The Adaptive Significance of Siblicide in Nazca Boobies Annikka Frostad Thomas Darwin, Evolution, and Galápagos Fall 2009
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1 TheAdaptiveSignificanceofSiblicideinNazcaBoobies AnnikkaFrostad Thomas Darwin,Evolution,andGalápagos Fall P a g e
2 Introduction Galapagos is home to an incredible collection of seabirds, many found nowhere else in the world. One such bird, the elegant and slightly comical Nazca booby, is one of three booby species found in the archipelago. It is the booby you are second most likely to see when visiting, and there are between 25,000 and 50,000 breeding pairs living only on Espanola, San Cristobal, and Genovesa. Nazca boobies feed primarily on fish and plunge dive offshore from heights of up to 328 feet, gracefully collapsing their wings at the last moment before they enter the water (Kricher 2006: 108). Unlike its red and blue footed cousins, the Nazca booby s feet are not vibrant, but rather a plain olive. Whatever beauty their feet may lack is more than made up for by pristine white body feathers, and wings and tail rimmed with pure black plumage. As elegant as the adult Nazca booby is, as a chick it exhibits some rather unsightly behavior murder. Without fail, Nazca boobies are obligately siblicidal; their normal two egg clutch is always reduced to one by either unsuccessful hatching of one egg, or siblicidal aggression of the older chick (Anderson 1990b: 346). This strange behavior is not unique to the Nazca booby species, blue footed 2 Page
3 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: ). 3 P a g e
4 Anderson1988 ThebehaviorofNazcaboobychicksisconsideredsiblicidebecauseit makesadirectand significantcontributiontotheimmediatedeathofasiblingnestmate, butitisimportanttodistinguish itfromtheformofsiblicidepresentinanothergalapagosboobyspecies.inblue footedboobybroods, chicksaresiblicidalonlyifthereisnotenoughfood,andthisiscalledfacultativesiblicidebecauseitis conditionalontheperpetrator simmediateecologicalandphysiologicalsituation. Bycontrast,Nazca boobysiblicideisobligate,meaningthatitdoesnotdependonecologicalconditions,butis persistent [and]unconditional (Anderson1990b: ). Theimmediatequestionthatfollowsishowsuchabarbaric,andseeminglydetrimental, behaviorevolvedinthisavianspecies.thesiblicidalnestlinglosesinclusivefitnesswhenitkillstheb chickbecauseitsharesonaveragehalfofitsgeneswithitssibling,sotheremustbesomegainindirect fitnessotherwisethisbehaviorwouldnothaveevolved.onehypothesiswhichwouldseemtonicely explainthisbehaviorisrecurrentfoodscarcity,becausethegrowingachickwouldhaveunhindered accesstoparentalresourcesonceitkilleditsnestmate,andwouldhaveasurvivalandreproductive advantagebydevelopingonschedule.davidandersonandhisresearchteamtestedthishypothesisby experimentallydoublingnazcaboobybroodstoseewhetherornottheparentscouldactuallyprovide enoughfoodtofeedtwogrowingchicks.theirprocedurewastotakeeggsfromdifferentneststhat 4 P a g e
5 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 5 P a g e
6 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 Hormones2001 (Tarlow2001:15 19).Overall,hormonalcorrelatesneedtoberesearchedfurthertodeterminetheir exactroleinsiblicideofnazcaboobies. 6 P a g e
7 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 Anderson1990b affectedclutchsize.theresultswerethat92%ofsupplementedfemaleslaidtwoeggs,andonly 70%ofcontrolfemaleslaidtwoeggs,suggestingthattheoptimumclutchsizeforNazca boobiesremainstwo,despitetheevolutionofsiblicide(clifford2002:278). Iftwo eggclutchescontinuetobefavored,thentheremustbesomereproductive advantagetohavingtwoeggsdespitethattheextracostofthesecondeggdoesnotresultina secondsurvivingchick.therearethreehypotheseshereexploredthataimtoexplainwhatthis 7 P a g e
8 advantagemightbe,theiceboxbenefithypothesis,theprogenychoicebenefithypothesis,and theinsurance EggHypothesis.TheIceboxBenefitHypothesisassumesthattheBchickis essentiallyastoreoffreshfoodfortherestofthefamilyandthatfamilieswiththisextrafood haveareproductiveadvantageoverfamilieswithoutabchickduringtimesoffoodshortage (Boag2005:381).Therehasneverbeenanobservedcaseofwithin familycannibalisminnazca boobies,andevenbchicksthatdiewithinthenestscrapearesimplyleftuntiltheyare eventuallygroundintothenestsubstrate. Bchicksthatareejectedfromthenestusuallydie ofpredationbyotheranimalssuchassallylightfootcrabs,starvation,andinonlyoneobserved case,cannibalismbyaneighboringunrelatedadultnazcabooby(boag2005: ).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). 8 P a g e
9 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 9 P a g e
10 1% 2.4%ofthebooby sdailyenergyexpenditure(anderson1990b:344).thefactthatbeggs contributedthesurvivinghatchlingin19.2%of two eggclutches showsthatthereisa significantadvantagetotwoeggsthatoutweighstheparentalinvestmentoflayingtheegg(itis importanttonotethatthebegghatchlingsurvivorsdidnotkilltheachick,theysurvivedafter eithertheachickfailedtohatchordiedbeforethebchickhatched)(anderson1990b:342). Thechartbelowillustratesthatnotonlywastheprobabilityoffledginghigherinnaturaltwoeggclutches,butwasalsohigherinexperimentallydoubledclutchesthanreducedclutches, consistentwiththeinsuranceegghypothesis predictionthattwoeggsshouldalwaysbe advantageous(clifford2001:340). Conclusions Clifford2001 Wewillprobablyneverbeabletodetermineexactlywhatcausedobligatesiblicideto evolveinnazcaboobies,butthemostpromisingexplanationseemstobethatsomepast selectionpressure,probablyfoodscarcity,causedasiblicidalalleletoinvadethepopulation thatcannotrevertevennowthattheselectionpressureisgoneandparentsareabletoforage fortwochicks.throughtheinvestigationofseveralhypotheses,itappearsmostlikelythatthe Nazcaboobiesoptimumclutchsizecontinuestobetwodespitetheeffectsofsiblicidebecause thebeggprovidesasignificantinsurancevalueagainsttheprematurefailureoftheaeggor 10 P a g e
11 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: ). 11 P a g e
12 Bibliography *AllpicturestakenbyAnnikkaFrostad Thomasexcepttheonemarkedwithabluestarinthe corner,whichisfromanowbrokenwebsitewhichcanonlybeaccessedat < t=firefox a>. Anderson,DJ."Theroleofhatchingasynchronyinsiblicidalbroodreductionoftwobooby species."behavioralecologyandsociobiology25.5(1989): JSTOR.Web.5 Sept.2009.< Anderson,DavidJ."TheRoleofParentsinSibilicidalBroodReductionofTwoBoobySpecies." Auk12.4(1995): JSTOR.Web.5Sept < Anderson,DavidJ."EvolutionofObligateSiblicideinBoobies.2:FoodLimitationandParent OffspringConflict."Evolution44.8(1990): JSTOR.Web.5Sept < Anderson,DavidJ."EvolutionofObligateSiblicideinBoobies.1.TestoftheInsurance Egg Hypothesis."AmericanNaturalist135.3(1990): JSTOR.Web.5Sept < Boag,PeterT,andDavidJAnderson."Contributionsofmarginaloffspringtoreproductive successofnazcabooby(sulagranti)parents:testsofmultiplehypotheses."wilson 12 P a g e
13 JournalofOrnithology118.2(2006): BioOne.Web.7Sept < >. Clifford,LD,andDJAnderson."ClutchsizevariationintheNazcabooby:atestoftheegg qualityhypothesis."behavioralecology13.2(2002): Web.Sept < Clifford,LD,andDJAnderson."Experimentaldemonstrationoftheinsurancevalueofextra eggsinanobligatelysiblicidalseabird."behavioralecology12.3(2001): Web. 7Sept.2009.< Clifford,LD,andDJAnderson."FoodlimitationexplainsmostclutchsizevariationintheNazca booby."journalofanimalecology70(2001): Web.5Sept < % pdf>. Tarlow,ElisaM,MartinWikelski,andDavidJAnderson."HormonalCorrelatesofSiblicidein GalapagosNazcaBoobies."HormonesandBehavior40(2001):14 20.Web.5Sept < 13 P a g e
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