Entrapment Bias of Arthropods in Miocene Amber Revealed by Trapping Experiments in a Tropical ...

24 Pages·2015·7.1 MB·English

RESEARCHARTICLE
Entrapment Bias of Arthropods in Miocene
Amber Revealed by Trapping Experiments in
a Tropical Forest in Chiapas, Mexico
MónicaM.SolórzanoKraemer1,3*,AtahualpaS.Kraemer2,FraukeStebner1,Daniel
J.Bickel4,JesRust1
1 Steinmann-InstitutfürGeologie,MineralogieundPaläontologie,RheinischeFriedrich–Wilhelms-
UniversitätBonn,Bonn,Germany,2 DepartamentodeFísica,FacultaddeCiencias,UniversidadNacional
AutónomadeMéxico(UNAM),CiudadUniversitaria,DistritoFederalMexico,Mexico,3 Senckenberg
ForschungsinstitutundNaturmuseum,FrankfurtamMain,Germany,4 AustralianMuseum,SydneyNSW
2010,Australia
* [email protected]
Abstract
Allentomologicaltrapshaveacapturingbias,andamber,viewedasatrap,isnoexception.
OPENACCESS
Thusthefaunatrappedinamberdoesnotrepresentthetotalexistingfaunaoftheformer
Citation:SolórzanoKraemerMM,KraemerAS, amberforest,ratherthefaunalivinginandaroundtheresinproducingtree.Inthispaperwe
StebnerF,BickelDJ,RustJ(2015)EntrapmentBias
comparearthropodsfromaforestverysimilartothereconstructionoftheMioceneMexican
ofArthropodsinMioceneAmberRevealedby
amberforest,anddeterminethebiasofdifferenttrappingmethods,includingamber.We
TrappingExperimentsinaTropicalForestin
Chiapas,Mexico.PLoSONE10(3):e0118820. alsoshow,usingclusteranalyses,measurementsofthetrappedarthropods,andguilddis-
doi:10.1371/journal.pone.0118820 tribution,thattheambertrapisacomplexentomologicaltrapnotcomparablewithasingle
AcademicEditor:ClaudioR.Lazzari,Universityof artificialtrap.Attheorderlevel,themostsimilartraptoamberisthestickytrap.However,in
Tours,FRANCE thecaseofDiptera,atthefamilylevel,theMalaisetrapisalsoverysimilartoamber.Amber
Received:September5,2014 capturedahigherdiversityofarthropodsthaneachoftheartificialtraps,basedonourstudy
ofMexicanamberfromtheMiddleMiocene,atimeofclimateoptimum,wheretemperature
Accepted:January22,2015
andhumiditywereprobablyhigherthaninmodernCentralAmerica.Weconcludethatthe
Published:March18,2015
sizebiasisqualitativelyindependentofthekindoftrapfornon–extremevalues.Wesuggest
Copyright:©2015Kraemeretal.Thisisanopen
thatfrequentspecimensinamberwerenotnecessarilythemostfrequentarthropodsinthe
accessarticledistributedunderthetermsofthe
formeramberforest.Selectedtaxawithhighernumbersofspecimensappearinamberbe-
CreativeCommonsAttributionLicense,whichpermits
unrestricteduse,distribution,andreproductioninany causeoftheirecologyandbehavior,usuallycloselyrelatedwithatree–inhabitinglife.Final-
medium,providedtheoriginalauthorandsourceare ly,changesofdiversityfromtheMiddleMiocenetoRecenttimeinCentralandSouth
credited.
AmericacanbeanalyzedbycomparingtherichamberfaunasfromMexicoandtheDomini-
DataAvailabilityStatement:Allrelevantdataare canRepublicwiththefaunatrappedusingstickyandMalaisetrapsinCentralAmerica.
withinthepaperanditsSupportingInformationfiles.
Funding:Thisresearchwaspossiblethankstoa
postdoctoralfellowshipawardedtoM.M.S.K.,No.
SO894/3-1fromtheGermanResearchFoundation
(DFG)andtheSpanishMinistryofEconomyand
CompetitivenessGL2011-23948AMBARES2012- Introduction
2014.Thefundershadnoroleinstudydesign,data
Thestudyoftheevolutionofecosystemsovergeologicaltimeisoneofthemostintricatetopics
collectionandanalysis,decisiontopublish,or
preparationofthemanuscript. inpaleontologicalresearch,especiallyinterrestrialtropicalareaswithaveryhighorganismal
PLOSONE|DOI:10.1371/journal.pone.0118820 March18,2015 1/24
TaphonomyofArthropodsinAmber
CompetingInterests:Theauthorshavedeclared diversityandusuallyaverypoorfossilrecord.Amongthemostimportantandmostchalleng-
thatnocompetinginterestsexist. ingaspectsofinvestigationsintotheevolutionofpaleodiversityintropicalrealmsistheimpact
oftaphonomicprocessesonthefossilisationinformerecosystems.Theknowledgeofwhatis
beingconservedorlostunderspecificconditionsoffossilizationisessentialforinterpretingthe
formerecosystem(e.g.[1]).Arthropodsplayadominantroleinextanttropicalforests,butthe
historyoftheirpresentdiversityasdocumentedinthefossilrecordislimitedduetospecialized
fossilisationconditionsfoundinspecificdepositslikelacustrineormarinesedimentsandespe-
ciallyamberdeposits(e.g.[2]).Fossilsinamberarewellknownfortheirexceptionallydetailed
preservationandspeciesrichness.Theyareamongthemostimportantresourcesfortherecon-
structionofformerterrestrialenvironments,especiallyintropicalandsubtropicalregionslike
thoserepresentedbytheDominicanandMexicanambers(e.g.[2–9];amongothers).Twoof
themostcomprehensiveanalysesandcompletereconstructionsofaformeramberforestwere
carriedoutbyLarsson[10]onEoceneBalticamber,andbyPoinar&Poinar[7]onMiddle
MioceneDominicanamber.However,eventhewellinvestigatedBalticamberrepresentsonly
afractionofthebiotathatlivedintheformeramberforest.
Ambercontainsorganismsfromdifferenthabitatssuchastreebark,soilandlitter,freshwa-
ter,andevenmarinelittoralrealms,duetodifferencesintheprocessofmaturationoftheresin
[11]andduetorareentrapmenteventsovertime.
Theentrapmentofarthropodsfromsuchdifferentlocalenvironmentsinresinisahighly
selectiveprocess,dependingonfactorsliketheresinproducingtree,thesizeandbehaviorof
arthropods,seasonalityandregionalclimaticgradients,localandregionalenvironment,resin
composition,andinsectdehydration[1].However,fewtaphonomicanalysesofamberfaunas
havebeendonesofar(e.g.[12]).ThefirstmajorstudywasthatofBrues[13],whocompared
thefaunaofBalticamberwitharthropodstrappedfromaforestnearPetersham,Massachu-
settswithflypaper,apapercoatedwithastickymixtureofcastoroil,resins,andwax.Brues
[13]believedthattheflypaperhadthesamesamplingpropertiesasresinandfurthermorehe
assumedthattheecologicalconditionsoftheformerBalticamberforestwouldbesimilarto
thePetershamforest.Consequently,heconcludedthattheinsectfaunahadchangedconsider-
ablyovertime.However,hisbasicassumptionswererejectedlaterbyHenwood[14].Shecom-
paredextantfaunasfromdifferentNeotropicalrainforestscollectedwithdifferentkindsof
trapsinBrazilandMexicowiththeamberfaunafromMioceneDominicanamber.Henwood
[14]concludedthatthefaunatrappedwithemergencetrapswasmostsimilartotheDomini-
canamberfaunaandthatamberreflectsground–subterraneanlevelresinproduction.These
conclusionswererejectedbyPenney[15],whodemonstratedthatatleastinrecentNeotropical
rainforeststhespiderfaunafromDominicanamberismostcloselyrelatedtoextanttree–in-
habitingspeciesawayfromthegroundlayer.Inoneofthemostrecentworksaboutinsectsin
contemporaryresins,Zherikhinetal.[16]comparedthefaunaofRecentresinscollectedfrom
differentPinaceaeinmanylocalitiesacrossnorthernEurasiawithEoceneBaltic,Rovno,Bitter-
feldandMioceneDominicanambers.Theyfoundageneraltrendtowardsadecreaseintherel-
ativeabundanceoflivingarborealspringtailsandnematoceranfliesandanincreaseinthatof
truebugs,beetles,lepidopterans,andhymenopteransincomparisonwiththeamber.Penney
andLangan[17]comparedforthefirsttimethesizeofspidersfromDominicanandBalticam-
bersshowingthatoverall,thebodysizeofweb–spinningspidersinBalticamberwasgreater
thaninDominicanamber,whileforactivehuntingspidersthesizewassimilar.Theyconclud-
edthatthebehaviorofthespidersandmorphologyoftheresinproducingtreearemoreimpor-
tantfactorsfortheentrapmentthanthesizeoftheorganism.Generallyitisconsideredthat
small–sizedarthropodsaremorelikelytogettrappedinresin;howeverthishasneverbeen
studiedindetailforallarthropodsinamber.
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TaphonomyofArthropodsinAmber
ArthropodsfoundinTertiaryambersaregenerallycloselyrelatedtolivingrepresentatives,
buttoday,resinousforestssimilartotheTertiaryamberforests(e.g.,Balticamber,Sicilian
amber)arenon–existent,ortheyhavebeenalteredbystronganthropogenicimpact(Domini-
canamber).OneexceptionisMexicanamber.TheextantforestofthePacificcoastofSouthern
Mexico,inthestateofChiapas,inthebiospherereserve“LaEncrucijada”(Fig.1),showsgreat
similarityoffloralcompositionwiththeformeramberforest,characterizedasatropicallow-
landareaclosetomangroves[8,18].Inthisarea,almostallofthelivingplantswerealsorecog-
nizedbyGraham[19],Martínez–Hernández[20]andLangenheim[18]fromthepalynological
recordoftheamberbearingsediments[8].ThisincludesthegenusHymenaea,whichisthe
originalresinproducingtreefortheMexicanandDominicanambersandcopalfrommanyre-
gionsinSouthAmerica,MadagascarandEastAfrica.ThediversityoftheextantfloraofChia-
pashasbeencompiledbyBreedlove[21];additionally,thefloraandfaunafromthebiosphere
reserveweresummarizedbyCarabiasLilloetal.[22].Theconspicuoussimilarityofthefloral
compositionoftheseextantforeststotheformerforestsofMexicanamberprovidedtheoppor-
tunitytocomparethelivingfaunawiththefossilamberfauna,toaddressanalysesofthetapho-
nomicalbiasesandfiltersduringthefossilizationprocess.
MexicanandDominicanambersbelongtotheMiddleMiocene[8,23–25],aperiodof
warmandoptimalclimateconditionsformanyorganisms.Mexicanamberisoneofthemost
importantamberdepositsoftheworld,andtogetherwithDominicanamber,itprovidesde-
tailedinformationabouttheevolutionofbiodiversityandthedevelopmentofterrestrialeco-
systemsintheCentralAmericanandCaribbeanarea.However,foracomprehensive
reconstructionoftheancientamberforestitisnecessarytoobtainnotonlysystematic,
palaeoecologicalandbiogeographicalinformationfromtheamberanditsinclusions,butalsoa
betterunderstandingofthetaphonomicprocessesthattransferadiverselivingcommunity
intoafragmentaryfossiltaphocoenosis.
Tostudythoseprocessesmorethan50,000recentarthropodshavebeencollectedfrom
sevendifferenttypesoftrapsplacedintwocollectionsitesinChiapas,Mexicoandcompared
toalmost3,000Mexicanamberfossilarthropodspecimensfromvariousinstitutions.Besides
taphonomicstudies,thepresentworkisalsoananalysisofthearthropoddiversityofthebio-
spherereserveforestasanintrinsicresultofthecollectingwork.Thedistributionofthecollect-
edfaunawasstudiedintwodifferentcollectionareasinordertocharacterizespecialhabitats
andcomparethemwiththefaunafromtheformerMexicanamberforest.Sincethehabitat
characterizationdependsalsoontheseason,thefieldworkwascarriedoutduringthetwo
principalseasons,therainyseasonandthedryseason;theconditionsdifferedmainlyintem-
perature,humidity,durationofsunlight,numberofpredators,andlifecyclesofsome
arthropods.
Thepresentworkhighlightsthedifficultyoffindingatrapresemblingamber–formingresin
anditsfunctionasanentomologicaltrap,andthedegreetowhichtheamberfaunaisrepresen-
tativeofthetotalpotentialfaunaldiversityfromaformeramberforest.Basedonthesimilarity
oftheformerMioceneMexicanamberforestwiththelowlandforestinthesouthofMexicowe
testdifferenthypothesesonthebiasofamberfaunasmorerigorouslycomparingthefollowing
variables:1)collectingsites,howdifferentorsimilararebothcollectingplacesincomparison
withtheamberfauna;2)dryorrainyseason,howimportantisseasonalitywithrespecttobi-
asesofdifferenttraps;3)peculiaritiesofdifferenttypesoftraps,4)sizedistributionandguilds
oftrappedarthropodscomparedwithamber.Although,thepresentstudyhadtheintentionto
compareinclusionsinamberwithinclusioninfreshresintoo.Although,thiswasnotpossible
becauseofthesmallamountofresinproductioninthetestedtrees.
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TaphonomyofArthropodsinAmber
MaterialandMethods
Amber
The2,824Mexicanamberinclusionsusedinthisresearchforcomparisonwiththeentrapped
arthropodsbelongtofourcollections:(1)StaatlichesMuseumfürNaturkunde,(SMNS),Stutt-
gart,Germany;(2)UniversityofCalifornia,MuseumofPaleontology(UCMP),Berkeley,Cali-
fornia,USA;(3)MuseodePaleontología(IHNE),Chiapas,Mexico;and(4)Naturmuseum
Senckenberg(SMF),Frankfurt,Germany.Thelargestpartoftheworldwideavailablefossilma-
terialfromMexicanamberhasalreadybeenintensivelystudiedbySolórzanoKraemer[8].
However,twokilogramsofnewmaterialofTotolapaamber(containing107specimens),and
37piecesofPalenqueamber(containing226specimens)fromChiapas,Mexicohavebeen
addedfromanewsmallcollectionacquiredbytheNaturmuseumSenckenberg,Germany.
Forthepresentwork,wetakeallavailabledataonMexicanamberfromdifferentmuseums,
wherethecollectionsweretakenwithoutemphasisonspecialtaxaoranyotherpreviousselec-
tion(SMNScollectionandTotolapaandPalenqueamber).DataonDominicanamberspiders
havebeentakenfromPenney[15],becausethedatafromtheMexicanamberspiderswerenot
sufficienttogainastatisticallysignificantresult.DolichopodidaefromDominicanamberwere
surveyedbyDJBfromtheAmericanMuseumofNationalHistory(AMNH),NewYork.Data
onDominicanamberPsychodidaearefromGrund[26]andEDNA.
Fortheanalysisoftheambercollectionthepossiblebiasfactorofanthropogenicselection
ofspecialpiecesofamber(e.g.,withrespecttosizeandqualityofinclusions)mustbeconsid-
ered.Pike[28]hasdiscussedtheimpactofcollectingbiasindetail.Forthepresentstudythe
methodofambersamplingcouldnotbechosen,sinceitisnotpossibletocollectanadequate
amountofamberwithinclusionsinthefield.However,theanthropogenicbiasinthecollection
ofambercanbecontrolledtosomedegreebyusingunbiasedcollectionsforcomparison,
whichavoidsbothintentionalandunintentionalselectionofmaterial(e.g.[27,29]).
Recentarthropods
Theentrapmentexperimentsonrecentarthropodswerecarriedoutintwoareas.Thefirstone
islocalizedwithintheBiosphereReserve“LaEncrucijada”(Fig.1)atthesoutherncoastofChi-
apas,Mexico,referredtobytheresidentsas“Coquitos”.Thisregionislocatedveryclosetothe
coast,betweenmangrovesinazoneofconservation(ZC).Thispartofthereserveischaracter-
izedbyevergreenseasonalforest.Inthisarea,arthropodswerecollectedonandaroundBur-
seratrees,chosenforthepresentstudybecauseoftheabsenceofHymenaeainthisareaand
becauseitisalsoaresinproducingtree.Thesecondcollectionareaislocatedontheedgesof
thereserveandiscalled“LaCadena”.Inthisarea,arthropodswerecollectedonandaround
HymenaeatreesclosetoAcacoyahua15°21’N,92°41’W.Acacoyahuaislocated70mabove
sealevel;LaCadenaisnotaprotectedareaandischaracterizedbyevergreenforestbutalsoby
plantationsofcocoaandsomeotheragriculturalactivities.However,notmanyhumancom-
munitiesexistinthiszoneandalargeareaofforestremainsintact.Thedistancebetweenboth
collectionzonesisapproximately25km.MeanannualtemperatureinCoquitosis28°Candin
LaCadena27°C.TheannualprecipitationinCoquitosis2150mm,inLaCadena3600mm.
TherainyseasoniswelldelimitedbetweenMayandOctober.
Collectionmethods
Thefollowingsevencollectionmethods,representedintheFig.2,havebeenusedinbothcol-
lectionsites:
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TaphonomyofArthropodsinAmber
Fig1.Locationofcollectingsites“Coquitos”and“LaCadena”inChiapas,Mexicoandinredlocation
ofthemostimportantambermines,Simojovel,Chiapas.
doi:10.1371/journal.pone.0118820.g001
1. Arborealphoto–eclectorproducedbyEcoTech(hereafternamed“eclector”):Theeclector
trapswerechosensincetheyaresuitableforcatchingawiderangeofarthropodsontree
trunks(e.g.,wood–inhabitingspeciesandspeciesmovingaroundonbark,branches,etc.).
Theeclectoroperateswithahigh–gradesquareframeworkofsteelthatisfastenedoverthe
holdingdevicetothetrunk.Animalsthatfallwithintheeclectorsofthetrunkortheside
panelsofthetrapsystemcanlikewisebeseized.Theeclectortrapsusedforstandingand
fallentrunkshaveadiameterrangingfrom0.2to0.8m.
2. Stickytrap:The7.5x20cmyellowandtransparentstickytraps,odourlessandwithanin-
secticide–freestickymixtureareespeciallysuitableforcatchingthefaunaaroundthetrees.
Theycanbeacquiredfromagronomicproductstores.Stickytrapswereplacedhomo-
geneouslyfromthebasetothreemetershighineachtree.Arthropodsfromthestickytraps
werefirstdissolvedingasolineandthentransferredtoethanol.Becauseyellowandtrans-
parentwerenotstatisticallydifferent,botharehereafternamed“stickytrap”.
3. Pitfalltrap:Forpitfalltrapsweusedsmallplasticcups,whichareeasytofindeverywhere.
Theywereburiedinthesoilaroundthetestedtrees.Theyareespeciallysuitableforcatching
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TaphonomyofArthropodsinAmber
Fig2.Graphicrepresentationoftheusedtraps.STStickytrap,EOEclectortrapopen,EEclectortrap,MMalaisetrap,PTPitfalltrap,LTLighttrap,SN
Sweepnetting.
doi:10.1371/journal.pone.0118820.g002
ground–dwellingarthropods,particularlyspringtailsandgroundbeetlesbutalsomites
andants.
4. OpeneclectorsproducedbyEcoTech:Theopeneclectorisakindofeclectormadefortrees
thatarefallenontheground.Likethephoto–eclector,anopeneclectorcatchesawiderange
ofarthropods,suchasthoselivingindeadtreetrunks.
5. Malaisetrap:MalaisetrapswereacquiredfromBioform.AMalaisetrapisalarge,tent–like
structuretrapthatwaschosenbecauseitisespeciallysuitableforcatchingawiderangeof
principallyflyinginsectslikeHymenopteraandDiptera.Malaisetrapswerelocatedvery
closetothetreesandabout20mfromwaterbodies.
6. Lighttrap:ThelighttrapswereconstructedwithahangingbuckettrapacquiredfromBio-
formandLSDlampswithbatteriesfortwodays.Theywerecleanedandthelampwas
changedeverytwodays.Lighttrapswerechosenbecausetheyattractnocturnalactiveflying
andterrestrialarthropods.Incombinationwithhangingbucketsitwaspossibletohave
smalllighttrapsinalltheinvestigatedtrees.
7. Sweepnetting:Traditionalsweepnettingsampleswereusedforcollectingarthropods
aroundthetreesuptoadistanceofabout5mormore,inordertoconsiderthefaunaofthe
associatedvegetation.Collectionbythismethodwaspossibleonlyduringthedayanddur-
ingthetimewevisitedthecollectionplaces.
OneeclectorandoneMalaisetrapwereinstalled,alongwithfourlighttraps,tenstickytraps
collocatedonthetrunkandbranches,andfourpitfalltrapsforeachtree.Thekillingagentfor
eclectors,Malaise,Lighttrap,andpitfalltrapwasalcohol.Theeclectorswereplacedonthe
principaltrunkatabout4mheight.Thetrapswereinstalledoneachtreefortwoweeksand
specimenswerecollectedeverytwodays.Stickytrapswereinstalledforoneweek.Three
HymenaeacourbariltreesinLaCadenaandthreeBurserasimarubatreesinCoquitoshave
beenchosenforperformingthetrappingexperiments.TheBurseratreesweregrowingvery
closetothemangroveswampsandtheHymenaeatreesgrowabout25kmaway,nearthebor-
deroftheBiosphereReserveandclosetoariver.Finally,arthropodswerealsocollectedwith
“openeclectors”fromafallentrunkfoundineachcollectedarea.Thetreeswerebetween20
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TaphonomyofArthropodsinAmber
and30mapartfromeachother.Threecollectiontripsweremade:oneduringthedryseason
(April2011)andtwoduringtherainyseason(June–July2010,May–June2012),coveringthe
twomostimportantseasonsoftheregion.Fortherecentcollectionsthesameconditionswere
maintainedforalltrapsasfarasitwaspossible.Thearthropodswerestoredinglass–screw–
topvialsin70%alcohol.Allthespecimensweresortedattheorderlevel;forDipteraandAra-
chnidaalsofamilies,forthefamilyFormicidae(Hymenoptera)subfamiliesandforthefamilies
Dolichopodidae(Diptera)andPsychodidae(Diptera)evengenerahavebeenidentified(see
TablesA–FinS1File).Thebody,fromtheheadtotheendofabdomen,ofRecentandfossil
specimenswasmeasured.Formeasurementaprogressiveclassificationwasused:0–1mm,
1–2mm,2–3mm,3–4....to30mm,whichisthelargestsizeofanarthropodfoundintheana-
lyzedcollection.ForguildclassificationweusedthemethodestablishedbyMoranandSouth-
wood[30].TheNationalInstituteofEcology(SEMARNAT)inMexico,gavepermissionfor
thecollectionoflivingarthropodsfortheworkpresentedhere.Allarthropodswillfinallybe
housedintheBiologyDepartmentattheNationalUniversityofMexico(UNAM),Mexico
City,curatedbyProf.JuanJ.Morrone.
Comparisons
Clusteranalysis.Amberdataandlivinginsectdatawereincludedinaclusteranalysistocom-
pareallentomologicaltrapswiththeambertrap.FollowingHenwood[14],theclusteranalysis
distancesbetweensampleswerecalculatedusingtheManhattandistanceandthemethodused
wastheUPGMC,whichisthemostsuitablemethodtocomparetwopopulations[14].Howev-
er,tocompareourresultswithPenny[15]weusedalsotheBray–Curtisindex,whichisamod-
ifiedManhattanmeasurement.Bray–Curtisindexdiffersonlybyaconstant,incaseof
comparingpercentagestheconstantistwoandtheEuclideandistance,whichisusuallynot
takenintoaccountbecauseofthelackofdata;thismethodismoresensitivetothedissimilarity.
Inaddition,Euclidianmeasureisadirectmeasureofthedissimilarity,suchthatthisanalysis
canbeusedtoqualifythedatabycomparingthethreemethods.Fig.3showstheclustering
analysisforthethreedifferentmethodsforthetwochosenecologicalregionsinChiapas.
Toestimatethedegreesfordiversityofthedifferenttraps,weusedrarefactionanalysis(see
[31]).Thismethodconsistsofgeneratingatheoreticalcurvethatestimatesthenumberoftaxa
found.Forthisestimation,thenumberofspecimenswithinthecollectionistakenintoaccount.
Withthistheoreticalcurveitispossibletocomparethequantityoftaxaforallcollectionmeth-
ods,evenifthenumberofcollectedspecimensisdifferent.
ResultsandDiscussion
DespitethedifferenceofsizeofthecollectionsbetweenCoquitosandLaCadena,withLa
CadenaprovidingalmosttwicethenumberofspecimensincomparisonwithCoquitos,the
percentageofmostofthetrappedordersandfamiliesissimilarinbothareas(Tables1and2).
Bothcollectionplacesaretosomedegreedissimilar.Climaticconditionslikehumidityand
temperatureandfloralcompositionaredifferent(seeMaterialandMethods–recentarthro-
pods).Theseparametersplayanimportantroleforchangesinthediversityofarthropods.
HymenaeaforexamplewasonlyfoundintheevergreenforestinLaCadenaandaquaticEphe-
meropteraandTrichopteraareclearlybetterrepresentedinLaCadena(Table1),wherethehu-
midityishigherthaninCoquitosandafreshwaterstreamisrunningclosetotheHymenaea
trees.SomeDipterafamilieslikeMycetophilidaeorChironomidae,whichpreferhumidhabi-
tats,arealsobetterrepresentedinLaCadenathaninCoquitos(Table2).Ourambercollections
showthatwithinallinsectsattheorderlevel,Dipteraatfamilylevel,andArachnidaatfamily
level,goodagreementexistswithbothCoquitosandLaCadena(Figs.4,5,6).
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Fig3.Clusteranalysistocompareallentomologicaltrapswiththeamber.a)Manhattandistanceforall
orderscollectedinCoquitos,b)Bray–CurtisforallorderscollectedinCoquitos,c)Euclideandistanceforall
orderscollectedinCoquitosd)ManhattandistanceforallorderscollectedinLaCadena,e)Bray–Curtisforall
orderscollectedinLaCadena,f)EuclidiandistanceforallorderscollectedinLaCadena.STStickytrap,EO
Eclectortrapopen,EEclectortrap,MMalaisetrap,PTPitfalltrap,LTLighttrap,SNSweepnetting.
doi:10.1371/journal.pone.0118820.g003
Wecollectedinthedryandrainyseasonforthreeyearsindifferentmonths,sothatthedata
canbeinterpretedasbeingrepresentativeofregionalseasonality.Acomparisonattheorder
levelbetweenbothseasonswiththefaunaincludedinamberwasnotinformative,evenifwe
analysedgroupssuchastermites,whichareindicativeforaspecificseasonandabundantin
Mexicanamber.AccordingtoGomesdaSilvaMedeirosetal.[32]termites,synchronizedflight
occursindifferenttimesoftheyearinBrazil,butthepeakcoincideswiththeonsetoftherainy
season.Inourcollectiontermiteswereclearlymoreabundantduringtherainyperiod,princi-
pallyatthebeginningofthewetseasonduringMay.However,thetotalMexicanamberfauna
appearstoresembleamixtureofbothrainyanddryseasonfaunas.Seasonalitywasalreadyevi-
dentduringtheMiocene[33]intheAmazonianforestandaccordingtoJaramilloetal.[34]
theclimateinthelowlandforestoftheNeotropicswasalsosimilartotoday.Resinproduction
ofHymenaeatreesdependsofseveralgeneticandenvironmentalfactors.Themassiveamount
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TaphonomyofArthropodsinAmber
Table1.TotalarthropodscollectedinChiapas,Mexicowith7differententomologicaltrapsintherainyseasonaswellasinthedryseason.
Order SumofCountCoquitos %ofTotalCoquitos SumofCountLaCadena %ofTotalLaCadena
Diptera 7378 45.715 16852 48.812
Hymenoptera 2622 16.246 3748 10.856
Coleoptera 1554 9.628 3201 9.271
Collembola 1032 6.394 2991 8.663
Acari 849 5.260 2630 7.617
Lepidoptera 716 4.436 1092 3.163
Hemiptera:Auchenorrhyncha 576 3.568 1051 3.044
Aranea 488 3.023 730 2.114
Psocoptera 252 1.561 447 1.294
Heteroptera 180 1.115 400 1.158
Thysanoptera 136 0.842 373 1.080
Isoptera 127 0.786 333 0.964
Orthoptera 95 0.588 282 0.816
Blattodea 67 0.415 147 0.425
Hemiptera:Sternorrhyncha 31 0.192 115 0.333
Embidiina 12 0.074 49 0.141
Isopoda 9 0.055 21 0.060
Neuroptera 6 0.037 19 0.055
Pseudoscorpionida 5 0.030 18 0.052
Scorpionida 3 0.018 15 0.061
Ephemeroptera 1 0.006 4 0.011
Trichoptera 0 0.000 3 0.008
Mecoptera 0 0.000 2 0.005
Diplopoda 0 0.000 1 0.002
Chilopoda 0 0.000 0 0.000
TOTAL 16139 100 34524 100
doi:10.1371/journal.pone.0118820.t001
ofBraziliancopalfromAmazoniaisoftenattributedtoH.courbaril[35]butprobablyalsode-
rivesfromH.oblongifoliavar.palustris(Ducke)LeeandLangenheiminperiodicallyinundated
areas.Hymenaeaspp.thatgrowinmoistforestsorclosetostreamsapparentlysynthesizes
greatestquantitiesofresin,whereasspeciesthatliveindryforestsproducelessquantityof
resin,buttheyproducerelativelymoreduringthewetseasonthaninthedryseason[36].
Thus,theamberfromH.mexicana,theoriginplantofMexicanamber[37],generallycould
haveproducedresincontinuously,inwetanddryseasons.
TheformerMexicanamberforesthasalreadybeencharacterizedasalowlandforestnearby
mangroves[8,18],andtheDominicanamberforestasalowlandmoreinteriorneotropical
rainforest[3].However,thechironomidsStenochironomusandXestochironomus,freshwater
organismlivinginmountainstreamshavebeendescribedinDominicanamber[38].Boththe
extentoftheoriginalamberformingforestandthedistributionofHymenaeaduringtheMexi-
canMiddleMioceneisunknown.Hymenaeawasmostprobablydisseminatedbythesea,
reachingthecoastofSouthAmericaandthesouthofMexicoduringtheearlyCenozoic[39].
Today,somespeciesofHymenaeaarefoundalongthecoastgrowinginsandysoilsanddrier
ecosystems,whileotherspeciesofHymenaeagrowmainlyinevergreenforestecosystems[39].
MostofthecurrentlyknownMexicanamberhasbeenderivedfromtheareaofSimojovelde
AllendeinthestateofChiapas,southernMexico.However,moreminesareappearinginother
municipalitiesofChiapas[9].TheamberfromtheTotolapaandPalenqueregionsisgenerally
PLOSONE|DOI:10.1371/journal.pone.0118820 March18,2015 9/24
TaphonomyofArthropodsinAmber
Table2.TotalofFamiliesofDipteracollectedin“LaCadena”inChiapas,Mexicowith7differententomologicaltrapsintherainyseasonaswell
asinthedryseason.
Family SumofCountCoquitos %ofTotalCoquitos SumofCountLaCadena %ofTotalLaCadena
Culicidae 276 3.740 107 0.634
Ceratopogonidae 577 7.820 404 2.397
Chironomidae 307 4.161 1290 7.654
Psychodidae 464 6.288 631 3.744
Anisopodidae 0 0.000 1 0.005
Chaoboridae 0 0.000 2 0.011
Limoniidae 34 0.460 219 1.299
Tipulidae 0 0.000 6 0.035
Cecidomyiidae 952 12.903 5464 32.423
Sciaridae 414 5.611 3716 22.050
Keroplatidae 0 0.000 51 0.302
Mycetophilidae 29 0.393 422 2.504
Drosophilidae 2403 32.569 942 5.589
Muscidae 30 0.406 22 0.130
Asilidae 10 0.135 5 0.029
Phoridae 599 8.118 1899 11.268
Dolichopodidae 815 11.046 312 1.851
Tabanidae 46 0.623 2 0.011
Stratiomyidae 6 0.081 13 0.077
Scatopsidae 10 0.135 7 0.041
Tephritidae 0 0.000 11 0.065
Micropezidae 66 0.894 11 0.065
Empididae 50 0.677 46 0.272
Corethrellidae 0 0.000 3 0.017
OtherBrachycera 285 3.862 494 2.931
OtherNematocera 5 0.067 424 2.516
Total 7378 100 16852 100
doi:10.1371/journal.pone.0118820.t002
similarinfaunalcompositiontothatoftheSimojovelareaandtheyareprobablyofthesame
age[40,41].Thereare,however,somesignificantdifferences.Firstly,thelevelofpreservation
isparticularlygood,andsecondlymorethan7%ofthetotalsareaquaticinsects,likeEphemer-
opteraandTrichoptera,incomparisonwiththestudiedamberfromSimojovelwhichcontain
about2%aquaticinsects.
Theseresultsunderlinetheimportanceofanewanalysisofthepalaeoenvironmentofthe
Mexicanamberforest,comparedwithnewambermaterialfromnewcollectionsites.Probably,
theprincipalcongregationofHymenaeatreeswaswithinthelowlandforest,closetotheman-
groveforest.However,theamberforestprobablycoveredawiderareawithconditionsvery
similartotodayintheCentralandSouthAmericanlowlandforest.
Whichtrapisthemostsimilartotheamber?
Withthecollectedarthropodsfrombothcollectingareas,weobtaineddendrogramscomparing
alldifferenttypesoftrapswitheachother.Nosignificantdifferenceswerefoundbetweendif-
ferentmethodstoproducethecluster(UPGMC,UPGM,andsinglelinkage–clustering)aswell
asbetweendifferentdistancemeasures(Manhattan,andEuclidean),showingthatthediffer-
encebetweentrapsarelargeenoughtobedetectedwithourdata.Asexpected,both,
PLOSONE|DOI:10.1371/journal.pone.0118820 March18,2015 10/24