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ARTICLE Isotopicevidenceforinitialcoastalcolonizationand subsequentdiversi cationinthehumanoccupation ofWallaceaPatrickRoberts 1,2 ,JulienLouys 3,JanaZech1,CeriShipton 4,5,ShimonaKealy 4,5, So aSamperCarro4,6,StuartHawkins4,5,ClaraBoulanger 5,7,SaraMarzo1,BiancaFiedler1,NicoleBoivin1, Mahirta5,8,KenAplin4,9&SueO Connor 4,5Theresource-poor,isolatedislandsofWallaceahavebeenconsideredamajoradaptive obstacleforhomininsexpandingintoAustralasia.Archaeologicalevidencehashintedthat coastaladaptationsin Homosapiens enabledrapidislanddispersalandsettlement;however, therehasbeennomeanstodirectlytestthisproposition.Here,weapplystablecarbonand oxygenisotopeanalysistohumanandfaunaltoothenamelfromsixLatePleistoceneto HolocenearchaeologicalsitesacrossWallacea.Theresultsdemonstratethattheearliest humanforagerfoundintheregion c .42,000yearsagomadesigni cantuseofcoastal resourcespriortosubsequentnichediversi cationshownforlaterindividuals.Wearguethat ourdataprovidesclearinsightsintothehugeadaptive exibilityofourspecies,includingits abilitytospecializeintheuseofvariedenvironments,particularlyincomparisontoother homininspeciesknownfromIslandSoutheastAsia. https://doi.org/10.1038/s41467-020-15969-4 OPEN 1DepartmentofArchaeology,MaxPlanckInstitutefortheScienceofHumanHistory,07745Jena,Germany.2SchoolofSocialScience,TheUniversityof Queensland,StLucia,QLD4072,Australia.3AustralianResearchCentreforHumanEvolution,EnvironmentalFuturesResearchInstitute,Grif thUniversity, Nathan,QLD4111,Australia.4SchoolofCulture,HistoryandLanguage,CollegeofAsiaandthePaci c,TheAustralianNationalUniversity,Canberra,ACT 2600,Australia.5ARCCentreofExcellenceforAustralianBiodiversityandHeritage,AustralianNationalUniversity,Canberra,ACT2600,Australia.6Centre d ’ EstudisdelPatrimoniArqueologic,FacultatdeLletres,UniversitatAutònomadeBarcelona,08193Bellaterra,Spain.7MuséumNationald ’ HistoireNaturelle, DépartementHommeetEnvironment,CNRSUMR7194,HistoireNaturelledel ’ HommePréhistoriqueParis,France.8DepartmentofArchaeology, UniversitasGadjahMada,Yogyakarta55281,Indonesia.9Deceased:KenAplin. email: roberts@shh.mpg.de ; sue.oconnor@anu.edu.auNATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications1 1234567890():,;
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Recent,high-pro lestudiesofsymbolicmaterialculture (e.g.,ref.1),technologicalcomplexity(e.g.,ref.2),fossil morphologyandchronology(e.g.,ref.3),andgenetics4are demonstratinganincreasinglycomplexanddynamicpictureof thecapacitiesandinteractionsofdifferenthomininpopulations intheLatePleistocene(126 – 12ka),particularlyinAsia.Ifweare todeterminethe ‘ uniqueness ’ of Homosapiens ,thelastextant homininonthefaceoftheplanet,itisbecomingapparentthatwe mustexaminehowitsecologicaladaptationsdifferedfromthose ofothermembersofthegenus Homo5 , 6.Ithasbeensuggested thatLatePleistocenepopulationsof H.sapiens expandingacross theglobewereabletonotonly exiblyexploitvaried,andoften extreme,environments — includingdeserts,tropicalrainforests, high-altitudesettings,anddeep-seamaritimehabitats — butalso specializeintheoccupationofthem,enablingourspeciesasa wholetoproliferateevenwhilelocalcommunitiesmaysometimes havefailed6.Bycontrast,earlierandcontemporaneous Homo speciesexpandingintoEurasiaintheEarlyandMiddlePleistocene(2.6Ma – 126ka)madegeneralizeduseofforestandgrasslandmosaics7 , 8,potentiallymakingthemvulnerabletomore extremeLatePleistoceneenvironmentalchanges(e.g.,ref.3)and unabletosurviveonislandsdepauperateinlargeterrestrial fauna9. Testingthishypothesisisparticularlytimelygivenrecent nds thatimplyotherhomininspeciesmayhaveventuredintochallengingadaptivesettings4 , 10.Wallaceaprovidesanideal ‘ island laboratory ’ settinginwhichtodosointheincreasingly palaeoanthropologicallysigni cantSoutheastAsianregion.Wallaceaisanisolatedseriesofislandsthatwasneverconnectedto theneighboringPleistocenelandmassesofSundaorSahul, necessitatingwatercrossingstoreach9 , 11 – 15.Theseislandshave beenhypothesizedashostingdepauperateislandforest environments,lackinginreliableterrestrialproteinandcarbohydrateresources13 , 16 , 17.Signi cantly,whiletheseislandsarehome tosomeoftheearliest rmevidencefor H.sapiens eastofAfrica andtheMiddleEastc.45ka(refs.13 , 18 , 19),fossilandartifact nds havealsosuggestedthepresenceofearliermembersofthegenus Homo ontheislandofFloresfrom~1Ma(refs.20 , 21),Luzonfrom 0.7Ma(ref.22),andSulawesifrom~0.2Ma(ref.23).Although zooarchaeologicalrecordshaveprovidedsomeinsightsintothe ecologicalnichesofdifferenthomininpopulationsinWallacea9 , 24, moredirectassessmentsofoverallhomininresourcerelianceand palaeoenvironmentalchangeintheregionhavebeenlacking. Inthispaper,weexaminetheadaptationsoftheearliest knownfossilmembersofourspeciesinWallaceabymeansof isotopicanalysisofarchaeologicalhumantoothenamelfrom twoislands(TimorandAlor;Fig. 1 ).Timorhasyieldedthe earliestdatedmaterialcultureandfossilevidencefor H. sapiens inWallaceaatthesitesofAsitauKuru(formerlyJerimalai)andLaili18 , 19.Attheformer,faunalremainsandculturalartifactssuggestLatePleistocenehumanrelianceon marineshell shand sh,obtainedinpartthroughoffshore shing13.Lailialsoprovidesevidenceforearlyrelianceon marineresources18.Thisstandsincontrasttothegeneralized mixedgrasslandandwoodlandadaptationsassociatedwith otherhomininsintheregion9 , 24 , 25.However,humanreliance onpelagic shingatAsitauKuruhasbeenquestioned26. Moreover,thereremainsthepo ssibilitythatgiantrattaxa, withproposedpreferencesforclosedforestenvironmentsand anadultbodyweightofupto6kg,representedsigni cantfood resources;andtheyhavebeenidenti edinearlycoastaland inlandarchaeologicalcontextsinAlorandTimor(e.g.,ref.27). InsightsintotheenvironmentspresentonWallacea,aswellas humanrelianceondifferentecosystemsisdif culttoresolve Fig.1MapsshowingthelocationofthestudiedsiteswithinWallacea. AsitauKuru,LeneHara,MatjaKuru1and2(Timor),Makpan,andTronBonLei (Alor). ARTICLENATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-42NATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications
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usingtraditionalzooarchaeologicalmethodsalonedueto preservationbiasesandtheroleofnonhumanpredatorsinsite taphonomy(e.g.,ref.28). Here,weapplystablecarbon( 13C)andoxygen( 18O)isotope analysestohumanandfaunaltoothenamelfromsixLatePleistocene/Holocenearchaeologicalsequences(Fig. 1 )onTimorand Alor,inordertodeterminethevaryingrelianceofearlyhuman colonisersofWallaceaontropicalforestandterrestrialversus marineresources.Stablecarbonisotopeanalysisoffaunal (includinghominin)toothenamelintropicalregionshasbeen usedtoassesstheproportionofC3-dominatedwoodland/forest andC4grasslandbiomassindiets29 – 31.Inregionssuchas PleistoceneWallacea,wheresomeresearchershavesuggestedthat tropicalforestsdominatedterrestrialenvironments32,with grasslandsconsideredlargelyabsent,themostsigni cantdriver ofterrestrialstablecarbonisotopevariationwillbethecanopy effect,wherebylowlightandrespiredCO2causeforest-dwelling plantbiomassanditsconsumerstohavemorenegative 13C valuesthantheircounterpartsinmoreopenhabitats30 , 31. Meanwhile,marineproducerbiomasshashigher 13CthanallC3terrestrialplants33 , 34,enablingmarineconsumerstobedistinguishedfromterrestrialC3consumers35.Basedonresearch doneinEastAfrica30,SriLanka31,andJapan35,including extensivemodernstudies30,weexpectpreindustrialhumans relyingcompletelyontropicalforest,openC3resources,and marineresourcestohavetoothenamel 13Cvaluesofc. 14 ‰ ,c. 11 ‰ ,andc. 4 ‰ ,respectively. Stableoxygenisotope( 18O)measurementsfromanimaltooth enamelprovideadditionalpaleoecologicalinformationabout waterandfood,andhavealsobeenarguedtodistinguish terrestrialfrommarineconsumers36.Basedonexisting, published,andavailablechronologicalinformation,theLate Pleistocene – HolocenedepositsofAsitauKuru,MatjaKuru1and 2,LeneHara,Makpan,andTronBonLeiprovideauniquesuiteof humanandassociatedfaunalsamplesspanningtheearliestfossil appearanceof H.sapiens inWallacea,throughtheLastGlacial Maximum,andacrosstheTerminalPleistocene – Holocene transition18 , 19.Theyalsocoverbothcoastalandhinterlandhabitats(Fig. 1 ).Ampleterrestrialandmarineanimalremainsalso allowustobuildthe rstdetailedpaleoecologicalandpalaeoenvironmentalrecordsforPleistoceneWallaceaandtestassumptionsinrelationto:(1)pureC3terrestrialenvironmentsonTimor andAlorinthepast;(2)the 13Cdistinctionbetweenavailable terrestrialandmarineresources;and(3)environmentalshifts acrossthePleistocene – Holoceneboundaryproposedelsewhere inSoutheastAsia(e.g.,5 , 37).Thepreservationofasubsectionofthe analysedtoothenamelsampleswasalsocheckedusing Fouriertransforminfraredspectroscopy(FTIR)asperRoberts etal.31 , 38. Ourextensivefaunalbaselinedemonstratesthatterrestrialand marineenvironmentscanbeclearlydistinguishedisotopicallyin Wallaceaonthebasisofstableisotopeanalysisoffossiltooth enamel.Weshowthatatoothoftheearliestpreserved H.sapiens fossilfoundfromtheregionc.42 – 39,000yearsagoshowsthatthis individualmadesigni cantuseofcoastalresources.From20,000 yearsago,humanpopulationsshowanincreasingrelianceon interior,terrestrialenvironmentsontheislandsofbothTimor andAloratatimeofincreasingforestexpansioninIsland SoutheastAsiamoregenerally,thoughsomeindividualscontinue tointensivelyusemarineresources.Wearguethatourdatafurther demonstratesthehugeadaptive exibilityofourspecies, acutelyvisibleasitrapidlyandpersistentlycolonizedWallacean environments.Itsabilitytospecializeintheuseofmore extremeenvironmentsseemstostandincontrasttootherhominin speciesknownfromIslandSoutheastAsiabasedoncurrent evidence. Results Sites,samples,andchronology .Thedetailedstratigraphicand chronologicalinformationforthesixsitesstudied(Supplementary Note1)hasenableddivisionofthehumanandfaunalsamplesinto occupationphasesateachsite(Figs. 2 – 6 ).Todisplayandcompare ourdataonabroaderscale,wehavealsodividedthehumanand faunaldataintobroaderislandphasesofoccupationforTimorand Alor,respectively,basedonthestratigraphicandchronometric information(SupplementaryNote1,SupplementaryTables6and 7,Fig. 2 ).ForthesitesofAsitauKuru,LeneHara,MatjaKuru1, andMatjaKuru2onTimor,thissystemincludesfourbroad phases:aLatePleistocenepre-LGMphase(46,000 – 29,000years ago),aTerminalPleistocenephase(20,000 – 11,001yearsago),an EarlyandMiddleHolocenephase(11,000 – 4001yearsago),anda LateHoloceneNeolithicphase(4000 – 0yearsago).Forthesitesof Fig.2 13Cmeasurementsforhumanandfaunaltoothenamelfromthe islandsofAlorandTimoranalyzedinthisstudy. Datashownbyphases developedonthebasisofexistingandpublishedstratigraphic,and chronologicalinformation(SupplementaryNote1).Boxplots(showing medianandinterquartilerange — withoutliersindicated)ofterrestrialfauna areshowningreen(blackdiamondpoints)andthoseofmarinefaunain blue(blacksquarepoints).Humansamplesareshownaswhitesymbols dependingonsite(circle,AsitauKuru;diamond,MatjaKuru1and2;square, LeneHara;triangle,Makpan;andinvertedtriangle,TronBonLei).Source dataforFig.2canbefoundintheaccompanyingSourceData leinTable1 (Fig.2). NATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-4ARTICLENATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications3
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MakpanandTronBonLeionAlor,thephasingsystemincludes threebroadphases:aLatePleistocenepre-LGMphase (40,000 – 21,000yearsago),aTerminalPleistocenetoMiddle Holocenephase(15,000 – 7400yearsago),andaLateHolocene Neolithicphase(4000 – 0yearsago).Thespeci cassociateddates forthehumansampleswithinthesebroaderphasesarediscussed inthemaintextwhereappropriate. Stableisotopeanalysisofarchaeologicaltoothenamel .Faunal 13CfromtheLatePleistocene – HolocenesequencesofAsitau Kuru,MatjaKuru2,Makpan,andTronBonLei(Figs. 2 – 6 )show a 13Cdivisionintermsofterrestrialandmarinefauna(Fig. 2 , SupplementaryFigs.13and14,SupplementaryData1).Forthe islandofTimor,terrestrialfaunarecoveredfromthecoastalsite ofAsitauKuru(Fig. 3 )andinlandsiteofMatjaKuru2(Fig. 4 ) have 13Crangesof 14.9to 7.9 ‰ (mean = 11.6±1.8 ‰ ) and 14.9to 9.0 ‰ (mean = 12.0±1.4 ‰ ),respectively.By contrast,themarinefaunafromAsitauKuru(Fig. 3 )hasa 13C rangeof 8.3to3.7 ‰ (mean = 4.1±3.0 ‰ ).Thesituationis slightlymorecomplexonAlor(Fig. 2 )whereterrestrialfauna fromMakpan(Fig. 5 )has 13Crangingfrom 19.2 ‰ to 3.1 ‰ (mean = 8.7±3.5 ‰ ),andmarinefaunafromMakpan(Fig. 5 ) andTronBonLei(Fig. 6 )have 13Crangingfrom 6.4to4.9 ‰ (mean = 3.2±2.9 ‰ )and 8.9to4.7 ‰ (mean = 5.4± 3.5 ‰ ),respectively. AShapiro – Wilktestindicatedthatthe 13C( p = <0.05)and 18O( p = <0.05)oftheentirefaunaldataset( n = 223)werenonnormallydistributed.Mann – Whitney – Wilcoxontestsdemonstratedthe 13C( W = 9257, p = <0.05)and 18O( W = 5264, p = <0.05)offaunatobesigni cantlydifferentbetweenTimor andAlor.Consequently,thefaunal 13Cand 18Odatasetsofthe islands(Timor n = 111;Alor n = 112)wereseparatedfor subsequentanalysesunlessotherwisespeci ed.ForbothTimor andAlor,Shapiro – Wilktestsfoundtheresulting 13Cand 18O datasetsforeachislandtobenon-normallydistributed( p = < 0.05).Mann – Whitney – Wilcoxontestsfoundmarineandterrestrialfaunatobesigni cantlydifferentintermsof 13Conboth Timor( W = 2657, p = <0.05)andAlor( W = 2423, p = <0.05). Nodifferencewasfoundbetweenterrestrialandmarinefaunal groupsintermsof 18OoneitherTimor( W = 1507, p = >0.05) orAlor( W = 1375, p = >0.05). Intermsofterrestrialpalaeoenvironmentalconditionsand changesinLatePleistocene – HoloceneWallacea,ourdatadirectly con rmstheC3forest – woodlandpreferencesfornow-extinct giantrattaxaonbothTimorandAlor(Figs. 3 – 5 ;asperref.27). SeparationoftheterrestrialfaunadatasetfromTimor( n = 76) andKruskal – Wallisanalysisshowstheretobenosigni cant 13C differencesbyphaseonthisisland(Kruskal – Wallischi-squared = 3.157,df = 3, p = >0.05).Althoughsigni cantdifferencesin 18Owerenotedbetweenphases(Kruskal – Wallischi-squared = 13.647,df = 3, p = <0.05),pairwisecomparisonfailedtodrawout anyspeci cdifferences(>0.05)(SupplementaryTable8).Forthe Alorterrestrialfaunaldataset( n = 42),thesituationismore complicated.Here,aKruskal – Wallistest(Kruskal – Wallischisquared = 14.386,df = 2, p = <0.05)followedbypairwisecomparisondemonstratedsigni cant 13Cdifferencesbetweenphases A(40,000 – 21,000yearsago)andC(4000 – 0yearsago),andB (15,000 – 7400yearsago)andC(4000 – 0yearsago;Supplementary Table9).Nosigni cantdifferenceswerefoundfor 18O (Kruskal – Wallischi-squared = 2.321,df = 2, p = >0.05). Thedifferencebetweentheislandsisdrivenbythefactthatin theearliestphaseofoccupationonAlor(40 – 21,000cal.yearsBP) thereisanoverlapbetweenterrestrialandmarinefaunain 13C (Figs. 2 and 5 ).Fromthispoint,the 13Cofterrestrialfauna declinesthroughthephases,withterrestrialandmarinefauna becomingobviouslydifferentbetween15,000 – 7400cal.yearsBP and4000 – 0cal.yearsBP(Fig. 2 ).TheseresultssuggestthatC4resourcesmayhavebeenavailabletosometerrestrialfaunainthe earliestphaseofhumanoccupationonAlor,withtheirpresence decliningthroughtime.However,itisalsopossiblethatelevated rat 13Ccouldbeaproductofearlyaccesstomarineresources39. Finally,separationofthecombineddatasetofmarinefaunafor TimorandAlor( n = 105),andKruskal – Wallisanalysisand pairwisecomparison(Kruskal – Wallischi-squared = 17.975,df = 8, p = <0.05)showedsigni cant 13Cdifferencesbetweenreef taxasuchasBalistidae(Trigger shes)andmorewide-ranging taxa,suchas Scaridae (Parrot shes)(SupplementaryTable10), indicatingthepotentialutilityofisotopicanalysisofteethto distinguish shfromdifferentmarineniches(seealsoref.40). Ourlarge,robustfaunalbaselineenablesthelong-term ecologicalnichesofLatePleistocene/Holocenehumanforagers tobedirectlydeterminedforAsitauKuru,MatjaKuru2, Makpan,andTronBonLei,aswellastheadditionalsitesofLene HaraandMatjaKuru1whereonlyhumansampleswereavailable (Figs. 2 – 6 ; n = 26).Sampledhuman 13Cand 18Oranges between 14.1and 5.6 ‰ and 6.2to 3.2 ‰ ,respectively (Fig. 2 ,SupplementaryData2).Theearliesthumansampleinthe study,andtheearliestrecoveredfromWallacea,fromcontextB63 atAsitauKuru,datedtoc.42,440 – 38,853cal.yearsBP,hasa 13C valueof 5.6 ‰ (Fig. 3 ).Thisisindicativeofahighrelianceon marineresources,giventhelackofanyevidenceforC4resources inthispartofTimoratthistimeandzooarchaeologicalevidence forabundantmarineresources(Fig. 2 ).Themajorityofthe remaininghumanssampledfromtheTerminalPleistoceneand HolocenecontextsofAsitauKuru(Fig. 3 ),LeneHara(Fig. 3 ), MatjaKuru1and2(Fig. 4 ),andthesiteofMakpan(Fig. 5 )on Alor,have 13Cvaluesbetween 14.1 ‰ and 9.6 ‰ ,indicating humanrelianceonamixtureofterrestrialtropicalforest resourcesandmoreopenC3environments(Fig. 2 ). Indeed,Fig. 6 demonstratesthateventhe 13Cvaluesof humansexcavatedfromTronBonLei(SupplementaryNote1), withanassumedeconomicandculturalrelianceonmarine resources,havearangeofbetween 12.5 ‰ and 9.6 ‰ .With perhapstheexceptionoftheindividualfromsquareCwitha valueof 9.6 ‰ ,wholikelydemonstratessomecontributionof marineorC4resources,thisshowsthatterrestrialC3resources madeupthemajorityofthedietsoftheseindividuals.Nevertheless,itisclearthattwoTerminalPleistocene/Holocene individualsatMakpan,Alor( 8.1 ‰ ;15,000 11,000cal.years BP;Fig. 5 ),andMatjaKuru2,Timor( 5.6 ‰ ;Fig. 4 ; 11,000 – 4000cal.yearsBP)incorporatedasigni cantproportion ofC4/marineandmarineresourcesintotheirdiets,respectively, basedonassociatedfaunaldata(Fig. 2 ),suggestingthatdietswere diversebetweenindividualsandsocietiesduringtheTerminal PleistoceneandHolocene. Fouriertransforminfraredspectroscopy .Fullresultsofthe infraredindicesofsamplessubjectedtoFTIRanalysisareshown inSupplementaryData3.Allofthefossilandmodernenamel samplesdisplayedclassicenamelFTIRspectra(Supplementary Fig.15).Noadditionalbandsfromsecondarycarbonate(e.g. calciteat710cm 1;ref.41)wereobservedinthespectraofthe fossilsamples(SupplementaryFig.15).BoxplotsofAPI,BPI, WAMPI,PCI,andBAIforthegroupsof ‘ Modern ’ , ‘ Fossil Human ’ , ‘ FossilTerrestrialFauna ’ ,and ‘ FossilMarineFauna ’ are showninSupplementaryFig.16.Broadly,thereareminimal changesbetweenthegroupswithfossilsamplesperhapshaving marginallylowerAPI,slightlyhigherBPI,andhigherBAIthan the ‘ Modern ’ sample(SupplementaryFig.16).Analysisofvariance(ANOVA)andpost-hocTukeypairwisecomparisons ARTICLENATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-44NATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications
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supportthis, ndingnosigni cantdifferencesinA-sitecarbonation( F (3,55) = 1.194, p >0.05),B-sitecarbonation( F (3,55) = 1.387, p >0.05),PCI( F (3,55) = 1.845, p >0.05),orWAMPI( F (3,55) = 1.245, p >0.05)betweenthedifferentsamplegroups.By contrast,BAIdoesshowadifferencebetweenthegroups ( F (3,55) = 6.232, p <0.05),with ‘ FossilMarineFauna ’ and ‘ Fossil TerrestrialFauna ’ beingsigni cantlydifferentfrom ‘ Modern ’ samples(SupplementaryTable11). Poorpreservationofskeletalmaterialhasbeensuggested elsewhereintropicalrainforestenvironments,thoughsuch Fig.3IsotopedatafromAsitauKuru(Timor). Stablecarbon( 13C)andoxygen( 18O)isotopedatafromterrestrialandmarinefaunaltoothenamel samples,withhumansamplesshownaswhitecircles,displayedbysitephases(seeSupplementaryNote1). NATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-4ARTICLENATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications5
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Fig.4IsotopedatafromMatjaKuru1and2(Timor). Stablecarbon( 13C)andoxygen( 18O)isotopedatafromterrestrialfaunaltoothenamelsamples fromMatjaKuru2(Timor),withhumansamplesshownaswhitediamonds,displayedbysitephases(seeSupplementaryNote1).Regionalphasinghas beenusedforthe11,000 – 4000cal.yearsBPgroupingsoindividualsfromMatjaKuru1and2canbecombined.Thegroupingof16,000 – 11,000cal.years BPisonlyrepresentedbytwohumanindividualsfromMatjaKuru1asthereisnooccupationatMatjaKuru2atthistime(seeSupplementaryNote1). ARTICLENATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-46NATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications
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commentshavemainlyfocusedonorganicbonematerial42.The fossilenamelFTIRspectraproducedherearevirtuallyindistinguishablefrommodernspectra(SupplementaryFigs.15and 16).Theprecipitationofcarbonatemineralsislikelytobemore ofaprobleminthecontextofmoreporousmaterials,suchas bone43 , 44.Subtledifferencesnotedinfaunalenamelapatite duringfossilizationnotedhere,includingincreasedBAIand decreasedA-carbonateonphosphateindex,havealsobeen Fig.5IsotopedatafromMakpan(Alor). Stablecarbon( 13C)andoxygen( 18O)isotopedatafromterrestrialandmarinefaunaltoothenamelsamples, withhumansamplesshownaswhitetriangles,displayedbysitephases(seeSupplementaryNote1). NATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-4ARTICLENATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications7
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demonstratedinotherstudies,includingwithinthetropicsof SouthAsia,andhavebeenarguedtobeaproductofthereduction inorganicmaterialwithintheapatitematrixthroughtime31 , 38 , 45. Suchchangeisnotconsideredtohavemajorimpactsonoverall enamelapatitestructureorstablecarbonandoxygenisotope measurementsfromenamel45,asfurthersuggestedbythe preservationofexpectedecologicaldifferencesintheenamel hereandelsewhere29 , 31. Discussion Ourstableisotopedataallowustodirectlyassesstheecological relianceondifferentcategoriesofresourcesthataccompaniedour species ’ arrivalandsubsequentsettlingofWallacea.Theearliest humanstoarriveinthispartoftheworldseeminglyspecializedin theuseofcoastalresources.Whilewecannotcurrentlydistinguishbetweenpelagicandotherformsofoffshoreresourceuse13, andoursamplesizefromthisearlyperiodislimited,wecanbe con dentthatthe 13Cvalueforthisindividualindicatesarelianceonmarineresources.Following20,000cal.yearsBP,aclear diversi cationinhumanresourceuseacrossWallaceaemerges. Whilesomecoastalrelianceisindicatedbyoneindividualat MatjaKuru2,andperhapsalsoMakpan,mostindividuals demonstratebroaderuseofinteriorenvironments,including closedtropicalforesthabitats.Thismaybeconsideredsurprising, particularlygiventheongoingpresenceof shandshell sh9,the symbolicburialofanindividualatTronBonLeiwith shhooks (SupplementaryNote1),aswellasarchaeologicalevidencefor increasedtransferofmaterialculturebetweenislandsfromthis time46 , 47.However,toothenamel 13Cre ectsthewholedietof anindividual,andourdatahighlightsthenecessityofpaying moreattentiontothecontributionofplant(andterrestrialanimal)resourcestohumandietsontropicalislands,particularlyas thosepopulationsbecomemoreestablished — somethingalso recentlyurgedevenforthestudyofthelaterLapitaexpansionin thePaci c48 , 49. Thisstudypresentsthe rstdetailedpalaeoenvironmental informationforLatePleistocene – HoloceneWallacea,directly associatedwithrecordsofhumanbehavior.Ourdataindicates that,onTimor,tropicalforestenvironmentsremainedprevalent throughoutthepast45,000years,onlydecreasingduringtheLate Holocenewiththearrivalofhuman-induceddeforestationduring theIronAge27 , 50.ThereisnoevidenceforthepresenceofC4grasslandenvironmentsinthevicinityofanyofthesitesstudied. Bycontrast,onAlor,C4resourcesmayhavebeenavailabletosome smallmammals,andpresumablyalsohumans,duringtheearliest Fig.6IsotopedatafromTronBonLei(Alor). Stablecarbon( 13C)andoxygen( 18O)isotopedatafromterrestrialandmarinefaunaltoothenamel samples,withhumansamplesshownaswhiteinvertedtriangles,displayedbysitephases(seeSupplementaryNote1). ARTICLENATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-48NATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications
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periodofoccupation(40,000 – 21,000yearsago).Fromthispoint onward,theseresourcesdisappearastropicalforestenvironments expandedacrosstheTerminalPleistocene – Holoceneboundary. Whileitremainspossiblethatelevated 13Cforsomefaunainthe earlierphaserepresentsconsumptionofmarineresources,this palaeoenvironmentalpatternofincreasingtropicalforestsduring theTerminalPleistocenehasalsobeendocumentedelsewherein bothIslandandMainlandSoutheastAsia5.Inthesecases,the expansionoftropicalforestduringtheTerminalPleistoceneand EarlyHolocenehasalsobeenassociatedwithincreasinglyspecializedhumanhuntingofarborealandsemi-arborealmammalsand theuseoftropicalforestplants5. Ourisotopicevidencesupportshumancolonizationmodelsof WallaceaandAustraliathatsuggestarapid,initialcoastalcolonization,followedbylaterinlandsettlement12 , 14,atleastwith regardstothesitesstudiedhere.Thismodeofcolonization isdistinctfromisotopicandmaterialevidencefromtheWetZone rainforestsofLatePleistoceneSriLanka31 , 51andarchaeological evidencefromtheNiahCavesinBorneo52thatindicatededicated,specializedtropicalforestforagingbyearlyhumanpopulationsintheseregionsfrom45,000yearsago.Thisfurther highlightsthepotentialroleofsophisticatedseafaringinthe humancolonizationofeasternWallaceaandAustralasia12 , 13 , 53.A later,increasedfocusonterrestrialresourcesornearshorecoastal resourcesduringtheTerminalPleistoceneandHolocenehasalso beenarguedonthebasisofzooarchaeologicalevidencefrom Timor,andelsewhereinIslandSoutheastAsia18 , 54.Thissubsistencepatternoccursalongsideanincreaseinoccupation intensityacrossWallaceafromtheTerminalPleistocene,aswell asanincreaseinformalizedlong-distancetradingnetworks,and islikelyrepresentativeofexchangebetweensettledgroupsinthe region46 , 47. Theadaptive exibilityvisibleinthecolonizationofalmostall oftheEarth ’ scontinentsbyourspeciesintheLatePleistocene standsinstarkcontrasttotheadaptationsofotherhominin species3 , 6 , 9 , 24.Whilethereissomeevidencethatotherhominins mayhavemadewatercrossings20 – 23orventuredintohighaltitudeenvironments10,wherepresent,existingzooarchaeological/paleontologicalandpalaeoenvironmentalevidencesuggestsa general,albeitdiverse,focusonmixedgrasslandandwoodland environments,withdispersalsandcontractionsoftenrelianton climaticallydrivenenvironmentalchange24 , 55.Futureisotopic analysisandmoredetailedzooarchaeologicalworkarerequiredto testthisdistinction,bothinWallaceaandbeyond.However,there isclearevidencethatdifferentpopulationsof H.sapiens wereable tospecializeinavarietyofextremeenvironmentsevenasour speciesasawholegeneralizedintheuseofmultiplesettings6. This exibility,perhapssupportedbyuniquecapacitiesofinnovation,technologicalsophistication,andsocialcommunication (e.g.,ref.56),enabledadaptationtoavarietyofconditions,not justthroughspacebutalsothroughtime,thatwouldeventually leaveusthelasthomininstanding. MethodsSites,samples,andchronology .Wesampledavailablehumanandanimalteeth fromtheLatePleistocene – HolocenedepositsofAsitauKuru,MatjaKuru1and2, andLeneHaraontheislandofTimorandMakpanandTronBonLeiontheisland ofAlor.Existing,includingpublished,stratigraphic,andchronologicalinformation wascompiled,inordertoenabletheplacementofsamplesintheirpropercontext. Alloftheavailabledatesused,stratigraphicinformation,andaccompanying archaeological ndscanbefoundinSupplementaryNote1,Supplementary Figs.1 – 12,andSupplementaryTables1 – 7.Theavailablesampleswereselectedon thebasisofoccupationphasesnotedandpublishedforeacharchaeologicalsite (SupplementaryNote1,SupplementaryTables1 – 7).Basedontheseestablished sequences,sampleswerealsogroupedintoanoverall ‘ phasing ’ foreachofthe islandsofTimorandAlortoprovidelargersamplesizesforthebroaderevaluation ofadaptivecontextforthearrivalofhumansoneachisland,hypothesized palaeoenvironmentalchangesacrosstheTerminalPleistocene/Holoceneboundary, andchangesfollowingthearrivalof ‘ Neolithic ’ materialcultureduringtheHolocene(SupplementaryNote1,SupplementaryTables6and7). Althoughbonecollagenisfrequentlytheprimarytissueusedintheisotopic determinationofancientdiets,itisoftendegradedandnearlyimpossibletoextract fromarchaeologicalremainsinthehumidtropics,particularlythosedatingbackto thePleistocene57 , 58.Thisisthecaseforthesitesstudiedhere.Bycontrast,tooth enamelconsistsprimarilyofaninorganicfractionextremelyresilientto postmortemdiagenesis59,meaningthatitisthefossiltissueofchoicefortropical dietaryreconstruction58 , 60.Toothidenti cationandanalyseswereconductedatthe AustralianNationalUniversity(ANU).Fish,reptile,andnon-muridmammal identi cationswerefacilitatedthroughcomparisonswithspecimensfromtheANU ArchaeologyandNaturalHistoryOsteologyLaboratoryreferencecollection.Murid identi cationswerefacilitatedthroughcomparisonswitharchaeologicalandfossil specimenscollectedfrompreviousANUexpeditions,materialheldinKA ’ sprivate collections,theAustralianNationalWildlifeCollectionoftheCommonwealth Scienti candIndustrialResearchOrganisationNationalFacilitiesandCollections, anddescriptionsandillustrationsinAplinandHelgen61andGlover62. Toothenamelrecordsanisotopicdietarysignaturefortheperiodofenamel formationthatwillvarydependingonthespeciesandtoothsampled.Forhumans, thelongestisotopicsignatureisprovidedbythirdmolarsthatcandevelopanytime between7and13yearsofage,andthemidtolateteenageyears63 , 64.While collagen 13Cisalsobiasedtowardproteincomponentsofthediet65,toothenamel 13Cre ectsthatofthewholedietduringformation.Duetotherarityoffossil humanremainsinPleistocenearchaeologicalsites,wesampledalloftheavailable humanteethpresent(SupplementaryData2).Theresultisoneofthelargest collectionsofhumantoothenameldatathatspanstheLatePleistocene/Holocene (seerefs.31 , 60forcomparisoninSriLanka)andthe rstforIslandSoutheastAsia. Whilesomeoftheseteethcomefromskeletonsthathavebeenagedandsexed,the majorityarelooseteeth.Subtlevariationsin 13Cand 18Obetweenteethcould occurasaresult,particularlyforteethformedduring ‘ weaning ’66.However,overall thisminor ‘ noise ’ willnothinderthetestingofthemajor 13Cdistinctionsbetween closedcanopyC3resources,C3opensettings,C4resources,andmarineresources. Stableisotopeanalysisofarchaeologicaltoothenamel .Allteethorteeth fragmentswerecleanedusingair-abrasiontoremoveanyadheringexternal material.Enamelpowderforbulkanalysiswasobtainedusinggentleabrasionwith adiamond-tippeddrillalongthefulllengthofthebuccalsurface,inordertoensure arepresentativemeasurementfortheentireperiodofenamelformation.All enamelpowderwaspretreatedtoremoveorganicorsecondarycarbonatecontaminates.Thismethodfollowedestablishedprotocolsthathavebeenapplied elsewheretoPleistocenetoothenamelinthetropics,whereithasproventobe effective31 , 60 , 67 , 68,enablingfuturecomparisonbetweendatasets.Sampleswere washedin1.5%sodiumhypochloritefor60min,followedbythreerinsesinpuri edH2Oandcentrifuging,before0.1Maceticacidwasaddedfor10min,followed byanotherthreerinsesinpuri edH2O.Sampleswerethenlyophilizedfor24h. Followingreactionwith100%phosphoricacid,gasesevolvedfromthesamples weremeasuredbystablecarbonandoxygenisotopeanalysisusingaThermoGas Bench2connectedtoaThermoDeltaVAdvantageMassSpectrometeratMPISHH. 13Cand 18OvalueswerecomparedagainstInternationalStandards (IAEA-603( 13C = 2.5; 18O = 2.4);IAEA-CO-8( 13C = 5.8; 18O = 22.7); USGS44( 13C = 42.2))andin-housestandard(MERCK( 13C = 41.3; 18O = 14.4))usingIsodat3.0softwarefromThermoElectronCorporation.Replicate analysisofMERCKcarbonatestandardssuggeststhatmachinemeasurementerror isc.±0.1 ‰ for 13Cand±0.2 ‰ for 18O.Whileeachsamplewasmeasuredonly oncetopreservematerialforfutureanalyses,asisstandardforthisapproach, overallmeasurementprecisionandreproducibilityfortoothenamelsampleson thismachinesetupwasstudiedthroughthemeasurementofrepeatextractsfrom anin-housebovidtoothenamelstandard( n = 20; 13C = 12.4±0.2 ‰ ; 18O = 8.0±0.3 ‰ ). Fouriertransforminfraredspectroscopy .Whilereliable 13C-and 18O-based dietaryandenvironmentalindicatorshavebeendemonstratedacrossmillionsof years29,protocolstocheckthestructuralpreservationoffossiltoothenamel samplesremainimportant(seeref.69).Thisisparticularlythecaseintropical forestenvironmentswithion-richsoilsandhighhydrologicalactivity.Onemeans tocheckenamelpreservationistheapplicationofFTIR,whichabsorbsradiationat discretevibrationalfrequenciesrelatedtothepresenceandcrystallographic environmentofkeyfunctionalgroups(seerefs.45 , 70 , 71).Thepolyatomicionsof interestarephosphates(PO43 ),carbonates(CO32 ),andhydroxylgroups(OH). Theobservedabsorbancebandsofenamelcanbeascribedtotheinternalvibrations ofthesemoleculargroups41 , 72(SupplementaryTable12). WeusetheempiricalindicesfromSponheimerandLee-Thorp70,andRoche etal.45tocharacterizethecrystal-chemicalpropertiesofenamelbioapatite (SupplementaryTable12).Thepossiblepresenceofcalcitewasassessedinall samplesbycheckingforapeakat710cm 1(refs.41 , 70).14 ‘ FossilHuman ’ ,15 ‘ Fossil TerrestrialFauna ’ ,and15 ‘ FossilMarineFauna ’ samplesweresubjectedtoFTIR analysisfollowingpretreatment,inordertodeterminetheremainingpotentialfor diageneticstructuralandcompositionalmodi cationofenamelafterpretreatment. Sampleswererandomlyselectedtocoveravarietyofthetemporalphasesandallof thesitesstudied(SupplementaryData3).Thefossilspectrawerecomparedtothose NATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-4ARTICLENATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications9
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availablefor15modernprimateandcervidsamples,andhistorical(latenineteenth andearlytwentiethcentury)humanenamelsamples( ‘ Modern ’ ),frompopulations livingintropicalforestenvironmentsinSriLankaalreadypublishedbyRoberts etal.73(SupplementaryData3). Forallsamples,powderedenamelwasanalysedbetween400and4,000cm 1by FTIRwithAttenuatedTotalRe ectance(FTIR-ATR — BrukerVertex70v)using theOPUS8.5softwarefromBruker.Eachsamplewasmeasuredthreetimes.The backgroundwassubtractedandabaselinecorrectionwascarriedoutusingthe OPUS8.5softwarefromBruker.Thebaselinesofthespectrawerenormalizedand allthreespectraofeachsamplewereaveragedbeforecalculationofthevarious infraredindices.Toensurebetterreproducibilityofthemeasurements,onlyspectra withaminimumabsorbanceof0.06forthehighestphosphatebandat ~ 1035cm 1weretakenintoaccount.ThereproducibilitiesoftheindicesBPI,API,BAI,and PCIare±0.01,±0.007,±0.1,and±0.1,respectively. Statisticalanalysis .All 13Cand 18Odatasetsweretestedfornormalityusing theShapiro – Wilktestandhistogramobservations.Followingobservationsofalack ofnormality,thesigni canceof 13Cand 18Ovariationbetweenthetwoislands (TimorandAlor),andbetweenterrestrialandmarinefaunaoneachislandwere testedusingMann – Whitney – Wilcoxontests.Thesigni canceof 13Cand 18O variationbetweentaxaandbetweenthedifferentperiodswastestedusing Kruskal – Wallistests.Wheresigni cant,thesetestswerefollowedbyapairwise Wilcoxoncomparisontodeterminewhichgroupsweresigni cantlydifferentfrom eachother.Inallcases,thedatasetbeingtestedanditssizeareexplicitlystated.All statisticalanalyseswereconductedusingthefreeprogramRsoftware74. AllFTIRindexvaluesweretestedfornormalityusingtheShapiro – Wilktest andhistogramobservations.Analysisofvariance(ANOVA)followedbyposthoc TukeypairwisecomparisonswereperformedforeachofthemainFTIRindicesof enamelapatite(PCI,BAI,BPI,API,andWAMPI — per45andde nedin SupplementaryTable12)acrossthesamplegroups(i.e., ‘ FossilMarineFauna ’ , ‘ FossilTerrestrialFauna ’ , ‘ FossilHumans ’ ,and ‘ Modern ’ ),inordertodetermine statisticaldifferencesinenamelcrystallinityandstructurebetweenfossiland modernsamples.Allstatisticalanalyseswereagainconductedusingthefree programRsoftware74. Reportingsummary .Furtherinformationonresearchdesignisavailablein theNatureResearchReportingSummarylinkedtothisarticle.DataavailabilityAllofthedatareportedinthepaperarepresentedinthemaintextorin theSupplementaryNotes,Tables,Figures,andData les.Thesourcedataunderlying Fig. 2 andSupplementaryFig.16areprovidedasaSourceData le.Thesourcedatafor Fig. 2 ,aswellasSupplementaryDataFiles1and2,alsounderlieFigs. 3 – 6 .Allotherdata supportingthe ndingsandinterpretationsofthisstudyareavailableinexisting publicationsandtheSupplementaryInformationprovidedalongsidethismanuscript. ThefaunalandhumanremainssampledfromTimor-Lestearecuratedinthe ArchaeologycollectionattheCollegeofAsiaandthePaci c,AustralianNational University,AustraliaunderthesitecodesJ(AsitauKuru),MK(MatjaKuru),andLH (LeneHara).ThesematerialsaretobereturnedtoTimor-Lesteuponconstructionofa nationalmuseumstorehouse.ThefaunalandhumanremainsfromAlorarehousedin theDepartmentofArchaeology,UniversitasGadjahMada,Indonesia,underthesite codesTBL(TronBonLei)andMP(Makpan).Allsitecodesarefollowedbysuf xesofa singleletterdenotingtheexcavationsquareandanumberdenotingthespit.Received:26January2020;Accepted:6April2020; References1.Aubert,M.etal.Earliesthuntingsceneinprehistoricart. Nature 576 ,442 – 445 (2019). 2.Akhilesh,K.etal.EarlyMiddlePalaeolithiccultureinIndiaaround385-172 kareframesOutofAfricaModels. Nature 554 ,97 – 101(2018). 3.Rizal,Y.etal.Lastappearanceof Homoerectus atNgandong,Java,117,000108,000yearsago. Nature 577 ,381 – 385(2020). 4.Reich,D.etal.Denisovaadmixtureandthe rstmodernhumandispersalsintoSoutheastAsiaandOceania. Am.J.Hum.Genet. 89 ,516 – 528 (2011). 5.RabettR.J. HumanAdaptationintheAsianPalaeolithic (Cambridge UniversityPress,Cambridge,2012). 6.Roberts,P.&Stewart,B.A.De ningthe ‘ generalist-specialist ’ nichefor Pleistocene Homosapiens . Nat.Hum.Behav. 2 ,542 – 550(2018). 7.Zhu,R.X.etal.Earlyevidenceofthegenus Homo inEastAsia. J.Hum.Evol. 55 ,1075 – 1085(2008). 8.Gamble,C. Timewalkers:ThePrehistoryofGlobalColonization (AlanSutton Press,Cheltenham,1993). 9.O ’ Connor,S.etal.HominindispersalandsettlementeastofHuxley ’ sLine:the roleofsea-levelchanges,islandsize,andsubsistencebehaviour.Curr. Anthropol. 58 ,S567 – S582(2017). 10.Chen,F.etal.AlateMiddlePleistoceneDenisovanmandiblefromtheTibetan Plateau. Nature 569 ,409 – 412(2019). 11.Bird,M.,Taylor,D.&Hunt,C.PalaeoenvironmentsofinsularSoutheastAsia duringthelastglacialperiod:asavannacorridorinSundaland? Quat.Sci.Rev. 24 ,2228 – 2242(2005). 12.Bird,M.I.etal.EarlyhumansettlementofSahulwasnotanaccident. Nat.Sci. Rep. 9 ,8220(2019). 13.O ’ Connor,S.,Ono,R.&Clarkson,C.Pelagic shingat42,000yearsbeforethe presentandthemaritimeskillsofmodernhumans. Science 334,1117 – 1121 (2011). 14.Kealy,S.,Louys,J.&O ’ Connor,S.ReconstructingpalaeogeographyandinterislandvisibilityintheWallaceanArchipelagoduringthelikelyperiodofSahul Colonization,65 – 45000YearsAgo. Archaeol.Prospect. 24 ,259 – 272(2017). 15.Norman,K.etal.AnearlycolonizationpathwayintonorthwestAustralia7060,000yearsago. Quat.Sci.Rev. 180 ,229 – 239(2017). 16.O ’ Connell,J.F.&Allen,J.Therestaurantattheendoftheuniverse:modeling thecolonizationofSahul. Aust.Archaeol. 74 ,5 – 31(2012). 17.SamperCarro,S.C.etal.HumanmaritimesubsistencestrategiesintheLesser SundaIslandsduringtheterminalPleistocene-earlyHolocene:Newevidence fromAlor,Indonesia. Quat.Int. 416 ,64 – 79(2016). 18.Hawkins,S.etal.OldesthumanoccupationofWallaceaatLailiCave,TimorLeste,showsbroad-spectrumforagingresponsestolatePleistocene environments. Quat.Sci.Rev. 171 ,58 – 72(2017). 19.Shipton,C.etal.Anew44,000-yearsequencefromAsitauKuru(Jerimalai), Timor-Leste,indicateslong-termcontinuityinhumanbehaviour. Archaeol. Anthropol.Sci. 11 ,5717 – 5741(2019). 20.Morwood,M.J.etal.Furtherevidenceforsmall-bodiedhomininsfromthe LatePleistoceneofFlores,Indonesia. Nature 437 ,1012 – 1017(2005). 21.VandenBergh,G.D.etal. Homo oresiensis -likefossilsfromtheearlyMiddle PleistoceneofFlores. Nature 534 ,245 – 248(2016). 22.Ingicco,T.etal.EarliestknownhomininactivityinthePhilippinesby709 thousandyearsago. Nature 557 ,233 – 237(2018). 23.VandenBergh,G.D.etal.EarliesthomininoccupationofSulawesi, Indonesia. Nature 529 ,208 – 211(2016). 24.Roberts,P.&Amano,N.Plasticpioneers:Homininbiogeographyeastofthe MoviusLineduringtheLatePleistocene. Archaeol.Res.Asia 17 ,181 – 192 (2019). 25.Brumm,A.etal.Ageandcontextoftheoldestknownhomininfossilsfrom Flores. Nature 534 ,249 –253(2016). 26.Anderson,A.Theantiquityofsustainedoffshore shing. Antiquity 87 , 879 – 895(2013). 27.Louys,J.etal.NewgenusandspeciesofgiantratfromAlorIsland,Indonesia. J.Asia-Pac.Biodiv 11 ,503 – 510(2018). 28.SamperCarro,S.C.,Louys,J.&O ’ Connor,S.Methodologicalconsiderations foricthyoarchaeologyfromtheTronBonLeisequence,Alor,Indonesia. Archaeol.Res.Asia 12 ,11 – 22(2017). 29.Lee-Thorp,J.A.,Sealy,J.C.&vanderMerwe,N.J.Stablecarbonisotoperatio differencesbetweenbonecollagenandboneapatite,andtheirrelationshipto diet. J.Archaeol.Sci. 16 ,585 – 599(1989). 30.Levin,N.E.etal.in TheGeologyofEarlyHumansintheHornofAfrica (edsJ. Quade&J.G.Wynn.)215 – 234(GeologicalSocietyofAmericaSpecialPaper 446,Boulder,Colorado,2008). 31.Roberts,P.etal.Fruitsoftheforest:Humanstableisotopeecologyand rainforestadaptationsinLatePleistoceneandHolocene(~36to3ka)Sri Lanka. J.Hum.Evol. 106 ,102 – 118(2017). 32.Monk,K.A.,deFretes,Y.&Reksodiharjo-Lilley,G. TheEcologyofNusa TenggaraandMaluku (PeriplusEditions,Jakarta,Indonesia,1997). 33.Smith,B.N.&Epstein,S.Twocategoriesof13C/12Cratiosforhigherplants. PlantPhysiol. 47 ,380 – 384(1971). 34.Fry,B. StableIsotopeEcology (Springer,NewYork,2006). 35.Kusaka,S.etal.Carbonisotoperatiosofhumantoothenamelrecordthe evidenceofterrestrialresourceconsumptionduringtheJomonperiod,Japan. Am.J.Phys.Anthropol. 158 ,300 – 311(2015). 36.Clementz,M.T.&Koch,P.L.Differentiatingaquaticmammalhabitatand foragingecologywithstableisotopesintoothenamel. Oecologia 129 ,461 – 472 (2001). 37.Cannon,C.H.,Morley,R.J.&Bush,A.B.G.Thecurrentrefugialrainforests ofSundalandareunrepresentativeoftheirbiogeographicpastandhighly vulnerabletodisturbance. PNAS 106 ,11188 – 11193(2009). 38.Roberts,P.etal.FossilherbivorestableisotopesrevealmiddlePleistocene homininpalaeoenvironmentin ‘ GreenArabia ’ . Nat.Ecol.Evol. 2 ,1871 – 1878 (2018). ARTICLENATURECOMMUNICATIONS|https://doi.org/10.1038/s41467-020-15969-410NATURECOMMUNICATIONS | (2020) 11:2068 |https://doi.org/10.1038/s41467-020-15969-4|www.nature.com/naturecommunications
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39.Polis,G.A.etal.In FoodWebsattheLandscapeLevel (edsPolis,G.A.,Power, M.E.&Huxel,G.R.)200 – 216(UniversityofChicagoPress,Chicago,Illinois, USA,2004). 40.Schoeninger,M.J.&DeNiro,M.J.Nitrogenandcarbonisotopiccomposition ofbonecollagenfrommarineandterrestrialanimals. Geochim.Cosmochim. Acta 48 ,625 – 639(1984). 41.Farmer,V.C. TheInfraredSpectraofMinerals (TheMineralogicalSociety, London,1974). 42.Tappen,M.Boneweatheringinthetropicalrainforest. J.Archaeol.Sci. 21 , 667 – 673(1994). 43.Lee-Thorp,J.A.&vanderMerwe,N.J.Aspectsofthechemistryofmodern andfossilbiologicalapatites. J.Archaeol.Sci. 18 ,343 – 354(1991). 44.Michel,V.,Ildefonse,P.&Morin,G.Assessmentofarchaeologicalboneand dentinepreservationfromLazaretCave(MiddlePleistocene)inFrance. Palaeogeogr.Palaeoclimatol.Palaeoecol. 126 ,109 – 119(1996). 45.Roche,D.etal.PreservationassessmentofMiocene-Pliocenetoothenamel fromTugenHills(KenyanRiftValley)-throughFTIR,chemicalandstableisotopeanalyses. J.Archaeol.Sci. 37 ,1690 – 1699(2010). 46.Reepmeyer,C.etal.Kisar,asmallislandparticipantinanextensivemaritime obsidiannetworkintheWallaceanArchipelago. Archaeol.Res.Asia 19 , 100139(2019). 47.Shipton,C.etal.ShellAdzes,ExoticObsidian,andInter-Islandvoyagingin theearlyandMiddleHoloceneofWallacea. JICA https://doi.org/10.1080/ 15564894.2019.1581306 (2019). 48.Maxwell,J.J.etal.Timingandimportanceofarboricultureandagroforestry inatemperateEastPolynesiaSociety,theMoriori,Rekohu(ChathamIsland). Quat.Sci.Rev. 149 ,306 – 325(2016). 49.Tromp,M.etal.Exploitationandutilizationoftropicalrainforestsindicated indentalcalculusofancientOceanicLapitaculturecolonists. Nat.Hum. Behav. https://doi.org/10.1038/s41562-019-0808-y (2020). 50.O ’ Connor,S.&Aplin,K.Amatterofbalance:anoverviewofPleistocene occupationhistoryandtheimpactoftheLastGlacialPhaseinEastTimorand theAruIslands,easternIndonesia. Archaeol.Ocean 42 ,82 – 90(2007). 51.Wedage,O.etal.Specializedrainforesthuntingby Homosapiens 45,000years ago. Nat.Commun. 10 ,739(2019). 52.Barker,G.,Farr,L. ArchaeologicalInvestigationsintheNiahCaves,Sarawak (TheArchaeologyoftheNiahCaves,Sarawak2) (McDonaldInstitutefor ArchaeologicalResearch,Cambridge,2016). 53.Balme,J.Ofboatsandstring:themaritimecolonisationofAustralia. Quat. Int. 285 ,68 – 75(2013).54.Boulanger,C.etal.Coastalsubsistencestrategiesandmangroveswamp evolutionatBubogIRockshelter(IlinIsland,Mindoro,Philippines)fromthe LatePleistocenetothemid-Holocene. JICA 14 ,584 – 604(2019). 55.Louys,J.&Turner,A.Environment,preferredhabitatsandpotentialrefugia forPleistocene Homo inSoutheastAsia. C.R.Palevol 11 ,203 – 211(2012). 56.Boyd,R.,Richerson,P.J.&Henrich,J.Theculturalniche:whysociallearning isessentialforhumanadaptation. PNAS 108 ,10918 – 10925(2011). 57.Krigbaum,J.NeolithicsubsistencepatternsinnorthernBorneoreconstructed withstablecarbonisotopesofenamel. J.Anthropol.Archaeol. 22 ,292 – 304 (2003). 58.Krigbaum,J.ReconstructinghumansubsistenceintheWestMouth(Niah Cave)Sarawak)burialseriesusingstableisotopesofcarbon. AsianPerspect. 44 ,73 – 89(2005). 59.Wang,Y.&Cerling,T.Amodeloffossiltoothandbonediagenesis: implicationsforpaleodietreconstructionfromstableisotopes. Palaeogeogr. Palaeoclimatol.Palaeoecol. 107 ,281 – 289(1994). 60.Roberts,P.etal.Directevidenceforhumanrelianceonrainforestresourcesin latePleistoceneSriLanka. Science 347 ,1246 – 1249(2015). 61.Aplin,K.P.&Helgen,K.M.QuaternarymuridrodentsofTimorPartI:new materialof Coryphomysbuehleri Schaub,1937,anddescriptionofasecond speciesofthegenus. Bull.Am.Mus.Nat. 341 ,1 – 80(2010). 62.Glover,I. ArchaeologyinEasternTimor,1966 – 67.TerraAustralis11 (DepartmentofPrehistory,ResearchSchoolofPaci cStudies (Australian NationalUniversity,Canberra,1986). 63.Hillson,S. DentalAnthropology (CambridgeUniversityPress,Cambridge, 1996). 64.Scheid,R.C. Woelfel ’ sDentalAnatomy 7thedn(Lipincoot,Williams& Wilkins,Philadelphia,2007). 65.Ambrose,S.H.&Norr,L.In PrehistoricHumanBone:Archaeologyatthe MolecularLevel (edsLambert,B.&Grupe,G.)1 – 37(Springer,Berlin,1993). 66.Wright,L.E.&Schwarcz,H.P.Stablecarbonandoxygenisotopesinhuman toothenamel:Identifyingbreastfeedingandweaninginprehistory. Am.J. Phys.Anthropol. 106 ,1 – 18(1998). 67.Sponheimer,M.etal.Hominins,sedges,andtermites:Newcarbonisotope datafromtheSterkfonteinvalleyandKrugerNationalPark. J.Hum.Evol. 48 ,301 – 312(2005). 68.Lee-Thorp,J.A.etal.IsotopicevidenceforanearlyshifttoC4resourcesby PliocenehomininsinChad. PNAS 109 ,20369 – 20372(2012). 69.Schoeninger,M.J.etal.Isotopicalterationofmammaliantoothenamel. Int.J. Osteoarchaeol. 13 ,11 – 19(2003). 70.Sponheimer,M.&Lee-Thorp,J.A.Isotopicevidenceforthedietofanearly hominid, Australopithecusafricanus . Science 283 ,368 – 370(1999). 71.Nagy,Z.K.etal.Comparativeperformanceofconcentrationandtemperature controlledbatchcrystallizations. J.ProcessControl 18 ,399 – 407(2008). 72.LeGeros,R.Z.CalciumphosphatesinOralBiologyandMedicine. Monogr. Oral.Sci. 15 ,1 – 201(1991). 73.Roberts,P.etal.HistoricaltropicalforestrelianceamongsttheWanniyalaeto (Vedda)ofSriLanka:anisotopicperspective. Hum.Ecol. 46 ,435 – 444(2018). 74.RCoreTeam. R:Alanguageandenvironmentforstatisticalcomputing (R FoundationforStatisticalComputing,Vienna,Austria,2013).AcknowledgementsForpermissiontoconduct eldwork,wethanktheSecretariadoEstadodaArtee Cultura,Timor-Leste,andtheIndonesianMinistryofResearch,Technology,andHigher Education(RISTEK)ForeignResearchPermitDivision(S.O ’ .C.1172/FRP/E5/Dit.KI/V/ 2016).ThisprojectwasfundedbytheMaxPlanckSociety,aEuropeanResearchCouncil StarterGrantawardedtoP.R.(no.850709),anAustralianResearchCouncilLaureate FellowshipawardedtoS.O ’ .C.(FL120100156),andtheAustralianResearchCouncil CentreofExcellenceforAustralianBiodiversityandHeritage(CE170100015).Wewould liketothankthelandownersandvillagersofAlorandTimor-Leste,staffandstudents fromtheUniversitasGadjaMada,PusatPenelitianArkeologiNasional,andBalai ArkeologiBalifortheirassistanceinthe eld.WealsothankCartoGISANUfortheir assistance.AuthorcontributionsP.R.,J.L.,C.S.,S.K.,andS.O ’ C.designedtheresearch;P.R.,J.L.,J.Z.,C.S.,S.K.,S.S.C.,S. H.,C.B.,S.M.,B.F.,K.A.,andS.O ’ C.collectedthedata;P.R.,J.L.,J.Z.,C.S.,S.K.,S.S.C.,S. H.,C.B.,andS.O ’ C.analyzedthedata;P.R.,J.L.,J.Z.,C.S.,S.K.,S.S.C.,S.H.,C.B.,S.M.,B. F.,N.B.,M.M.,K.A.,andS.O ’ C.wrotethepaper.CompetinginterestsTheauthorsdeclarenocompetinginterests.AdditionalinformationSupplementaryinformation isavailableforthispaperat https://doi.org/10.1038/s41467020-15969-4 . Correspondence andrequestsformaterialsshouldbeaddressedtoP.R.orS.O. Peerreviewinformation NatureCommunicationsthanksJohnKrigbaumandtheother, anonymous,reviewersfortheircontributiontothepeerreviewofthiswork.Peer reviewerreportsareavailable. Reprintsandpermissioninformation isavailableat http://www.nature.com/reprints Publisher ’ snote SpringerNatureremainsneutralwithregardtojurisdictionalclaimsin publishedmapsandinstitutionalaf liations. 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