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TheAdaptiveSignificanceofSiblicideinNazcaBoobies

AnnikkaFrostad‐Thomas

Darwin,Evolution,andGalápagos

Fall2009

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Introduction

Galapagosishometoanincrediblecollectionofseabirds,manyfoundnowhereelseinthe

world.Onesuchbird,theelegantandslightlycomicalNazcabooby,isoneofthreeboobyspeciesfound

inthearchipelago.Itistheboobyyouaresecondmostlikelytoseewhenvisiting,andthereare

between25,000and50,000breedingpairslivingonlyonEspanola,SanCristobal,andGenovesa.Nazca

boobiesfeedprimarilyonfishandplungediveoffshorefromheightsofupto328feet,gracefully

collapsingtheirwingsatthelastmomentbeforetheyenterthewater(Kricher2006:108).Unlikeitsred

andblue‐footedcousins,theNazcabooby’sfeetarenotvibrant,butratheraplainolive.Whatever

beautytheirfeetmaylackismorethanmadeupforbypristinewhitebodyfeathers,andwingsandtail

rimmedwithpureblackplumage.

AselegantastheadultNazcaboobyis,asachickitexhibitssomeratherunsightlybehavior—

murder.Withoutfail,Nazcaboobiesareobligatelysiblicidal;theirnormaltwo‐eggclutchisalways

reducedtoonebyeitherunsuccessfulhatchingofoneegg,orsiblicidalaggressionoftheolderchick

(Anderson1990b:346).ThisstrangebehaviorisnotuniquetotheNazcaboobyspecies,blue‐footed

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boobychickssometimesexhibitsiblicide,buttheconditiondoesbringupsomeinterestingquestions.In

particular,whyhassiblicideevolvedinthisspecies,andgiventhatithas,whydoNazcaboobiesstilllay

twoeggs?Fortunately,theNazcaboobyhasbeenthecentralobjectofstudyforDavidAndersonfor

morethantwodecades,andthereisdataavailableoninvestigationsintothemanyhypotheses

regardingsiblicideinthisspecies.Afewareunsupported,someseemfairlylikely,butthereisstillno

concreteevidence,anditisunlikelywecaneverknowtheexactevolutionaryhistoryofsiblicide.

Theevolutionofsiblicide

ANazcaboobynestconsistsofarelativelyflatcircularareaclearedofdebrismarkedbyasimple

guanoring,Nazcasdonotdigoutaslightbowl‐shapeddepressionlikeblue‐footedboobiesdo,nordo

theyuseanysortofextranestingmaterialtoprotectorinsulatetheeggs(Anderson1995:864).Nazca

boobieslaytheirfirsteggontheirbaregroundnestandimmediatelystartincubating,layingtheusual

secondeggfourtoninedayslater(Clifford2002:275).Thislayingasynchronyisdirectlyproportionalto

thehatchingasynchronyoftheeggs,whichis“amongthelongestofallbirds…resulting[in]sizeand

developmentaldisparities”(Clifford2002:374).Bythetimethesecondchickisborn,thefirst‐bornchick

orAchickissignificantlylargerthanthesecond‐bornbecauseithashadseveraldaysoffeedingand

growing(Kricher2006:310).Thesizedifferencethatresultsfromhatchingasynchronyisadeath

sentencefortheBchickbecauseitmakesitmucheasierfortheAchicktoexpelitby“graspinginits

beakthesiblingsneck,appendage,orskinandextendingitsnecktothrusttheB‐chickacrossthenest

scrape.”Thegraphbelowclearlyshowsthesharpdeclineindaysittakesforbroodreductionasthe

hatchingasynchronyincreases.Onceachickisoutofthenestscrapetheparentboobieswillnot

acknowledgeit,anditwilldiequicklyeitherbypredation,starvation,ortemperaturechange(Anderson

1995:861‐862).

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Anderson1988

ThebehaviorofNazcaboobychicksisconsideredsiblicidebecauseit“makesadirectand

significantcontributiontotheimmediatedeathofasiblingnestmate,”butitisimportanttodistinguish

itfromtheformofsiblicidepresentinanotherGalapagosboobyspecies.Inblue‐footedboobybroods,

chicksaresiblicidalonlyifthereisnotenoughfood,andthisiscalledfacultativesiblicidebecauseitis

“conditionalontheperpetrator’simmediateecologicalandphysiologicalsituation.”Bycontrast,Nazca

boobysiblicideisobligate,meaningthatitdoesnotdependonecologicalconditions,butis“persistent

[and]unconditional”(Anderson1990b:337‐338).

Theimmediatequestionthatfollowsishowsuchabarbaric,andseeminglydetrimental,

behaviorevolvedinthisavianspecies.ThesiblicidalnestlinglosesinclusivefitnesswhenitkillstheB

chickbecauseitsharesonaveragehalfofitsgeneswithitssibling,sotheremustbesomegainindirect

fitnessotherwisethisbehaviorwouldnothaveevolved.Onehypothesiswhichwouldseemtonicely

explainthisbehaviorisrecurrentfoodscarcity,becausethegrowingAchickwouldhaveunhindered

accesstoparentalresourcesonceitkilleditsnestmate,andwouldhaveasurvivalandreproductive

advantagebydevelopingonschedule.DavidAndersonandhisresearchteamtestedthishypothesisby

experimentallydoublingNazcaboobybroodstoseewhetherornottheparentscouldactuallyprovide

enoughfoodtofeedtwogrowingchicks.Theirprocedurewastotakeeggsfromdifferentneststhat

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werelaidatthesametimeandputtheminthesamenesttoseeiftheparentswouldbeabletofeed

both,andthesewerecomparedtocontrolgroupsofsingle‐eggnests.Itwasnecessarytoexperimentally

doublethebroodsbecausethatwaytherewouldbelittletonohatchingasynchrony,andconsequently

thechickswouldbelesslikelytosucceedinexpellingoneanotherfromthenestscrape.Theresults

werethatparentswithtwochicksinthenestincreasedtheirforagingeffortsandwereabletokeeptwo

chicksfed.Atpeakfoodintake,doubledbroodsgotonly41%morefoodthansingletons,whichledthem

tobeslightlysmallerwithage,butstillarelativelyhealthysize(Anderson1990a:2073).

Anderson1990

Eventhoughthedoubledbroodshadchicksthatwereaprettyhealthysize,theydidhavea

highermortalityratethansinglechicks,meaningthateventhoughthereisnotcurrentlyenoughfood

scarcitytonecessitatesiblicide,atsomepointinthepasttheremayhavebeenastrongenoughpressure

toevolveobligatesiblicide(Anderson1990a:2074,2077).Itiseasiesttothinkoftheevolutionof

obligatesiblicideastheinvasionofanallelewhosephenotypeissiblicidalbehavior.Duringatimeof

strongselectionpressuretoexcludenestmatesfromthelimitedfoodsource,achickbornwiththe

alleleforsiblicidalbehavior(asaresultofgeneticmutation)wouldbeatanadvantage,andthisallele

couldquicklyinvadeapopulation(Anderson1990a:2078).Oncethepopulationsis“fixedonthe

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siblicidalstrategy…thenonsiblicidalstrategycouldnotinvade[because]mostbroodscontaininga

nonsiblicidalAchickshouldalsocontainasiblicidalBchick,”thereforeeventhoughthereisapparently

nolongeranystrongselectionpressureforsiblicideitpersistsbecausethenonsiblicidalallelecannot

reinvade(Anderson1990a:2079).

OnestudydoneduringthesiblicidalagerangeofNazcaboobies(zerotosevendays)aimedto

findouthowthreehormonesgenerallyrelatedtoaggressionanddevelopmentinotheranimalsrelated

tosiblicideinNazcaboobies.Thethreehormonesstudiedwerepickedbecausetestosteroneis“often

involvedinaggressivebehaviorofvertebrateanimals,”andprogesteroneandcorticosterone“maybe

invovldedinbodymassregulations…[which]typicallyinfluencestheoutcomeofaggressivecompetition

amongnestingbirds”(Tarlow2001:14‐15).Theresearcherspredictedthattestosteronewasresponsible

forthedirectregulationofsiblicidalbehaviorandthatprogesteroneandcorticosteroneprovidedthe

developmentaladvantage(specificallyarapidincreaseinbodymassrelativetolength)thatenabledthe

successofthesiblicidalbehavior.Whattheyfoundwasthatyoungchicks“showedendocrinechanges

consistentwiththehypothesisthatsteroidhormonesmaybeinvolvedintheregulationoffatalsocial

interactions.”ThelevelsofCORTandPshowapreliminarycorrelationtotheincreaseintheAchick’s

bodymasswhenithasasecond‘challenge’eggitsharethenestwith.Animportantpartofalarger

chartisshownherethatillustratestheoveralllevelsoftestosteroneforyoungchicks.AspredictedAis

highest,buttheoneaboveBisasamplethatwastaken

duringanaggressivesiblicidalact(theonlyobservedcase

ofaBchickejectinganAchicksuccessfully)

andindicatesthat“thesecretionof[testosterone]maybe

adirect,butshortduration,responsetoasocialchallenge

(Tarlow2001:15‐19).Overall,hormonalcorrelatesneedtoberesearchedfurthertodeterminetheir

exactroleinsiblicideofNazcaboobies.

Hormones2001

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Thepersistenceoftwo‐eggclutches

ItisclearfromthecurrentstateofsiblicideinNazcaboobiesandtheapplicationof

gamestheorydescribedabovethatNazcaboobiesarehighlyunlikelytoeverreverseto

nonsiblicidalbehavior.Whenthisfactsettlesin,itstirsupanotherveryimportantquestion:

whydoNazcaboobiesstilllaytwo‐eggclutcheseventhoughtheyonlyeverhaveonechick?

Thefirstpossibleexplanationisthattheymightactuallybeinthemiddleofevolutiontoward

one‐eggclutches,asitseemsthatparentswouldhaveahigherfitnessbynotwastingenergyon

asecondeggthatwillnotresultinafledgling.Thiswastestedbyobservinghowmanyclutches

arenaturallyoneortwoeggs.Thepercentagefluctuatesfromyeartoyear,inthechartbelow

threeconsecutiveyearsareshownandthelastshowsmoreone‐eggthantwo‐eggclutches.

However,1986wasanElNinoyear,meaningthat

foodfortheNazcaboobywasprobablyscarce.To

testthehypothesisthatfoodscarcitycausesthe

unusuallyhighamountofone‐eggclutches,mothers

weresupplementedfoodtoseeiffoodintake

affectedclutchsize.Theresultswerethat92%ofsupplementedfemaleslaidtwoeggs,andonly

70%ofcontrolfemaleslaidtwoeggs,suggestingthattheoptimumclutchsizeforNazca

boobiesremainstwo,despitetheevolutionofsiblicide(Clifford2002:278).

Iftwo‐eggclutchescontinuetobefavored,thentheremustbesomereproductive

advantagetohavingtwoeggsdespitethattheextracostofthesecondeggdoesnotresultina

secondsurvivingchick.Therearethreehypotheseshereexploredthataimtoexplainwhatthis

Anderson1990b

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advantagemightbe,theIceboxBenefitHypothesis,theProgenyChoiceBenefitHypothesis,and

theInsurance‐EggHypothesis.TheIceboxBenefitHypothesisassumesthattheBchickis

essentiallyastoreoffreshfoodfortherestofthefamilyandthatfamilieswiththisextrafood

haveareproductiveadvantageoverfamilieswithoutaBchickduringtimesoffoodshortage

(Boag2005:381).Therehasneverbeenanobservedcaseofwithin‐familycannibalisminNazca

boobies,andevenBchicksthatdiewithinthenestscrapearesimplyleftuntiltheyare

“eventuallygroundintothenestsubstrate.”Bchicksthatareejectedfromthenestusuallydie

ofpredationbyotheranimalssuchasSallyLightfootcrabs,starvation,andinonlyoneobserved

case,cannibalismbyaneighboringunrelatedadultNazcabooby(Boag2005:385‐386).Because

ofthelackofanyevidencethatsupportswithin‐familycannibalismatanytime,theIcebox

BenefitHypothesisisprettycertainlynottheexplanationforthepersistenceoftwo‐egg

clutches.

TheProgenyChoiceBenefitHypothesisassumesthattheBchickwilllivelongenoughto

competewiththeAchickforthepermanentspotinthebrood,andalsoassumesthat

sometimestheBchickwillwin.Thiscompetitionwouldresultinthestrongestchicksurviving,

meaningthattheparentshaveincreasedreproductivefitnessbyraisingthechickthatismost

likelytocontinuethegeneticline(Boag2005:381).However,thechartbelowshowsthatthe

averagecohabitationtimeisveryshort,infact,“broodreductionoccurredwithin10daysofthe

[B]chick’shatchinginallnestsexceptone,”andduringthistendayperiodtheBchickisso

smallandfrailthatitcouldhardlybeanyrealchallengetotheAchick.Onlyonecaseoutof

1,901reallysupportstheProgenyChoiceBenefitHypothesis,soitisalsonotlikelyasthe

explanationforcontinuingtwo‐eggclutches(Boag2005:387).

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Humphries2005

ThethirdhypothesisinvestigatedhereistheInsurance‐EggHypothesis,whichassumes

thatthereproductivefitnesscostoflayingtheBeggislessthanitsininsurancevalueinthe

eventthattheAchickshouldeitherfailtohatchordiebeforetheBchickhatches(Evolution

1990b:337).Also,theInsuranceEggHypothesis“predictsthattwo‐eggclutchesshouldalways

yeiedhigherreproductivesuccessthandoone‐eggclutches”(Clifford2001:341).Researchers

recordedthehatchingandfledgingsuccessesofnaturaloneandtwo‐eggclutchestoseeif

therewasindeedareproductiveadvantagetolayingasecondegg.Theyfoundthattherewas

aninsignificantdifferenceinhatchingsuccessofindividualeggsbetweentheclutchsizes,but

thatthetwoeggclutcheshada“higherprobabilityofhatchingatleastonechick”(Anderson

1990b:343).Thishigherprobabilityofhatchingatleastonechickfromatwo‐eggclutchshows

areproductiveadvantage,butfortheInsuranceEggHypothesis,thecostoflayingtheeggmust

belessthanthisgain.ThecostoflayinganegghasnotbeendeterminedinNazcaboobies,but

fortherelatedred‐footedboobyithasbeendeterminedtobeanaveragedailyinvestmentof

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1%‐2.4%ofthebooby’sdailyenergyexpenditure(Anderson1990b:344).ThefactthatBeggs

“contributedthesurvivinghatchlingin19.2%of…two‐eggclutches”showsthatthereisa

significantadvantagetotwoeggsthatoutweighstheparentalinvestmentoflayingtheegg(itis

importanttonotethattheBegghatchlingsurvivorsdidnotkilltheAchick,theysurvivedafter

eithertheAchickfailedtohatchordiedbeforetheBchickhatched)(Anderson1990b:342).

Thechartbelowillustratesthatnotonlywastheprobabilityoffledginghigherinnaturaltwo‐

eggclutches,butwasalsohigherinexperimentallydoubledclutchesthanreducedclutches,

consistentwiththeInsuranceEggHypothesis’predictionthattwoeggsshouldalwaysbe

advantageous(Clifford2001:340).

Clifford2001

Conclusions

Wewillprobablyneverbeabletodetermineexactlywhatcausedobligatesiblicideto

evolveinNazcaboobies,butthemostpromisingexplanationseemstobethatsomepast

selectionpressure,probablyfoodscarcity,causedasiblicidalalleletoinvadethepopulation

thatcannotrevertevennowthattheselectionpressureisgoneandparentsareabletoforage

fortwochicks.Throughtheinvestigationofseveralhypotheses,itappearsmostlikelythatthe

Nazcaboobiesoptimumclutchsizecontinuestobetwodespitetheeffectsofsiblicidebecause

theBeggprovidesasignificantinsurancevalueagainsttheprematurefailureoftheAeggor

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chick.Somefurtherresearchisneededbothtounderstandthemechanismsthatcontrol

siblicideandwhytheBeggisneededasinsurance.Hormonalcorrelateshavebeen

preliminarilyinvestigated,butitisstillunclearwhyboobieshavesuchalowhatchingsuccess

thattheyneedtwoeggs.Nazcaboobies“hatch51%‐61%oftheireggs,whereassingle‐egg

[obligatelysiblicidal]speciesallhatchatleast85%oftheireggs.”Thisisonepossibleareaof

furtherresearchbecause“themajorityofunhatchedeggscontainnovisibleembryo,indicating

thatembryosdiedshortlyafterfertilizationorwereneverfertilized”;eithertheground

temperatureofthenestscrapeisabovethelethaltemperatureforavianembryos,orNazca

boobyinfertilityis“exceptionallyhigh,”eitherofwhichwouldbefascinatingareasforfurther

research(Anderson1990b:343‐345).

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Bibliography

*AllpicturestakenbyAnnikkaFrostad‐Thomasexcepttheonemarkedwithabluestarinthe

corner,whichisfromanowbrokenwebsitewhichcanonlybeaccessedat

<http://74.125.155.132/search?q=cache:C01bYGI2_NgJ:www.v‐

liz.com/galapagos/murder.htm+nazca+booby+chick+pushes&cd=4&hl=en&ct=clnk&gl=us&clien

t=firefox‐a>.

Anderson,DJ."Theroleofhatchingasynchronyinsiblicidalbroodreductionoftwobooby

species."BehavioralEcologyandSociobiology25.5(1989):363‐368.JSTOR.Web.5

Sept.2009.<http://www.jstor.org/stable/pdfplus/4600352.pdf>.

Anderson,DavidJ."TheRoleofParentsinSibilicidalBroodReductionofTwoBoobySpecies."

Auk12.4(1995):860‐869.JSTOR.Web.5Sept.2009.

<http://www.jstor.org/stable/pdfplus/4089018.pdf>.

Anderson,DavidJ."EvolutionofObligateSiblicideinBoobies.2:FoodLimitationandParent‐

OffspringConflict."Evolution44.8(1990):2069‐2082.JSTOR.Web.5Sept.2009.

<http://www.jstor.org/stable/pdfplus/2409616.pdf>.

Anderson,DavidJ."EvolutionofObligateSiblicideinBoobies.1.TestoftheInsurance‐Egg

Hypothesis."AmericanNaturalist135.3(1990):334‐350.JSTOR.Web.5Sept.2009.

<http://www.jstor.org/stable/pdfplus/2462250.pdf>.

Boag,PeterT,andDavidJAnderson."Contributionsofmarginaloffspringtoreproductive

successofNazcabooby(Sulagranti)parents:testsofmultiplehypotheses."Wilson

13|P a g e

JournalofOrnithology118.2(2006):244‐247.BioOne.Web.7Sept.2009.

<http://www.bioone.org/doi/pdf/10.1676/05‐106.1>.

Clifford,LD,andDJAnderson."ClutchsizevariationintheNazcabooby:atestoftheegg

qualityhypothesis."BehavioralEcology13.2(2002):274‐279.Web.Sept.2009.

<http://beheco.oxfordjournals.org/cgi/reprint/13/2/274>.

Clifford,LD,andDJAnderson."Experimentaldemonstrationoftheinsurancevalueofextra

eggsinanobligatelysiblicidalseabird."BehavioralEcology12.3(2001):340‐347.Web.

7Sept.2009.<http://beheco.oxfordjournals.org/cgi/reprint/12/3/340>.

Clifford,LD,andDJAnderson."FoodlimitationexplainsmostclutchsizevariationintheNazca

booby."JournalofAnimalEcology70(2001):539‐545.Web.5Sept.2009.

<http://www.wfu.edu/~djanders/labweb/reprints/Clifford%20and%20Anderson%20JAE

%202001.pdf>.

Tarlow,ElisaM,MartinWikelski,andDavidJAnderson."HormonalCorrelatesofSiblicidein

GalapagosNazcaBoobies."HormonesandBehavior40(2001):14‐20.Web.5Sept.

2009.<http://www.princeton.edu/~wikelski/Publications/HormBehav40.pdf>.