•Reviews•

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ExceptionallypreservedbrachiopodsfromtheChengjiangLagerstätte(Yunnan,China):

PerspectivesontheCambrianexplosionofmetazoansZHANGZhiFeia,b∗　HOLMERLarsErikc

　　∗ Correspondingauthor.Tel:+862988303553;fax:+862988302128.E-mail:elizf@nwu.edu.cn,zhangelle@126.com

aStateKeyLaboratoryofContinentalDynamics,EarlyLifeInstitute,NorthwestUniversity,Xi’an710069,China

bLPS,NanjingInstituteofGeologyandPalaeontology,ChineseAcademyofSciences,Nanjing210008,China

cDepartmentofEarthSciences,Palaeobiology,UppsalaUniversity,Villavägen16,SE-75236Uppsala,Sweden

Abstract　TheCambrianexplosionwascoinedtodescribethegeologicallysuddenappearanceofnu-merousbilaterianbodyplans (Phyla)aroundtheEdiacaran-Cambrian transition,around 565-520millionyearsago.Manyexplanationsandconjec-tureshavebeenpostulatedinordertoexplainthepatternanddurationofthisexplosiveradiationofmanydifferentphylaofearlymetazoans.Here,wefocusontheevolutionofaphylumofmarinesus-pension-feedinganimals—thebrachiopods,asex-emplifiedbytheexceptionallypreservedtaxafromthecelebrated Chengjiang KonservatLagerstätte(Yunnan,China).Theabundantsoft-bodiedpres-ervationatthesefossilquarriesgivesustheonlyfirminsightsintowhatbrachiopodslookedlikeandhowtheyfunctionedandlivedwhentheyfirstap-pearedontheEarth.StudiesofChengjiangbrachi-opodsdemonstratethattheearlyanimalsdevelopedaremarkablyvariedorganizationoftissuesandor-gansshortlyaftertheonsetofCambrianexplosion.In the marine suspension-feeding brachiopods,mostimportantlythetentaculatefeedingstructureofearlybrachiopodsisalreadydifferentiatedintotwoshapesoflophophore,anteriorlycoiled (spi-ralled)andposteriorlyarchingtentaclecrownsandtheuniquelattertypewaspreviouslynotdocumen-tedfromfossilandlivingbrachiopods.AlsounlikeanyknownRecentbrachiopod,alltheknownCam-brianbrachiopodsfrom Chengjianghaveanopendigestivetractthatwasdisposedeitherasa U-shapedgutinlinguliformandstemgroupbrachio-pods,orstraightgutwithaposterioranusinsomecalcareous-shelledstocks.Moreover,incontrastto

livinglingulids,alltheCambrianbrachiopodshaveanepibenthiclifestyleeithercementedbyaventralvalveorattachedbyvariablepediclestoestablishcomplexecologicalcommunityencompassingpri-marytierersandvariablesecondarytierers.Itisthereforeassumedthatbrachiopodswerethefirstbenthicmetazoanthatachievedtheirsuccessinec-ologicalstratificationandtieringcomplexitybylateAtdabanian.Thesetaearealsoimportantforthebrachiopodsuspension-feedinglifestyle,andintheChengjiangbrachiopodstheyincludetwotypes—cilia-likeandspine-likesetae.Themantlecanalsofdifferentbrachiopodspeciesarealsodistinctlyvariableinarrangement,mainlydisposedinpinnate,baculateandperipheralconditions.Ofthese,theperipheraldis-positionofmantlecanalsisforthefirsttimeproposedheresoastodifferentiatefromthebifurcateconditioninrecentlingulidsinthattheformerisdevoidofposte-riorlyextendingmaintrunksofsinus,butpossessesadivergingdorsalvasculamediaindichotomy.

Keywords　Cambrianexplosion;Chengjiangfauna;Metazoans;Brachiopods;Soft-tissuepreservation

1.Introduction

　　Thesuddenappearanceofmostmodernanimalbodyplansandtheextenttowhichtheyarecoinci-dentwiththeCambrianexplosion (inbothspeedanddimension)haslongbeenhotly-debatedtopicsofincreasinginterests[1—3].Numerousexplana-tionshavebeenproposedforunderstandingthe

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disparity (phylum: morphological distinctness)anddiversity(thenumberofspeciesinaphylum)andthetempoandpatternoftheexplosiveradia-tionofessentiallyallofthereadilyfossilizableani-malbody plansaroundthe Ediacaran-Cambrianboundary[4—6].Actually,anunderstandingoftheevolutionofphylaofmetazoans,inparticularwhattheylookedlikeandhowtheyfunctionedandinhabitedwhentheyfirstappearedontheearth,exclusivelyre-liesonhavingafossilrecordwithexceptionalpreserva-tion[2,7,8].Accordingly,fossilswithexceptionalpreservationhavelongkeptexcitingscientificinterestsandcuriositiesnotonlyfromthescientistsbutalsofromthepublicbecauseoftheirpotentialtoelucidatingusuallyunobtainableaspectsoforganism’sanatomy,behaviour,ecologyandevolution[9—12].

The Brachiopoda,comprisingatleast4800knowngenera(asdescribedintherecentlyrevisedtreatise)isoneofthemostsuccessfulinvertebratephylaintermsofabundanceanddiversityanddu-

rationinthegeologicalhistory [13].Theyap-pearedfirstintheEarlyCambriananddiversifiedthroughoutthePaleozoic,whentheydominatedthelow-level,suspension-feedingbenthichabitants[14].Todayapproximatelyonly180generastillsurvive,buttheycanlocallybeabundantinsomerestrictedrecenthabitats [13].Therefore,thelargemajorityoftheknownbrachiopodgeneraareexclusivelyknownfromtheirmineralizedshellsaspreservedinthefossilrecord.Incontrast,ourknowledgeofbrachiopodanatomyreliesheavilyonanalogieswiththeirextantrelativesduetothefactthatfossilsoft-tissuepreservationisverysparse[15].Recently,therecordsofsoft-partpreserva-tioninbrachiopodshaveincreasedwithoccurrencesintheOrdovicianandSilurian [16—20](Figure1).Nevertheless,mostofthesoftpartsrestrictedtofossilizedpedicles,notablyfromtheexceptionalCambriandeposits,suchastheBurgessShaleandChengjiangLagerstätten[21—24].

Figure1　Theoccurrenceofsoft-partpreservationofbrachiopodsingeologicalrecords.

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　　Untilnow,onlytwospeciesoflingulatesareknowntohavepediclespreservedintheclassicBurgessShalefauna [25,26].Incontrast,theChengjiangLagerstättenissuperblyextraordinary,andhasdis-tinctlysurpassedtheBurgessShaleintheexceptionalpreservationofbrachiopodsinthatthebrachiopodin-ternalanatomy,suchastheorganizationofthelopho-phoreanddigestivetractwereaswellpreservedwithexquisitefidelityindifferenttaxaofbrachiopodsinclu-dingthephosphatic-shelledandcalcareous-shelledspe-cies[15,23,24,27—29].Theremarkablediscoveryofexquisitelypreservedsoft-tissuesofbrachiopodshasintroducedanentirelynewlineofevidenceonthechar-acterstatesofinternaltissuesandorgansinearlybra-chiopods[21].ThesefossilsfromtheChengjiangfau-narepresenttheoldestevidenceonbrachiopodanato-my,andshedmuchlightonthecharacter-stateofin-ternaltissuesshelledbytwobiomineralizedvalves.Here,wesummarizethefindingsofsoftpartsillustra-tedinChengjiangbrachiopods,andoutlinethemor-phologicaltypesofsetae,mantlecanals,digestivetracts,lophophore,andpediclesofearlybrachiopodstocks.Inaddition,coupledwiththoseofrecentbra-chiopodsthesecharacteristicsarediscussedinsystem-aticandphylogeneticcontext.

2. Summary of the Chengjiang Fossil-Lagerstätte

TheChengjiangFossil-Lagerstätteisanexcep-tionalconservationdepositthatcontainsavarietyofa-bundantsoft-bodiedandbiomineralizedmetazoansre-presentingoneoftheearliestrecordsofCambrianex-plosion.ThefossilsarerecoveredfromthemudstoneoftheYu’anshanMember(Eoredlichia-WudingaspisTrilobiteZone),i.e.theupperpartoftheEarlyCam-brian Heilinpu (formerly Qiongzhusi)Formation,widelyexposedinawideareaaroundtheDianchiLakeofKunming(Figure2(a),(b)).Thestrataareordi-narilycorrelatedwiththelateAtdabanianorBotomanStageinSiberia,belongingtothenewlyunnamedCambrianStage3.Sofar,morethan10fossilquarrieswerefoundandmadeofheavyexcavationbythework-inggroupoftheEarlyLifeInstituteinNorthwestUni-versity, Xi’an of China. Studies of ChengjiangLagerstätterevealedmorethan200speciesofanimalsamong18phyla(Figure2(c)),ofwhicharthropodsincludingAnomalocardiidspredominatinspeciesabun-dance,markedlyexceeding100species[30].

Figure2　(a)MapshowingthefossillocalitieswheretheChengjiangfaunawasexcavated;(b)stratigraphicalcorrelationofthemud-richdepositsyieldingtheChengjiangfaunaincludedintheJianshansectionatHaikou,Kunming,China;(c)anewphylogeneticframeworkmodifiedfromEdgecombe(2011)[36]toshowtheoccurrencesofvariousmetazoansinChengjiangfaunaandtheirspeciesdiversity.

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　　TheChengjiangLagerstätteisveryimportantbecauseitnotonlyexpandsthetemporalandgeo-graphicdistributionofBurgessShale-typefaunas,butalsocontainsaseriesofexquisitelypreservedtaxathathaveradicallychangingourunderstand-ing of deep history ofsomeimportantanimalgroups,suchasChordataincludingtheagnathan-like Myllokunmingia and Haikouichthus [31,32].ItisintheChengjiangdepositsthatnearlyalltheCambrianrepresentativesofdeuterostomewererecovered[33],bycontrastintheclassicBurgessShaleonlytwogeneraofdeuterostomeshavebeendescribedindetail[34,35].Inaddition,thepres-ervationofsoft-tissues,suchasthelophophoreanddigestivecanal,ofbrachiopodsislargelyonlyknownfromtheChengjiang.

3.Brachiopodsandtheirsoftbodypreserva-tionintheChengjiangLagerstätte

3.1　GeneralcharactersofbrachiopodsThebrachiopodsareagroupofmarinesolitary

coelomateinvertebrates,withtheirsoftbodyen-closedinsideashellconsistingofapairofvalves,bothofwhichexhibitbilateralsymmetry,butdif-fersinsize,shape,andevenornamentation[37].Posteriortotheshell,thereisavariablydevelopedfleshystalk-likepedicle.Thespaceinsidetheshellisdividedintotwosections,i.e.theanteriorman-tlecavityandtheposteriorbodycavity.Thebodycavityaccommodatesthedigestiveandreproductiveorgansandmusclesystems.Themantlecavityisseparatedfrom thebodycavity bytheanteriorbodywallandlargelyoccupiedbythesuspension-feedingorganoftheciliatedlophophore.Brachio-podspossessenclosedtubularcirculatorysystem-mantlecanalsthatlinetheinnersurfaceofthevalves.Ourknowledgeofbrachiopodcharacteris-ticsandsoftanatomyreliesheavilyonanalogieswiththeirlivingrepresentatives[37],yetthesea-nalogieshavebeenuntestedregardingtheearlystocks.Inarecentdecade,aseriesofsoft-bodiedcharactersetshavebeenrecordedindifferenttaxaofbrachiopodsfromtheChengjiangfauna.What

theylookedlikeandhowtheylivedtogetherareal-sorevealedinsomefossilsexceptionallypreservedinsitu [11].

3.2　TheChengjiangbrachiopodsandthemor-phologicalvarietyoftheirsoftbodycharacteristics

Untilnow,10speciesofbrachiopodshavebeenreportedfrom theCambrian(Stage3)ChengjiangmuddydepositswidelyexposedinawideareaaroundKunming,easternYunnan(Figure2(a),(b))[38].Ofthem (Table1),Lingulellachengjiangensis[39]andLingulellotretamalongensis [39,40]havecharacteristiclinguloidfeatures,assignedtotheSuperfamilyLinguloideaoftheClassLingulata.Diandongiapista [41,42],themostabundantandmineralizedlingulatebrachiopodsintheChengjiangfauna,istheonlyrepresentativeoftheFamilyBots-fordiidaeasithasaventribiconvexshell withaslightlyconicalventralvalve.Xianshanellahaik-ouensis[43]isamuchmoreproblematiclingulid-likebrachiopod.Itwasoriginallyreferredtoasanobolidonaccountoftheroundedshellshapeandthesmallventralpseudointerareacharacteristics,butpresenceoflongandhollowspine-likesetaealongtheshellmarginmaypermitustopossiblyassignittoOrderSiphonotretida.TheorderAcrotretidaisrepresentedbyKuangshanotretamalungensis[44]whoseoccur-renceisslightlyyoungerthanthemuddydepositsthatyieldthehigh-diversityandrich-abundancesoft-bodiedChengjiangfauna.Apartfromtheorgano-phosphaticlinguliformbrachiopods,severaltypesofcalcareous-shelled (Rhynchonelliformea) brachio-pods have been described,including Kutorginachengjiangensis [15],Alisina.Sp [29]andthechileate brachiopod stem group Longtancunellachengjiangensis [24]fromtheChengjiangfauna,thoughtheyareovershadowedinabundancebythecoevallinguliformcousins [21].Inaddition,TheChengjiangfaunaalsocontainstwobizarresessilebenthosaffiliatedwiththebrachiopodstems,inclu-dingHeliomedusaorienta [22,45—47]andtheproblematicbrachiopodformerlydescribedastheno-mennudum “Wangyuiachengjiangensis”[28],but which have never been described formallyuntilnow.

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Table1　Taxonomy,high-disparityandlower-diversityofbrachiopodsrecoveredfromtheChengjiangLagerstätte(Cambrian,unnamedStage3),Yunnan,southwesternChina

Subphylum Class Order Superfamily Family Genera/species

Linguliformea Lingulata

Lingulida Linguloidea

ObolidaeLingulella?

chengjiangensis

LingulellotretidaeLingulellotretamalongensis

Botsfordiidae Diandongiapista

? Siphonotretida Siphonotretoidea ? Siphonotretidae? Xianshanellahaikouensis

Acrotretida Acrotretoidea AcrotretidaeKuangshanotreta

malungensis

Rhynchonelliformea

Kutorginata Kutorginida Kutorginoidea KutorginidaeKutorgina

chengjiangensisObolellata Obolellida Obolelloidea Trematobolidae Alisina.sp

Chileata Chileida ? ? Longtancunellachengjiangensis

StemgroupHeliomedusaorientaYuganothecaelegans

　　InthebrachiopodsrecoveredfromtheChengjiangfauna,thesoftpartpreservationismainlyrestrict-edtothesensoryfringeofsetae,thecirculatorysystemofmantlecanals,feedingorganizationoflophophore,thedigestivesystemandtheattach-mentstructureofpedicle(Table2)[21].Basedontheexceptionallypreservedfossils,themorpholog-

icaltypesoftheabovetissuesororgansaresum-marizedbelow.Inconjunctionwithstudiesofliv-ingrepresentatives,anattemptismadetodiscusshowtopolarizethemorphologicalcharactersandlifestylesintheevolutionarycourseofseparatecladesofbrachiopodstocksinthegeologicalhisto-ry.

Table2　OccurrencesandcharacterstatesofthesoftpartsinthebrachiopodsfromChengjiangLagerstätteL.c=Lingulellachengjiangensis;L.m=Lingulellotretamalongensis;D.p=Diandongiapista;

K.m=Kuangshanotretamalongensis;X.h=Xianshanellahaikouensis;K.c=Kutorginachengjiangensis;AL=Alisinasp;L.c=Longtancunellachengjiangensis;H.o=Heliomedusaorienta;

Y.e=Yuganothecaelegans.√/×=presenceorabsence;Ss=slimsetae;Sps=spine-likesetae;Ac=anteriorlycoiledorspiraledlophophore;Pa=posteriorlyarchinglophophore;U= U-shapedgutwithanopeninganus;Sg=straightgut;Ba=baculatecondition;Pi=pinnatecondition;Pe=peripheralcondition;

Mp=massivepedicleattachedontohardsubstrate;Tp=Thinpediclewithbulb-likeendburiedintosoftsediments.

L.c L.m D.p K.m X.h K.c AL L.c H.o Y.e

Setae√/× √ √ √ × √ √ √ √ √ √

States Ss Ss Ss Sps Ss Ss Ss Ss Ss

Lophophore√/× √ √ × × √ √ √ √ √ √

States Ac Ac Ac Ac Ac Ac Pa Ac

Gut√/× √ √ × × √ √ × √ × √

U U U Sg U U

Mantlecanals√/× √ √ √ × √ √ × √ × √

States Ba Ba Pe Pi Ba Pi Pi

pedicle√/× √ √ √ √ √ √ √ √ × √

States Tp Tp Tp Tp Mp Mp Mp Mp Tp

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　　3.2.1　SetaeSetaecanbefoundasahair-likefringealongthe

marginaledgeofshellvalves,probablyeitherfunc-tioningprimarilyasextendedsensoryorgansorser-vingasatactilesieveforthemantlecavity[48].Inthelivingbrachiopods,thereisnocomprehensivere-centstudyofthesetae,butthosethatareknownshow somevariationfrom onespeciestoanother[37].Thesetalfringecanextendbeyondtheshellmarginuptoseveralmillimeters,butshowvaria-tionsinlengthatdifferentportionofshellmargin.Forexample,thesetaeintheinfaunalLingulahavelongestsetae anteriomedially and posterolaterally[27].Theanteriorfringesofsetaeclusterandhelptheanteriorshellgapetoformthreepseudo-siphonssothatthelivinglingulidshaveanormalinfaunallifewithtwoinhalantcurrentsatbothlateralcornersandoneexhalantcurrentatmedianoftheanteriorshellmargin(Figure3(a)—(d))[49,50].

Thesetaeareoneofthemostimportantsoftpartsoffossilbrachiopods.TheearliestreportsoffossilizedsplendidmarginalsetaeareofMicromitrafromref.[51].Nevertheless,adetailedstudyofthematerialfromtheBurgesShalehasnotyetbeendone.InnearlyalltheChengjiangbrachiopods,themarginalsetaearepreservedinnumerousspecimens.Thebrachiopodsetaeshowasimilarmodeofpreser-vation,allofthemfossilizedasreddish-browntintswithpyrite[22].However,thesetaeofdifferenttaxashowsubstantialdifferencesinsize,thickness,length,aswellasintheirarrangementandappear-ancearoundtheshellmargin (Figure3(e)—(j))[21].InthestemgroupbrachiopodHeliomedusaorienta,thesetaecanbereadilyrecognizedinnearlyallspecimens[22,47].InthelingulateLingulellachengjiangensis,Lingulellotreta malongensis andDiandongiapista,aswellastherhynchonelliformKutorgina chengjiangensis, Alisina. sp. andLongtancunellachengjiangensis,however,these-taearelesscommonlypreserved[15,27,29,47,52].Thisissomewhatdifficulttoexplain,butmightbeduetothedelicacyandthinnessofthesetaeinthesixgeneraofbrachiopods(Figure3(e)—(f))[27].Inthedispositionandgeneralappearance,however,theyhaveagrossresemblancetothoseofHeliomedusaorienta [22].Incontrast,thesetaeofXianshanellahaikouensis appearto bespine-like(Figure3(g)—(j))[43].Theyappeartobediffer-entfromandlookdistinctlythickerandcoarserthan

theslimlinearsetaeintheotherChengjiangbrachio-pods[21].Therefore,inthelightofevidencede-rivedfromtheChengjiangfauna,thebrachiopodse-taecanbecategorizedintotwomorpho-types,i.e.slimlinearsetae(Figure3(e)—(f))andspine-likehornysetae(Figure3(g)—(j)).Itisreasonablyconceivablethattheslimsetaecouldbesupposedlyactivatedprimarilyasanextensionoftactilesensors,butthehornyspine-likesetaetendtoprotecttheor-ganismsfromdurophagouspredation,andtopreventfromcloggingthefilteringchamberfrom ambientseawater.

WhilstthesetaeofCambrianbrachiopodsex-hibitsomevariationsinmorphology(slimandsilk-likeandhornyspine-like),theyaresimilaringrossarrangement,andfringedequidistantlyalongthemantleedge.Incontrast,inlivinglingulidsthesetaearedisposedinthreepseudosiphonsattheanteriormantlemarginwithtwolateralaperturesforinhalantwaterandonemedianforexhalantwater[50,53](Figure3(c)—(d)).Itisthereforereasonabletoassumethattheevenlyfringedsetaealongtheentiremanteledgecouldbethegroundstateofsetaeofbrachiopods,andthethree-pseudosiphonarrange-mentofsetaeseeninRecentlingulids(Figure3a—d)isapomorphicandderivedasanadaptationtoaninfaunallifestyle[21,27].

3.2.2　MantlecanalsystemAllbrachiopodspossessanopencirculatory

systemcomposedofaseriesofbloodvesselsthatcommunicate with coelomic canals and sinuses[37].Mantlecanalsaretubularextensionofthecoelom,whichpermeatethebilobedmantlesthatlinetheanteriorinnersurfacesofthevalves(Fig-ure4(a)—(d)).Withinthevascularsystemsthecoelomicfluidcirculates,primarilyusedforrespi-ration[48].Infossilsofbrachiopods,mantleca-nalsareusuallypreservedasgroovesorridgesonthesurfaceofinteriormoldsofshellvalves.How-ever,intheChengjiangbrachiopodstheycouldbeexceptionallypreservedasreddish-brownimpres-sionsontheflattenedvalves(Figure4(e)—(j)).AsidefromHeliomedusaorienta,Alisina.spandthenewlyreportedacrotretoidbrachiopodKuangshanotre-tamalungensis [44],alltheotherbrachiopodsintheChengjiangfaunahaveimprintsofmantlecanalspre-served[21].Untilnow,thereare3differentpatternsofarrangementofmantlecanalsrecognizedintheexceptionallypreservedbrachiopods.Obviously,

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Figure3　ThedistinctdispositionofsetaeinRecentandCambrianbrachiopods.(a)—(d)RecentLinglides:(a)anatomyoflivingLingula,courtesyofDr.OuQiang (Beijing);(b)reconstructionofRecentlingulidswithmarginalsetae;(c)thethree-bundlesofsetaeinalivinglingulidinlife,withtheanteriormostmarginofvavlesonlyexposed;(d)the3pseudo-si-phonsofsetaeinlife.(e)—(j)EarlyCambrianbrachiopodsfromtheChengjiangfauna:(e)theslimsetaeinLingulellotretamalongensis;(f)theslimsetaeinKutorginachengjiangensis;(g)—(h)generalanddetailedviewofsetaeinXianshanellahaikouensis,notingasmalljuvenileanimalofunknownaffinityattachedontothemarginalsetae;(i)—(j)enlargedviewofthespine-likesetaeofX.haikouensis.

thevascularmarkingsofLongtancunellachengjiangen-sisandXianshanellahaikouensisandYuganothecaelegans (unpublished material)aredisposedinapinnatecondition[21].Incontrast,themantleca-nalsofLingulellotretamalongensisandLingulellachengjiangensisappeartobeinbaculateconditionthatcommonlyseeninPaleozoicorganophosphaticbrachiopods(Figure4(e)—(h)).Therein,theyconsistsofasingleofmaintrunksintheventralmantle (vasculalateralia)andtwopairsinthedorsalvalve,onepairofvasculalateraliaoccup-yingasimilarpositiontothesinglepairintheven-tralvalveandasecondpairofvasculamediapro-jectingfromtheanteromedianbodycavitynearthemidlineofthevalve.Interestingly,thispatternofbaculatemantlecanalswasalsorevealedintheear-liest-knowncalcite-shelledbrachiopod Kutorginachengjiangensis[15].Itishoweverdifficulttoas-sertthatsuchpatternofoneventralandtwodorsalpairsofvascularcirculatorycanals,widelydevel-opedin Cambrian calcite-and phosphatic-shelledbrachiopods,isofhomologues.Nevertheless,itisinDiandongiapistathatthereissuperblyspectac-ularpreservationofmantlecanalsystem [21,41].AlthoughthemantlecanalsofD.pistaconsistoftwopairsofvasculalateraliainventralanddorsal

valvesandonepairofvasculamediaindorsalvalve,thepallialsinustrunksgiveoffbranchesan-teriorlyandperipherallytoproduceanincreasinglydensearrayofblindlyendingbranchesnearthepe-ripheryofthe mantle margin.The mantlecanalsysteminD.pistaismarkedlydistinguishedfromthebifurcateconditioninRecentlingulids(Figure4(a)—(d))[50].InRecentlingulids,thevasculalateraliainbothvalvesdivideimmediatelyafterleavingthebodycavity,withashorterbranchofeach mainpallialtrunkextendingposteriorlytosupplythemantleposterolateralofthelateralbodywall,whilethelargerbrachesextendinganteriorlyandconvergingtowardthe midlineofthevalve(Figure4(a)—(d)).BecauseoftheinvariablebranchingperipherallyindichotomyfromthemaincanaltrunksinDiandongia [41],weareinclinedtocoinanewpattern (peripheraldisposition)ofmantlecanalstodifferentiatefromthebifurcationof mantlecanalsoccurringin Recentlingulids.Nonetheless,itisapparentthatoneventralandtwodorsalpairsofcanalsrepresenttheearliestpatternofmantlecanalsinCambrianbrachiopods.Thereafter,the Ordovician Pseudolingula [54,55],thePaleozoic-MesozoicLingularia [50,56]andtheTertiarytopresentLingulaandGlottidia

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[57]haveafundamentallydifferentmantlecanalsystem:thevasculamediaareabsentandthevas-culalateralia in both valvesbecomeanteriorlysubparallel.Thearrangementofmantlecanalsinlingulatesiscloselyassociatedwiththein-andex-halantwatercurrents[49].Consequently,thein-halantandexhalantcurrentsofCambrianandRe-

centlingulidsarereasonablyassumedtobediffer-entfromeachother.Therefore,thepresenceofdor-salvasculamediaisthegroundstateofthevascularsysteminlingulidsstocks,andalackofdorsalvascu-larmediaandanincreaseinthelengthandsubsidiaryramificationofthelateralmantlecanalsareadaptationsforaninfaunalandburrowinglifestyle[21].

Figure4　Thevariousdispositionsofthemantlecanalsystem.Abbreviations:Vm=vasculamedia,Vl=vasculalateria,Vr=visceralregion,Vv=ventralvalve,Dv=dorsalvalve.(a)and(b)ThemantlecanalsofventralanddorsalvalvesofLingula(courtesyofChristianEmig(France));(c)and(d)interpretativedrawings(modifiedfromTreatise)ofventralanddorsalmantleca-nalscomparedto(a)and(b);(e)—(f)dorsalandventralmantlecanalsofLingulellachengjiangensis;(g)and(h)interpretativedrawingsof(e)and(f);(i)and(j)dorsalandventralmantlecanalsofDiandongiapista;(k)and(l)interpretativedrawingsofdor-sal(k)andventral(l).

　　3.2.3　Thefilter-feedingorganizationoflo-phophore

Thelophophoreisatentaculateextensionofthemesocoelomthatembracesthemouthbutleav-estheanusoutside.Itsprimaryfunctionsaretogenerateaninhalantandexhalantflow ofwaterthroughthebivalve-enclosedmantlecavitysoastotrapparticulatefoodmaterial,andpermitventila-tion,as wellasassistintheremovalofwasteproducts[48].Thelophophorerepresentsoneofthe mostunusually preservedsofttissues,andnearlyallthe Cambrianrecordscomefrom theChengjiangLagerstätte.Sofar,allthebrachio-podsfromtheChengjiangfauna,asidefromDian-

dongiapista andtherecentlyknownacrotretoidKuangshanotretamalongensis,haveimprintsoflophophoralarmspreserved[23,27,58].Amongtheimprintsofthelophophore,thoseinLingulel-lachengjiangensis (Figure5(a)—(d)),Lingule-llotretamalongensis(Figure5(e)—(h))andHe-liomedusa(Figure5(i)—(l))areextremelyspec-tacular.Evidently,thelophophoreofL.malon-gensisandL.chengjiangensis (Figure5(a)—(d)and(e)—(h))iscomposedoftwoanteriorly-coiledandspiraledbrachialarms[58].Theyaredisposedsymmetricallyaboutthe mouth,attachedtotheanteriorbodywall,accommodatedintheanteriormantlecavity.Interestingly,insomespecimensof

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L.malongensisandL.chengjiangensistheirlo-phophoralarmsextendedandstretchedoutoftheshellvalves(Figure5(c)and (d)).Amazingly,theciliatedtentaclescouldbealsoextraordinarilyrevealedinanumberofspecimensofLingulellot-retamalongensis(Figure5(e)—(h))[23].How-ever,thelophophoreorganizationofHeliomedusaorienta (Figure5(i)—(l))isdistinctlydifferentia-tedfromthosefoundinChengjiangandrecentbra-chiopods[22].Althoughthepairedbrachialarmsariseas wellfrom theanteromedianbody wall,theyarchandextendposteriorly,andthensur-roundtheanteriorandlateralbodywall(Figure5(i)and(j)).Thisarrangementandstylizedatti-tudeofthelophophoreisdistinctfromtheanteri-orly-convergingspirallophophoresinotherfossilandextantbrachiopods [37].Inaddition,the

pairedbackwardpointingbrachialarmsinH.ori-entabeartwopalisadesoftentaclesincludingarowofsmalltentaclesandanarrayoflargetentacles(Figure5(k)and(l))[22].Thesmalltentacles,varyingbetween0.3and0.8mminlength,ispre-served as short,delicate,linear impressions,whichareclosedspaced,radiatingoutwardsalongeachlophophoralarm.Bycontrast,thelargeten-tacleslookmuchthicker(about125ìmindiame-ter)andextendoutwardsupto6mminlength.Insummary,knownfromtheChengjiangfaunathereareatleasttwoconfigurationsoflophophoreintheearly Cambrian brachiopods,namely anteriorlyspiraledlophophoreandposteriorlyarchinglopho-phore.Ofthem,theposteriorlyarchinglopho-phoreisdistinctive,neverseeninotherfossilandextantbrachiopods.

Figure5　ThevariationsoftheorganizationofthelophophoreinCambrianbrachiopods.(a)—(d)FossilsandinterpretativedrawingsofLingulellachengjiangensis;(e)and (f)theexquisitelypreservedlophophorewithtentaclesofLingulellotretamalongensis;(g)and(h)graphicdrawingsof(e)and(f);(i)—(l)generalanddetailedviewsofthelophophoreofHe-liomedusaorienta.(i)dorsalviewofthelophophoreorganization;(j)areconstructionofthelophophoreorganizationinHe-liomedusa,notingthetwopalisadesoftentacles;(k)and(l)enlargedviewandreconstructionofthetentacledetailsofthelo-phophoreinHeliomedsa.

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　　3.2.4　BodycavityanddigestivetractThebodycavityaccommodatesthemainmus-

cles,digestivetract,excretoryorgans,andrepro-ductivestructures,andoccupiestheposteriorpartofthespaceinsideshellvalves[48].IntheCam-brianbrachiopods,thevisceralcavityappearstobesmallandrepresentedbyapronouncedred-stained-pear-shapedregion[27].Itisroughlyestimatedtotakeuplessthan30% oftheshellvolume.How-ever,itisreallyintriguingthatthebodycavityofLingulellotretamalongensishasanessentiallypro-longedextensionbeyondthehingelineintoaconi-caltubesubtendedbythepseudointerarea(Figure6(a)—(d))[28].Suchafunnel-likeextensionofbodycavityinbrachiopodsisneverseenandhardlyenvisagedintheirlivingrepresentative.Itisintheelongatedpouch-likecavitythattheU-shapeddis-positionofthedigestivecanalofLingulellotretamalongensishasbeenwellrevealedinmanyspeci-mens[23,28].Thealimentarycanalisrepresen-tedbyanarrow,partially mud-filledpronouncedtube(Figure6(a)—(d)).Itarisesfromamouthatthebaseofthelessintricatelyspirallopho-

phore,andmainlycomprisesamouth,esophagus,stomach,intestineandanus.AsseeninL.malon-gensis,Lingulellachengjiangensisbearsasimilarconfigurationofdigestivetractthatwasalsopre-servedas U-shapedeither mud-infilledtubesorreddish-brownimpressions[23].Inaddition,theU-shapedalimentarycanalisalsofoundinsomespecimensofLongtancunellachengjiangensisandXianshanellahaikouensis [43,52].Inthepastfiveyears,therecordsofU-shapedgutinCambri-anlingulatebrachiopodsareincreasinglyexpandinginthenumberofgeneraandgeologicalrange[17].Incontrast,thecalcareous-shelledbrachiopodKu-torginachengjiangensisfromtheChengjiangfaunaisdifferentintermsofitsbearingaposteriorlyex-tendingstraightgutwithanopenanusplacedpos-teriomedially(Figure6(e)—(g))[15].Thusthereexistedatleasttwoconfigurationsofdigestivetractsinearlybrachiopods,suggestingthattheor-ganophosphatic-shelledlineagehasbeendistinctlyseparatedfrom calcareous-shelledstocksandre-flectingthedisparityofbrachiopodsbytheonsetofCambrianexplosion.

Figure6　OpeningdigestivetractsofCambrianbrachiopods,disposedasU-shapedwithananteriorlyplacedanus((a)—(d))andastraightgutwithanusposteriorlypositioned((e)—(g)).(a)—(d)FossilsandrelativeinterpretativedrawingsofLin-gulellotretamalongensis;(e)—(g)fossil,reconstructionanddetailsofastraightalimentarycanalsexcellentlyexhibitedinKutorginachengjiangensis.

　　3.2.5　PedicleThepedicleisastalk-likeattachmentstruc-

turebymeansofwhichbrachiopodsareattachedto

sedimentsorontosomehardsubstratesurface.Inthelightofevidenceofextantrepresentatives,thepediclesofarticulatedandnon-articulatedarenot

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homologousorgans,differinginstructure,func-tionandembryonicorigin[37].Thepedicleofor-ganophosphaticbrachiopodsdevelopsasanout-growthoftheposteriorbodywallwithacoelomicextensioninthecentre.Incontrast,thepediclerudimentofarticulatedbrachiopodsiscontinuouswiththe mantlerudiment,whichproducesboththeventralanddorsalvalves,andthereforethecartilage-like connective pedicle in calcareous-shellediscontinuouswiththebodywallofbothvalves.However,itseemsdifficulttomakeclearhowthedifferencesinextantbrachiopodscanbeinterpretedphylogenetically[21].

Thepedicleisoneofmostcommonlypreservedsoftpartsofbrachiopodsinthefossilrecords [16,19];however,theknownrecordsofpediclesmainlycomefromtheCambrianChengjiangfauna[11,21,27,29,39,41,43,52].AccordingtoZhangetal.(2008),thepediclesofCambrianbrachiopodscanbedividedintotwogroupsbasedontheirsize,lengthandthenatureofthesubstratetowhichtheywereatta-ched.Thefirstgroupischaracterizedbyhavingthick,strongandmoderatelylongpedicles(Figure7(a)—(d)),withtheirdistalendsattachedtosomeotheranimals’exoskeleton [11].ThefirstgroupincludesmainlyLongtancunellachengjiangensis [24,52],Kutorginachengjiangensis [15,21]andAlsina.sp.[29]andtheproblematicbrachiopod Xianshanellahaikouensis(Figure7(a)—(d))[21,43].Thesecondgroupincludesthepediclesthatarethinandlong,u-suallybearingabulb-likeendburiedintosediment(Figure7(e)—(i)).Thistypeofpedicleusuallyoc-cursinthemajorityoftheknownlinguliformsinclu-dingDiandongiapista [11,21,41],LingulellotretamalongensisandLingulellachengjiangensis [39]andanew problematicform—sometimesreferredtoas“Wangyuiachengjiangensis”inref.[28]—butwhichhasnotyetbeenproperlydescribed.Recently,someexceptionalpreservationsofpedicleimpressionswerealsodescribedin materialofAcanthotretellaspinosaandLingulellawaptaensisfrom theBurgessShale[25,26].ThepediclesinthetwoBurgessShalelin-guliformsarethin,slimandslender,unquestionablybelongingtothesecondcategory.Intriguingly,thepediclesofthe Early CambrianlinguliformsfromsouthernChinaarecommonlystraight,andonlyinafewcasescangentlyfoldedcurvesbeobserved [21,27,41].Bycontrast,theBurgessShalepedicleofbothinAcanthotretellaspinosaandLingulellawap-taensisexhibitsamuchmoreflexiblenature,usuallytightlyfoldedasseriesofS-shapesandevenself-knots[25].Despitetheexistingdifferencesinpreservation,

thereareanumberofimportantsimilaritiesbetweenthedescribedpediclesofEarlyand MiddleCambrianlinguliforms.Allofthemshowindicationsofacentriccoelomiclumen and exterior circular annulations.ThesecharacteristicfeaturesarealsopresentinthepedicleofAcanthotretelladecaiusreportedfromtheslightlyyoungerGuanshanfauna[19].

Inspiteoftheoverallmorphologicalsimilari-tiesofthepediclesinthe2ndcategory,itisalsoreasonabletosubdividetheknownCambrianlingu-liformpediclesintothefollowing3differentfunc-tionaltypesonthebasisoftheirfunctionsfortheirrelativeshellvalves:(1)thetightlyfoldedandflexibletype,suchasthoseinAcanthotretellaspi-nosaandKuangshanotretamalungensis,possiblysuspendingtheirrelativeshellagainstspongeorlargealgae(Figure7(j)—(m));(2)holo-buriedpedicleswithheavyshell,bywhichthebrachiopodisevidentlyanchoredintosoftsubstrate,forexam-ple,Yuganothecaelegans (Figure7(g));(3)semi-buriedpedicleswithonlythedistalpartbur-iedintosedimentstosuspendtheirlightshella-bovethesediment-waterinterface,suchasthoseofLingulellotretamalongensis (Figure7(e))andLingulellachengjiangensis(Figure7(f))[11].

Asforfossillinguloidbrachiopods(SuperfamilyLinguloidea),aburrowinglifestylewastraditionallyassumed,analogoustotheir moderncounterparts.Linguloidswithpreservedpediclesandtracefossilsin-terpretedaslinguloidburrowsconfirmedthisassump-tion[53].However,withmorefindingsofexception-allypreservedCambrianbrachiopodswithpediclesdur-ingthelastyears,itbecameevidentthatawiderrangeofpediclemorphologiesandlifestylesexistedamongearlybrachiopodsthanpreviouslyassumed[11,44].Untilnow,thereisnounequivocalCambrianrecordofbrachiopodswithaburrowinglifestyleasseeninmod-ernlingulids,andalltheCambrianindividualswithei-therlongthread-likeorshortandrobustpedicleshaveanepibenthiclifestyle[27,59,60].Itisthereforetoassumethatvariablepediclesmaybegoodadaptationsfordifferentsessilelifestyle.AmongtheChengjiangbrachiopods,Xianshanella,Kutorgina,AlisinaandLongtancunellalived assecondarytierers (Figure7(a)—(d)),attachedbymeansoftheirmassivepedi-clesdirectlytovariousskeletalorganisms.ItisshouldbenotedthattheearlyCambrianacrotretoidKuangsh-anotretamalungensisdevelopedaslimthread-likepedi-clethatcould wrapandsuspendtheirminuteshellfromlargerorganismsatdifferentheightsabovetheseafloor(Figure7(j)—(m))[44].Thepedicleattach-mentmechanism maybemuchmoreefficientforthe

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micromorphicbrachiopodstopositiontheirshellstodifferenttierlevels whereprimarylinguloidtiererscouldnotreach.Itisthereforepossibletoproposethatacrotretoidscouldbemoresuccessfulinoccupyingepi-faunaltiersascomparedwithotherCambrianforms.Evidently,Diandongia,LingulellotretaandLingule-llafromtheChengjiangfaunarepresentprimarytiererswiththeirpedicleentirelyorpartiallyburiedinsedi-

mentsforanchorage(Figure7(h)—(i))[11].Itisworthwhiletobementionedthatnoevidenceofpedicleis so far discovered in Heliomedusa from theChengjiangfauna[18,22,45,47],which,likeDi-andongia,isoftenfoundtoserveasabasibiontatta-chedbyotherorganisms[11].ItisprobablethattheadultHeliomedusawasafree-lyingsuspension-feedingbenthos[11].

Figure7　ThedifferentmorphologyofthepedicleattachmentstructuresinCambrianbrachiopods.(a)—(d)Themassivepediclewiththeendattachedontohardsubstrateprovidedfromotherorganisms:(a)Kutorginachengjiangensis;(b)Xianshanellahaikouensis;(c)Longtancunellachengjiangensis;(d)Alisina.sp.(e)—(h)Theslimpediclesendedbyabulb-likestructureburiedintosoftsedi-ments:(e)Lingulellotretamalongensis;(f)Lingulellachengjiangensis;(g)unpublishedmaterialofYuganothecaelegans;(h)Di-andongiapistapreservedwiththinpedicle(lowerright)andattachedbyapedicleofLongtancunella(upperleft).(i)Detailedviewofthepedicleof(h)toshowthepediclelumeninDiandongiapista.(j)—(m)generalandcloseviewofpediculateattachedacrotretoidKuangshanotretamulungensis.

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　　Therefore,Cambrianbrachiopodshaveoccu-pieddistincttiersofspaceandtrophicnichesonthesoft-substratum [11].Theyexhibitedatleastfivetypesoflifestyles:pedicle-anchoring,pedicle-attaching,free-lying,cemented epifaunal,andsemi-infaunal.The pedicle attachment wasthemostcommonrelationshipofCambrianbrachio-podswiththesubstratewheretheyinhabiteddur-ingtheCambrianexplosioninterval[21].

4.Concludingremarksandoutlook

Thebrachiopodsrepresenttheoldestandbestknownexamplesofbenthicsuspension-feedersthates-tablishedvariabletieringstructureofcommunity(in-cludingprimary,secondaryandvariabletiers)duringtheCambrianexplosioninterval.ItisthustoclearthatthetieringcomplexityofCambriansuspension-feedingcommunitieshadbeeninitiatedandestablishedalreadybytheEarlyCambrian.Inmanycases,theprimarytieringbrachiopods,forexample,Diandongia andHeliomedusa,haveordinarilybeenfoundtoserveasbasibiontsforotherbenthicorganismtoattach[11].Therefore,theirshellvalves,functioningasapave-ment,playedanimportantroleinCambriansubstrateevolution,andacceleratedthedevelopmentoftieringecologicalstructureofothersuspensionfeeders.Inad-dition,thesoft-bodiedfossilsprovideuniqueinsightsintheevolutionaryacquisitionofmorphologicalnovel-tiesandthecharacterstatesofEarlyCambrianbrachio-pods.Evidently,theearlyCambrian(Stage3)brachi-opodshadacquiredafullydevelopedorganizationoftissuesandorgansystemalthoughpredationpressureonbrachiopodsstartedtoberapidlyincreasedbytheCanglangpuan(Series2,Stage4)[61].Theorganiza-tionoftissuesandorgansystemsincludingthesetae,mantlecanals,lophophore,digestivetractandpedicle,haddiversifiedandshowedaseriesofvariationsinmorphologicalstyle:

• Setaeincludetwomorphotypes,shortcili-um-likeandlongspine-likeforms,allofwhichareequidistantlydisposedalongtheshellmargin.

• Mantlecanalsaremorphologicallyvariable,includingthebaculate,pinnatepatternandanewperipheralcondition. The pinnate condition ismuchmorecommonlydevelopedinearlybrachio-podsthanpreviouslyexpected.

• Thelophophorecomprisesatleasttwotypesofdevelopmentalforms,anteriorlycoiledand

posteriorlyarchingorganization.• Thedigestivetractexhibitedtwotypes,U-

shapedandstraightformcomposedofa mouth,esophagus,stomachandanopeninganus.

• Thepediclescan beseparatedintotwomorpho-typesonthebasisoftheirsize,lengthandthenatureofthesubstratetowhichtheywereat-tached:① massivepedicleswiththeirendattachedtohardshellsofotherorganisms;② thinandelongatedpedicleswithbulb-likeend.Meanwhile,thesecondarytypecould befurthersubdividedinto,andcomprisesthetightlyfoldedandflexiblepediclespossiblywrappedaroundspongeorlargealgaeexemplifiedbytheacrotretoid Kuangsha-notretamalungensisandtheMiddleCambrianAc-anthotretellaspinosa.

Whilst no acknowledged brachiopods areknownfromtheMeishucunian (Cambrian,Terre-neuvian)ofsouthernChina[62],thereoccurrep-resentativesfrom8familiesofcrownbrachiopodsand two stem groups from the ChengjiangLagerstätten,displayingtheearliest-knowndiver-sificationofbrachiopodsandtheirhigh-disparityofmorphologyandanatomyduringtheintervalofCam-brianexplosiveradiationofmetazoans.Nevertheless,eachfamilyisexclusivelyrepresentedby monotaxicandmonospecificindividuals,signifyinglow-diversityofbrachiopodsduringthetimeinterval.Theoccur-renceofhigh-disparityandlowdiversityofbrachiopodsisinaccordancewiththeCambrianexplosiveradiationofhigh-ranksofothermetazoans[7].

TheexceptionallypreservedbrachiopodsfromtheChengjiangfaunahaveimportantconsequenceforunderstandingthemorphologicalnoveltiesandevolutionaryacquisitionofdiagnosticcharacteris-ticsofbrachiopodsduringtheCambrianexplosion.Inconjunctionwiththoseexhibitedinlivingrepre-sentatives,thediscoveryofsuchsoft-tissuechar-acters,suchaslophophoresandalimentarycanalsinCambrian,unquestionablycontributetodeter-minatetheevolutionarypolarityofthekeydiag-nosticcharacteristicsofthephylumBrachiopodaa-mongthesuperfamilyLophotrochozoa[2].AfullphylogeneticanalysisoftheCambrian-Ordovicianbrachiopodshasonlybeenpartlyinitiated[63]andwedonotyethaveacompleteunderstandingofbrachiopodphylogenyandtheirphylogeneticrela-tionshipstootherlophotrochozoans[64,65].

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Acknowledgements

ThisworkwassupportedbytheNationalNaturalScienceFoundationofChina (40702005,41072017,40830208),the973Project(2013CB835002)and111ProjectofChina(P201102007),andSwedishResearchCouncil(VR2009-4395,2012-1658toLEH).ZZFacknowledgesgrantsfromtheFokYingTungEduca-tionFoundation,theChinaScholarshipCouncil,andtheMinistryofEducationofChina(FANEDD200936,NCET-11-1046).WethankZhaiJP,ChengMR(inXi’an)fortechnicalassistance.

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ZhangZhifei

ZhangZhifeiisaProfessorofPalaeontologyattheDepartmentofGeologyinNorthwestUniversity,Xi’anofChina.HereceivedhisBachelor’sfromLifeSci-enceCollegeandMaster’sandPh.D.fromtheDepartmentofGeology,bothinNorthwestUniversity,Chinabeforehefinishedone-yearpostdoctoralvisitingstudyatfacultyofEarthScienceinUppsalaUniversity,Sweden.Heisinterest-edintheevolutionofCambrianBurgessShaletypesoft-bodiedfaunas.Hisre-searchisfocusedonexceptionallypreservedbrachiopodsandotherlophotrocho-zoanfossils.HewasawardedforNationalExcellentDoctoralDissertationofChinain2008andwaselectedasNewCenturyExcellentTalentsinUniversityofChinaanddistinguishedPalaeontologistsinthePalaeontologySocietyofChinain2011.HeiscurrentlyamemberoftheInternationalSubcommissiononCambrianStratigraphyWorkingGroupsforStage3,andvicesecretarygeneralofPalaeon-tologySocietyofChina.