittingmodel;asynchrony,
X2= 9.06,
df = 1, P = 0.026, n = 54 pairs; see Fig. 1).
Amongpairsthatdivorced,asynchrony
of previouspartnerswassimilarregardless
of which
April 1999]
Divorcein Penguins
lOO
Males: n= 116
Females: n= 94
8o
507
= 1, P = 0.097; see Fig. 1). Among pairs in
whichthefemalereturnedto thecolonyearlier
than the male (n = 18), divorcetendedto occur
more frequentlyas asynchronyincreased,but
6o
thistendencywasnot significant
(asynchrony,
40
X2 = 3.33, df = 1, P = 0.068;experience,X2 =
0.22, df = 1, P = 0.63). FemaleEmperorPenguinsreturnedearlierthan malesbothin 1968
and 1969, the differencebeing significantin
20
o
o-1
2-10
>10
1969 (Wilcoxon'srank-sum test, z = 2.15, n• =
92, n2= 86, P = 0.031).Femalesalsospentsignificantly more time betweenreturning and
pairing(œ= 4.4 + 7.3days,n = 70)in 1969than
did males (• = 1.9 _+5.0 days, n = 73; Kolmo-
Days after arrival
lOO
gorov-Smirnovtest, D = 0.26, P = 0.013). Consequently, 82% of males and 56% of females
pairedwithin 24 hoursaftertheirarrival(Fig.
2). Fordivorcedpairsin whichpairingdateof
the first-arrived mate was known, the second
partnerreturnedto the colonyafterits previous mate was paired in 7 casesand while its
previousmate was unpairedin 12 cases.
o-t
2-1o
>to
Days after arrival
FIc.
2.
Time elapsedbetween arrival and courting in King Penguins(top) and between arrival and
pairing in EmperorPenguins(bottom).Gray bars =
males, black bars = females.
sexreturnedthe earliest.Independent
of fidelity, femalesbegan courtingsignificantlyfaster
after returningto the colony(• = 1.9 _+4.3
days,n = 94) than did males (œ= 4.0 _+6.3
Data on breedingsuccessin the previous
year were availablefor 74 pairs of King Penguins.ForEmperorPenguins,dataonbreeding
attemptsin thepreviousyearwereavailablefor
36 pairs,but we knewtheoutcomeof thoseattempts for only six pairs. Consideringreproductiveperformance
percapita(i.e.overthetotal numberof individualsor pairsstudied),in
both speciespairsthat divorcedproducedas
many chicksas thosethat reunitedin the next
year (data for King Penguins;divorce, X2 =
0.06, df = 1, P = 0.8, experience,X2 = 0.01, df
= 1, P = 0.91, n = 74). However,high-quality
days, n = 116; D = 0.25, P = 0.003). Consequently,63%of females,but only 38% of males, King Penguins(i.e. successfulbreedersin next
were seen courtingpotential partnersduring to lastbreedingcycle)tendedto divorcelessof-
the 24 hoursafter their arrival(Fig.2). In divorcedpairs,the partnerthat arrivedearliest
was already performing courtship display
when its previousmatereturnedin 37 cases,
ten than poor-qualityones,althoughthe differencewas not significant(quality,X2 = 3.12,
df = 1, P = 0.077;experience,X2 = 0.63, df = 1,
P = 0.43, n = 69).
Olsson(1995)founda slightsurplusof males
In EmperorPenguins(n = 26 pairs),neither in theKingPenguincolonyhe studiedonSouth
its imporasynchrony
of previouspartners,northesexof Georgia,althoughhe did not assess
the partnerthatreturnedfirst,norexperiencetance.In our Iles Crozetcolony,428 of the 989
of breedingpairs (one breedingattemptvs. bandedKing Penguinscouldbesexed,yielding
morethanoneattempt)affectedtheprobability a ratio of 1.53 malesper female (259males,169
of divorce. Yet, the latter factor tended to de- females).Yet, malesare easierto identify than
pendon theinteractionbetweentheformertwo femalesbecausethey performdisplaysmore
we mayhaveoverestimatfactors,althoughnot significantlyso (asyn- often.Consequently,
chrony,X2 = 0.51, df = 1, P = 0.47; sex,X2 = ed theproportionof malesin theKingPenguin
2.20, df = 1, P = 0.14;experience,X2 = 1.90,df population.
In theEmperorPenguin,
Isenmann
= 1, P = 0.17;asynchronyx sex,X2 = 2.74, df (1971) and Jouventin(1971) showed that reand was still alone in one case.
508
BRIED,
JIGUET,
ANDJOUVENTIN
males outnumberedmales by about 10% at
PointeG•ologie.Forbothspecies,
reproductive
performance
in theyearbeforedivorcing
or reuniting did not differ significantlyfrom that in
the yearfollowinga divorceor rematingwith
[Auk,Vol. 116
theyreturnedto thecolonylater(dateof return,
X2 = 4.97, df = 1, P = 0.026, n = 44). We knew
the qualityof thenew andtheformermatesfor
five individualsthat divorced,and they were
similarin all cases.ForEmperorPenguins,the
very small numberof individuals for which reMate retentionvs.divorce:
Costsandbenefits.- productiveperformance
wasknownduringthe
Retainingone'spartner or divorcinghad no previousbreedingseason
precludedtheanalysignificanteffecton reproductiveperformance sesthatwe performedfor KingPenguins.
a previous partner
in the nextyearin KingPenguins,
evenif we
controlledfor previousbreedingexperience.
In
DISCUSSION
EmperorPenguins,divorcedindividuals tend-
ed to producemoreoffspring(œ= 0.47chicks)
Factorsin divorce:'14synchrony
of return" and
than thosethatremated(œ= 0.17chicks)with 'fat-storage"hypotheses.--Mate
retention in our
theirpreviouspartners,but the differencewas KingPenguincolonyoccurredmorefrequently
not significant(preliminarymodel;experience, if bothpartnersof the previousyearreturned
P = 0.14;best-fittingmodel;mate retention,X2 synchronously
at the startof thebreedingsea= 3.28, df = 1, P = 0.07; sex, X2= 0.47, df = 1, son,confirmingBarrat's(1976)hypothesisfor
P = 0.49,n = 63). In neitherspeciesdid dateof KingPenguinsin anothercolonyon IlesCrozet
arrival (earlieror later than previouspartner) andOlsson's
(1998)resultsfromSouthGeorgia
or sexhavea significant
effectonbreedingsta- Island.In EmperorPenguins,asynchrony
also
tus (breederor nonbreeder)
duringtheyearfol- might play a role,but only in thosepairs in
lowing a divorce.
whichfemales(i.e.the mostrepresented
sex)
Individualqualityand matechoice.--InKing return the earliest. However, and like in OlsPenguins,
high-qualityindividuals(seeabove) son's(1998)King Penguincolony,the incidence
tendedto returnto thecolonyearlierthanbirds of divorcewashigh (50%in CrozetKing Penthathadfailed,but thedifference
wasnotsig- guins and 60% in EmperorPenguins;Fig. 1)
nificant (Wilcoxon'srank-sum test, z = 1.84, n• evenwhen asynchrony
was low, confirming
= 18, n2 = 96, P = 0.065).The probabilityof that this factor alone was not sufficient to exsuccessfully
raisinga chicktendedto behigher plain high divorceratesin Aptenodytes
penin pairs with at leastone high-qualitymate guins.
(20%,n = 15)thanin pairsformedby twolowOlsson(1998)alsosuggested
thatmateshiftqualitymates(0%,n = 18),but again,the dif- ing in King Penguinsdependedon the amount
ferencewasnot quitesignificant(Fisher'sexact of fat stored.Accordingto the "expensivefattest,P = 0.08).Because
high-qualityindividu- storing"hypothesis,attainingfat reservesbealsappearedto be at a reproductive
advantage, fore matingis costlyowing to decreased
mawe examinedwhethermatequalitywasanim- neuverabilityin thewateranddecreased
fightportant criterionin mate choice.Low-quality ing ability,andbecause
storingfat to ensurereindividualswere significantlymore likely to mating with one'spartner from the previous
obtaina high-qualitypartnerthanwerehigh- yearcanimplylatebreeding.Thus,individuals
quality ones,and the interactionbetweenin- would face a tradeoff between the costs of didividualqualityandreturndatealsohada sig- vorceand thoseof materetention.In Emperor
nificanteffectonthequalityof thematechosen Penguins,
femalesreturnto thecolonyin April
(individual quality,X2= 4.48,df = 1, P = 0.034, with lowerfat reservesthan do males(Pr•vost
date x individualquality,X2= 5.54, df = 1, P 1961).Onceashore,theyfastuntil egglaying,
= 0.018,n = 54). Preliminarymodelsfailedto whichoccursin May. Thereafter,theyunderreveala significanteffectof experience.
Mate take a long foragingtrip at sea to replenish
quality did not seemto dependon return date their body reserves.Meanwhile,males take
in high-qualityindividuals(sex,X2= 0.13,df = chargeof incubation(Pr•vost1961).Their fast
1, P = 0.72; date, X2 = 0.74, df = 1, P = 0.39, n will end at the beginningof chickrearing,
= 10). In contrast,low-qualityindividuals(i.e. when femalesrelievethem (Isenmann
1971).
failed breederstwo cyclesearlier) were more Wetherefore
suggest
thatfemaleEmperorPenlikely to obtaina low-qualitypartnerwhen guins face a tradeoffbetweenreplenishing
April 1999]
Divorce
in Penguins
theirbodyreserves
beforefastingduringcourtship,andthepotentialcostsof divorceandlate
breeding,or of notbreedingat all if theycannot
find a male. Storing and carrying fat also is
costlyfor adult males,which havelower survival ratesin this species(Jouventinand Weimerskirch1991),partly because
they aremore
vulnerableto predationat seathan are females
(Jouventin1974).While at sea during this period, theirmaneuverability
is decreased,
which
alsois consistentwith the "expensivefat-storing" hypothesis.In both species,laying (and
hence,mating)as early aspossibleshouldenable the female to limit the duration of her for-
509
constraints
than the lattertwo speciesthatlive
at lower latitudes (Marchant and Higgins
1990).
Absence
of a nestsite.--Penguinsgenerally
live in huge colonies(Marchantand Higgins
1990). Locating one'sprevious partner among
several thousand individuals apparently is
mucheasierfor penguinsthatbuildnestsor dig
burrows (Jouventin1982), and theseterritorial
speciestend to exhibitstrongnest-sitetenacity
(60 to 98% for nine species)and high mate fidelity(up to 97%;Williams1996).Nonetheless,
Williams (1996) found no significantcorrelation between
mate
retention
and nest-site
fi-
aging trip at sea before she relievesher incu- delity among14 speciesof penguins.In addibating mate. Simultaneously,
the probability tion,if individualsdivorcesimplybecause
they
that males would exhaust their fat reserves and
areunableto locatetheirpreviouspartner,then
abandontheireggsshoulddecrease.
Individu- divorce should occur less frequentlyin the
als of both sexes should obtain a mate before
their body reservesare reduced to a critical
threshold;beyondthisthreshold,abreedingattemptalmostinvariablywouldresultin failure.
Factorsin divorce:
Sexratio.--FemaleEmperor
Penguins,whichseemto returnearlierandare
slightly more numerousthan males, tend to
monopolizeeachsolitarymaleuponits arrival
at the colony(Isenmann1971,Jouventin1971)
so that pair formationoccursalmostimmediately after maleshave arrived (Isenmann1971,
this study).As a result,the earliera femalereturns at the onsetof the breedingcycle(1) the
higherthe probabilityshewill get a mate (Isenmann1971),and(2) thelowertheprobability
that her previousmatewill alreadybe paired
with anotherfemale.Consequently,
the unbalanced sex ratio in Emperor Penguins,combined with the body-reserveproblem noted
above(plusthe physiological
synchrony
of individualsandtheadvantageofbreedingasearly aspossible),maybe a factorin divorcein this
species.Monopolizingpartners has not been
recordedin King Penguins.Moreover,YelloweyedPenguins(Megadyptes
antipodes)
andLittle
Penguins(Eudyptula
minor)havehigh matefidelity (82%;Richdale1947,Reilly and Cullen
1981,Dann and Cullen 1990)despitebiasedsex
ratios.Therefore,a biasedsexratio is unlikely
to be a generalfactorin divorceamongsphenisciforms.TheEmperorPenguinseemsto be an
exception,
but onlybecause
the differentphases of its breedingcycleoccurmore synchronously than in King Penguins,and Emperor
Penguinsare under much more severetime
smallestcolonies.Yet, Barrat (1976) and Olsson
(1998) obtainedsimilar resultsto ours in King
Penguincoloniesof different sizes(29% mate
retentionin a 56,000-paircolonyand 19%in a
colonyof 150individuals,respectively;
dataon
colonysize in Voisin[1971]and Olsson[1998]).
Anotherconsequence
is that divorcewouldbe
no more than a by-product,with divorcedindividualsmaking the bestof a bad situation.
Divorce and mate choice.--We failed to find an
advantageof mate retention or a cost of divorce. Furthermore, the combination of factors
notedabovewasinsufficientto explainthehigh
incidenceof divorcewhenasynchrony
waslow.
Olsson(1998) explainedthis phenomenonby
speculatingthat many birds previouslyhad
mated with a lower-qualitypartner than they
couldhaveobtainedhad theymanagedearlier
to storeenoughfat prior to the fastingperiod;
under theseconditions,divorcewould be adaptive. Olsson(1998) predictedthat, in the absenceof time constraints
causedby thefat-storageproblem,birdswould choosea partnerof
ashigh a qualityaspossiblein an "ideal-free"
manner (Fretwell and Lucas 1970). Olsson
(1998)suggestedthat the absenceof territorial
behaviorin King Penguinswould enableindividualsto assess
potentialpartnersrapidly and
with low costwhen movingthroughthe colony. Thus,they couldchoosethe mostsuitable
mate as long as they could afford to sample
mates,becauseof fat-storingconstraints.
These
predictionssupportedthe "better-option"hypothesis(Ens et al. 1993, Choudhury 1995),
whichstatesthatonememberof a pair initiates
510
BRIED,JIGUET,
ANDJOUVENTIN
[Auk, VoL 116
divorceif it hasthe opportunityto improveits patibility" hypothesis(Coulson1966,Rowley
reproductivesuccessby obtaininga higher- 1983).Yet,it shouldbe moreinterestingto test
this hypothesisusing the true breedingexpequality mate.
Our resultssuggestthat mate quality was rience(i.e. that sinceindividualshaveentered
not linkedto returndatefor high-qualityKing the breedingpopulation)combinedwith qualPenguins,althoughthe latter tendedto arrive ity. The behavioralplasticityof Aptenodytes
with predictionsof
first and to havethehighestbreedingsuccess. penguinsis in accordance
The fact that these tendencies were not statisthe "better-option"hypothesis,as previously
for King Penguinsby Olsson(1998).
tically significantmay be explainedby small suggested
the latest-arrivinginsamplesize.In contrast,high-qualityindivid- Our resultsconcerning
uals were particularly attractivefor low-quali- dividualscan be explainedby the "musicalty ones,which had more difficulty obtaining chairs"hypothesis,whichstatesthat individa King
them as partnersas time elapsed.Yet, late ualssettleonthebestterritoryavailable;
breedingincreases
theprobabilityof failure,in- Penguinreturning too late will find its previdependentof quality(Olsson1996).Therefore, ousbreedingarea occupiedand will have to
our results are consistent with the "ideal-free"
settle elsewherein the colony(Barrat 1976).
predictsthat divorce"may be
mate-choice
hypothesis.However,the propor- Thishypothesis
tion of high-qualityindividuals and evenly a side-effect of differential arrival of the sexes"
matchedpartnersmust not vary greatly be- (Choudhury1995).In the EmperorPenguin,
tween different colonies,as suggestedby di- maleswould replaceterritoriesas "chairs,"at
vorceratessimilarto oursin SouthGeorgiaand least in some cases.
in Barrat's(1976)colony.In the moresynchro- In most cases,however,accessto potential
nouslybreedingEmperorPenguin,the lackof partners doesnot seemvery difficult nor time
data on individual quality precludesfirm con- consumingfor King Penguinsand Emperor
clusions.Yet,the absence
of territorialityreach- Penguins,whichhave to facetwo conflicting
(1) theyhavelongbreedingcycles
es its highestlevelin this species(Stonehouse constraints:
1953);breederswalk with theireggor chickon relativeto theirlargebodysize(Stearns1992);
isseverely
contheir feet and congregate
in "huddles"when and(2) theirbreedingschedule
the weatherbecomesespeciallyharsh(Pr•vost strainedsuchthattheymustsaveasmuchtime
1961, Isenmann1971). Thus, searchingfor a aspossibleto rear their chickwithin the limits
conditions.
In lightof this
new partnershouldnot be very costlyfor this setby environmental
specieseither Moreover,the numberof male scenario,Olsson(1998)may not havedevoted
partners available per unpaired female de-
sufficient attention to the role of the absence of
creasesas time elapses,which enabledIsen- nestingsitesand territorialbehavioron mate
retention.Hence,we suggestthat divorceis
penguins,not only beunpairedfemalessimultaneously
by usingthe commonin Aptenodytes
in theabsence
playbackof a male'scallsduring the last days causeit is notcostly,butbecause
of
nest
sites
that
serve
as
meeting
points(e.g.
of the courtshipperiod.At this time, thesefeHinde
1956,
Morse
and
Kress
1984),
mate remales probablywould have paired with the
penfirst available male. Consequently,Emperor tentioncouldbe maladaptive.Aptenodytes
Penguinsmay alsoperformmatechoicein an guinsseemto have adoptedan "optimal divorce" strategy (McNamara and Forslund
"ideal-fred'
manner Our conclusions are consistentwith Olsson's(1998).In bothspeciesof 1996)thatenablesthemto adapttheirbreeding
Aptenodytes
penguins, only some individuals cyclesto seasonalchangesin their environment.
(probablythelatestarrivals)wouldseeka partner, not to improve their breedingsuccess
ACKNOWLEDGMENTS
(whichhasa greaterchanceto decrease
astime
elapses),but to limit the risk of not breeding
We thank the Institut Fran•aispour la Recherche
altogether.
et la Technologie
Polairesand theTerresAustraleset
Conclusion:
Why is divorceso common?--We AntarctiquesFran•aisesfor financial and logistical
failed to discovera link amongdivorce,breed- support, respectively.We are indebted to P. Isening experience,
andbreedingfailurein thepre- mannfor kindlyprovidingdatafromhis 1968study.
viousyear, giving no supportto the "incom- We alsothankM. Salamolard,E Lagarde,F.Cu•notmann and Jouventin(1970) to attract up to 20
April 1999]
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in Penguins
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