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Reevaluating the Taxonomic Status of Ceriops Australis (Rhizophoraceae) Based on Morphological and Molecular Evidence

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Reevaluating the Taxonomic Status of Ceriops Australis (Rhizophoraceae) Based on Morphological and Molecular Evidence Botanical Studies (2009) 50: 89-100. taXONOMY Reevaluating the taxonomic status of Ceriops australis (Rhizophoraceae) based on morphological and molecular evidence Chiou-RongSHEUE1,*,Yuen-PoYANG2,Ho-YiLIU2,Fu-ShanCHOU3,Hsiu-ChinCHANG1,Peter SAENGER4,ChristopherP.MANGION5,GlennWIGHTMAN5,JeanW.H.YONG6,andChi-Chu TSAI7,** 1Department of Biological Resources, National Chiayi University, 300 Syuefu Rd., Chiayi 600, Taiwan 2Department of Biological Sciences, National Sun Yat-sen University, 70 Lien-hai Rd., Kaohsiung 804, Taiwan 3 Liouguei Research Center, Taiwan Forestry Research Institute, 198 Chunghsing Village, Liouguei 844, Kaoshiung County, Taiwan 4School of Environmental Science and Management, Southern Cross University, Lismore NSW 2480, Australia 5Department of Natural Resources, Environment and the Arts, PO Box 496, Palmerston NT 0831, Australia 6 Natural Sciences, National Institute of Education, 1 Nanyang Walk, Nanyang Technological University, 637616 Singapore 7Kaohsiung District Agricultural Improvement Station, 2-6 Dehe Rd., Changihih Township, Pingtung County 908, Taiwan (ReceivedDecember24,2007;AcceptedAugust19,2008) ABSTRACT. Ceriops australis(White)Ballment,Smith&Stoddart,amemberofthemangrovefamily Rhizophoraceae,wasoriginallyrecognizedasC. tagal var.australisWhitebutwasraisedtospeciesrank basedsolelyonisozymefeaturesandtheonlydistinctivemorphologicalfeatureofthehypocotyl.Therefore, itwasconsideredasiblingspeciesofC. tagal (Perr.)C.B.Rob.Thegoalofthisstudywastotestthe previousassessmentthat C. australisandC. tagal differconsistentlyonlyinhypocotylmorphology,inorder toreevaluatethetaxonomicstatusandtoestablishitsgeographicrange.Principalcomponentsanalysiswas employedtoanalyze29morphologicalcharactersofherbariumspecimensfromAustralia,Madagascar,and SumatratentativelyidentifiedasC. australisandC. tagal, andtwowelldifferentiateddistincttaxawere recognized.Inaddition,bothofthedetailedmorphologicalfeaturesbasedonfreshandherbariummaterials andtheintronsequencesoftrnLgenefromplastidDNAsupportthisconclusion.Thisfindingdisagrees withpreviousassessmentandsupportsthecurrenttaxonomicstatusofC. australis.Here,akeytothesetwo speciesisprovided,andareviseddistributionrangeofC. australisisestablished.ThisistheinitialreportofC. australis’occurrenceinapartofIndonesia,inadditiontoareasofAustraliaandPapuaNewGuinea. Keywords:Australia;Ceriops tagal;Ceriops;Distribution;Indonesia;Mangroves;PapuaNewGuinea;Plastid DNA;Principalcomponentsanalysis. INTRODUCTION Thelastrevisionofthegenus Ceriopswasdoneby Hou(1958),withtwospeciesrecognized:C. tagal(Perr.) CeriopsArn.isoneofthemangrovegenerainthe C.B.Rob.andC. decandra (Griff.)DingHou.Some20 familyRhizophoraceae,withawidespreadgeographical additionalnames,includingseveralinfraspecificnames rangefromeasternAfricathroughouttropicalAsia,and weresynonymizedforthem,butavarietynameC. tagal northernAustraliatoMelanesia,andthroughMicronesia (Perr.)C.B.Rob.var.australisC.T.Whitenamedby northtosouthernChina(Tomlinson,1986).Ittypically White(1926)wasnotlisted. growsintheinnermangroves,oftenformingpurestands White(1926)noticedaformofC. tagalinwhichthe onbetterdrainedsitesorbecomingstuntedinexposedand propaguleshadsmooth,teretehypocotylsratherthan highlysalinesites,withinthereachofoccasionaltides theangledorribbedhypocotylstypicalofC.tagalfrom (Hou,1958). AustraliaandPapuaNewGuinea.Heinitiallyintendedto describethisformasanewspeciesdistinctfromC.tagal, *Correspondingauthor:E-mail:[email protected]; basedonthe“lessdistinctlyveined,andmoreinclined Tel:+886-05-2717827;Fax:+886-05-2760164. torecurved”leaves(White,1926).Afterexamining **Co-Corresponding author.E-mail:tsaicc9017@yahoo. additionalspecimens,however,hefoundthosedifferences com.tw;Tel:+886-08-7746735;Fax:+886-08-7229466. betweenthenewformandC.tagalwerenotconstant 90 Botanical Studies, Vol. 50, 2009 except for the hypocotyl morphology.Thus,White analyze29morphologicalcharacters(25quantitativeand describedtheformasavariety,C.tagal var.australis. 4binarycharacters,Table1),andthePC-ORDpackage Basedontheanalysisofstarchgelelectrophoresisof (McCune and Mefford, 1999) was used to analyze isozymesfromC.tagalvar.tagal,C.tagalvar.australis charactervariablematrices.Thepossibledifferentiated andC.decandrainnorthernAustralia,Ballmentetal. characters identified in this analysis will be used to detect (1988)foundauniformgeneticstructurewithineach diagnosticfeaturesinthefollowinganalysis. taxonandahighlevelofgeneticdivergenceamongtaxa. For each taxon having a distinct isozyme profile and the Fresh plant materials for morphological evidenceofreproductiveisolation,theauthorsproposed characterization threedistinctivespeciesandhenceraisedWhite’svariety FreshplantmaterialsofC. australisandC. tagal tospecificrankasC. australis,despitethefactthatthe weresampledfromCapeYork,Cairns,andCardwellof extentofdivergenceinmorphologicalcharactersother northeasternQueenslandandfromtheDarwinareaof thanpropagulemorphologyremainedunclear (Ballment et theNorthernTerritoryofAustraliaduring2005to2007 al.,1988).Ceriops australiswasthenclaimedasasibling formorphologicalcharactersinvestigationandmolecular speciesofC. tagal (Ballmentetal.,1988). study. Three branches from each of five individuals in a Duetotheconfusionregardingdiagnosticcharacters, populationwerecollected.Charactersoffreshmaterials itisstillunknownhowfarnorthofAustraliaC. australis wereinvestigatedbyaLeicaMZ75stereoscopeand extends(Duke,2006).Misidentificationofthesetwo photographedwithanOlympusC7070digitalcamera. morphologically similartaxahasbeenquitecommonin VoucherspecimensweredepositedattheHerbariumof herbaria(Sheue,personalobservation).Makingafield theDepartmentofBiologicalResources,NationalChiayi identification of C. australis is very difficult at any time University(CHIA). otherthanthefruitingstagewithahypocotyl.Thus, adetailedstudyofthesetwomorphologicallysimilar Herbarium specimens for determining speciesisvital. distribution range Thegoalsofthisstudy,therefore,aretodetectthe Theloanedspecimens(Appendix)fromherbariaBM, differencesbetween C. australisandC. tagal,basedon DNA, GH, K, L and MO were identified as C. australis abroadanddetailedmorphological assessmentaidedby orC. tagalthroughthefollowingtwosteps.Inthefirst moleculardata,andtoestablishthegeographicdistribution step,specimenswithviviparousseedlingsattachedonthe rangeofC. australis.Hereweapplyprincipalcomponents shootsweredeterminedandusedforgettingdiagnostic analysistomorphometricdataobtainedfromherbarium features for identification. In the second step, specimens specimensandinvestigatetheDNAfeaturesofthetrnL lackinghypocotylswereidentifiedaccordingtothe intronofcpDNA.Wealsousedetailedcharactersfrom diagnostic features obtained from the previous first step. freshandherbariummaterialstoreevaluatethetaxonomic Eachspecimenwascarefullyexaminedatleastthrice.In statusofthesespecies.Theresultswillbeusefulfor addition,afewspecimensofC. australisexaminedfrom fieldworkidentificationandherbariumexamination, HerbariaBOandCALwereincorporatedintheresults. conservation,andforclarificationoftherelationship betweenthesespecies. Molecular evidence Materials. PopulationsofC. australisandC. tagal MATERIALS AND METHODS were mainly sampled at five sites on the northeast QueenslandcoastandnorthNorthernTerritorycoast Herbarium specimens and morphometric inAustraliaduringtheperiodfrom2003to2007.In analysis addition,C. tagal collectedfromSingaporeandIndia Asithasbeenreportedthatonlyviviparousseedlings andC. decandra collectedfromIndiawereanalyzed couldbeusedtodifferentiate Ceriops australisfrom together (Table 2). Three to five leaves were taken from C. tagal,theformerhavingterete(smooth)hypocotyls eachindividualandstoredwithsilicagelinzip-lock andthelatterhavingridgedhypocotyls(White,1926; plasticbagsuntilDNAisolation.Voucherspecimenswere Ballmentetal.,1988),specimensofbrancheswithboth depositedattheHerbariumofNationalChiayiUniversity vegetativeandreproductivefeatures,includingviviparous (CHIA). seedlings,wereexaminedforthismorphometricstudy. DNA extraction. Usingthecetyltrimethylammonium FifteenspecimensfromtheNorthernTerritory(OTUs bromide(CTAB)methoddescribedpreviously(Doyle 1-8)andQueensland(OTUs9-15)ofAustralia,tentatively andDoyle,1987),totalDNAwasextractedfromfresh identifiedasC. australis,and15herbariumspecimens etiolatedleaves.Ethanol-precipitatedDNAwasdissolved tentatively identified as C. tagalrepresentingpopulations inTE(Tris-EDTA)bufferandstoredat-20ºC.Qiagen ofNorthernTerritoryfromAustralia(OTUs16-22), (Valencia,CA,USA)columnswereusedtocleanthe Madagascar(OTUs23-26),andSumatra(OTUs27-30) DNAsamples,whichweredifficulttoamplifybyPCR. were used in the morphometric study (Appendix). TheapproximateDNAyieldswerethendeterminedusing Principalcomponentsanalysis(PCA)wasconductedto aspectrophotometer(modelU-2001,Hitachi). SHEUE et al. — Reevaluating the taxonomic status of Ceriops australis 91 PCR amplification and electrophoresis. Theprotocols the first two principal coordinates. Only the first ordination forPCRwereasfollows.A50-µlmixturecontained40 axiswasconsidered(Table1).Forcomponents,theten mMTricine-KOH(pH8.7),15mMKOAc,3.5mMMg highesteigenvectorvaluesbelongedtoreproductive (OAc)2,3.75µg/mlBSA,0.005%Tween20,0.005% characters,exceptleaflength;accordingly,theseinclude Nonidet-P40,fourdNTPs(0.2mMeach),primers(0.5 surfaceofhypocotyl(HS),lengthoffruit(FL),lengthof µMeach),2.5unitsofAdvantage2DNApolymerase hypocotyl(HL),lengthofcalyxlobe/widthofcalyxlobe (Clontech),10nggenomicDNA,plusa50-µlofmineral (CLL/CLW),widthofcalyxlobe(CLW),thicknessof oil. Amplification
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