SEEDLING MORPHOLOGY IN CLEMATIS (RANUNCULACEAE) AND ITS TAXONOMIC IMPLICATIONS

14 Pages·1991·5.4 MB·English

by  Frederick B Essig

SEEDLING MORPHOLOGY IN
CLEMATIS (RANUNCULACEAE) AND
ITS TAXONOMIC IMPLICATIONS
FREDERICKB. ESSIG
DepartmentofBiology
UniversityofSouthFlorida. Tampa, FL33620, U.S.A.
ARSTRACT
Seedsot58speciesoiClematisandClematopsiswereobtainedfromavarietyofsources,
germinated,andtheirseedlingandjuvenilemorphologyobserved.Twoverydistinctive
patterns emerged, each consisting of aclusterof characters. In Type I scedlmgs, the
eophyllsarealternateandtoothed.Hypocotylsareelongate(exceptinCleniatopiis),elevat-
ingthecotyledonsandapicalbudaboveground,andbudsarelackingintheaxilsofthe
cotyledons.SuchseedlingsaresimilartothosefoundinrelatedgenerasuchasAnerrione.and
are found inClematisin the infrageneric taxaClematis. iMsiantha. Connatae, Tuh/tlosae.
Atragene. Meclatis. Cheiropsis. Behaeaiilhera. Naraveliopsis. Papuasuae, and in thegenus
Ckmatopsis. InTypeIIseedlings,leavesarepairedfromthebeginning,butthefirst1—3
pairsareusuallyreducedtocataphylls.Leavesaregenerallyentire,oftenbecominglobedor
divided, but not toothed. Hypocotylsare short, keeping thecotyledon basesand the
epicotylatfirstsubterranean.Budsaretypicallypresentintheaxilsofthecotyledons.Such
seedlingsarefoundintheinfragenerictaxaCrispae,Viticella,Patentes,Rectae,AndAugustifo-
liae. Thesedifferencesinseedlingmorphologyandsomecorrelatedcharacterssuggesta
fundamentalsplitinthegenusandabasisforarevisedinfragenericclassification.
RHSUMl-.N
Semillasde58especiedeClematisyClematopsisfuerenobtenidodeorigenesdiversos,se
germino,ysusmorfoligiajuvenilseobservio.Dosmodelosdistintossemanifcstaron,catla
unoconsiteenungrupodevarioscaractercs.EnlasplantasdesemillcrosdelTipoUnolos
eofilossonalternosydentados.Loshipocotilossonalargados(conexclusiondeCkmatopsis),
yelcvanloscotiledonesylayemacimerasobrelaticrra.Yemassonausentedelasaxilasdo
loscotiledones. Plantasdeseimllerosdeeste tiposonsemejanteaaquellashalladoen
generos relatados como Anemone. Se encuentran en las taxa infragenericas Clematis.
Lasiantha. Connatae. Ti/bulosae. Atragene, Meclatis. Cheiropsis. Bebaeantehra, Naraveliopsis.
Papi/asicae,deClematisyenelgcneroClematopsis.LnplantasdesemillerosdelTipoII,todas
hojassonopuestas,perlaspareaI—3sonusualmentereduciendoacatafilos.Lashojasson
usualmenfeenteras,frecuentementelobadosperonodentados.Hipocotilossoncorto,ylas
basesdeloscotiledonesylayemacimerasec]uedansubtcrraneo.Yemasseencuentranenlas
axilasdeloscotiledones.Plantasdesemillerosdeestetiposehallanenlastaxainfragerericas
Crispae. Viticella. Patentes. Rectae. yAngi/stifoliae. Estasdiffcrencias morfologicasdelas
plantasdesemillerosyalgunescaracterescorrelativessugeronunadivisionfundamentalin
elgeneroyunfundamentopararevisarlaclasificacioninfragcncrica.
SiDA 14(3):377-39(). 1991.
378
INTRODUCTION
ThegenusClematisisalargeanddiversegenusofthepresumedlyarchaic
family Ranunculaceae. Found on every continentexcept Antarctica, the
approximately300speciesofClematisoccurinnearlyeveryclimaticzone
fromthetaigatotheequatorialtropics,anddisplayawidevarietyofboth
vegetativeandfloralforms. Therehasbeen nocomprehensiverevisionof
thegenussincethatofKuntze(1885),buttherehavebeenrecenteffortsto
developamoderninfragenericclassification. Authorshavesubdividedthe
genus invariousways(see Keener& Dennis, 1982, forareview), some
dividingitintosubgenera,othersdividingitintosections.Tamura(1967)
divided Clematisinto 12sections(Table 1)inthemostcomprehensiveof
recent classifications. His great familiarity with Asiatic Ranunculaceae
allowedhimtodefinefairlypreciselyvariousinfragenerictaxaoccurringin
thatregion, butspeciesfromotherregions, particularlyAfricaandNew
Zealand, arc sometimesdifficult toplace in his system. Tamuradid not
attempt togroup hissections intosubgenera, perhaps feeling thatthere
was insufficient basisforrecognizingmajordivisions within thegenus.
Keenerand Dennis(1982), on theotherhand, dividedthenativeand
naturalized North American species into four subgenera, drawing upon
earliersubgenericconcepts. Theydid notattempttoincorporatetheold
world taxa into their system, or to further divide their subgenera into
sections, etc., stating that a new world-wide monographic treatment
wouldbe needed inordertoaccomplishthis. Thus, thereconciliationof
Tamura'ssectionalclassificationwiththesubgenericsystemofKeenerand
Dennisremainstobedone.
Tamura'ssystememphasizesfloralandinflorescencecharacters,ascanbe
seeninTable 1.Thebestandmostnaturalclassificationsystemsgenerally
result, however, whenafull rangeofcharacters from flower, fruit, seed,
seedling, and vegetative shoots are employed. Study of additional
characters,particularlyvegetativecharacters,andperhapsalsocytological
ahdchemicalcharacters, isthereforeneededinthisgenus.Acomprehens-
ivenewclassificationshouldreflectmajorlinesofevolutionatthesubgene-
riclevel,andlinkthesections, subsections,etc. inahierarchicalfashion.
Inbuildingupacollectionottropicalancisubtropicalspecieso(Clematis
attheUniversityofSouthFloridaBotanicalGarden,strikingdifferencesin
seedling morphology and related vegetative features were noticed,
suggestingthatasurveyofthegenuswouldbeworthwhile.Littlehasbeen
recordedconcerningseedlingmorphologyinClematis,despitethefactthat
numerous species have been cultivated over the past two centuries.
Lubbock(1892)describedandillustratedtheseedlingsofthreespecies(C
rectaL., C. orientalisL. (asC. graveolensLindl.), and C. (Atragene)alpina
379
Tahm;I.C^lassificarionoftheClematisailiiinceaccordingtoTaimira1956,1967),withdistinguishing
charactersasreportedbyTamiira;asteriskindicatestaxaknowntohaveTypeIIseedlings.
GenusC^i.EMAILS[leavesopposite,sepalsvalvatej
SectionViiirtki[sepalserect,oftencolored,stamenhlamentshairy]
SubsectionCi»i)httiii:[woodyvines,leavesroothed]
Subsection li/bidosae[erectsemi-slitiibs,leavestoothed]
*SubsectionCnspae[perennialherbsorweak-stemmedvines,leavesentire]
SectionBehaeantheni[asinViorna,butHewersfasciculatewithnewgrowth]
SectionAlrat^ene[flowerswithstamen-iierned"petals,' leavestoothed]
SectioniWixliilis[sepalsspreadingtoerect,mostlyyellowtoorange,stamenhlamentshairy]
SubsectionOrientales[flowersfewtomanyinaxillaryorterminalclusters]
Subsection'l'c/>Jg//ticae[singleflowersterminatingnewshoots)
SectionClt'iiuitis[sepalsspreading,whitish,stamenlilamentsglabrous,leavesmostlyroothed]
SubsectionP/entuinae[flowers3^3.5cmdiam.,stamen(rlamentsdilateddownwattl]
SubsectionVita/hue[flowers•3cmdiam.,stamenfilamentsfiliform]
SubsectionDkjiccic[asaliove,butflowersmostlydioecious]
SubsectionAnUatin:[asabove,butstamenconnectiveprojected]
SubsectionPcipnastcat:[similartoabo\e.differenceinstructureofpanicle]
SubsectionCnissifiiiide[stamenfilamentsrugulose,leavesconacious,entire]
*SubsectionRectcH'[antlierselongate;le<ivesentire]
*SubsectionAngusnldUae[asabovebutfiowetslarge,with6se[-)als]
SectionCheifupiii[flowersfasciculatewithnewgrowth,large,bisexual,sepalsspreading]
SectionLiDuintha[asabovebtitflowersdioecious]
SectionVilnella[flowerslarge,sepalsspreading,colored,stamensglabfous,leavesentire]
SubsectionUlonclin-[flowerssolitary,axillary,subtendedby(wobracteoles,stylesplumose]
•SubsectionVuuella[asabove,butstylesshort,not[dumosej
*SectionPa/eriles[asabovebutflowersfrombudproducedinfall]
SectionPtmiiinpii[achenesstronglycompressedandwinged,leavesentire]
SectionFrulia-lLi[woodyshrul")swithverysmallleaves]
SectionNanircl/ops/s[antherconnecti\-esmuchprolonged,similartoFapz/asiuie]
C'renusArchiclcmati.s[leavesalternatethroughout,otherwisesimilartoCo/iruj/^/e]
(ienus(Mcmatopsis[flowerslarge,sepalsimbricate,otherwisesimilarto(.o/iruiUic]
GenusNaraveiia[flowerswithelongate,petal-likestaminodes]
(L.) Miller). The seedling morphologyofC mta described by Lubbock
agreeswiththe"Type11" morphologydescribed inthispaper, whilethat
forC.grai'eolemandC.alpimiagreewiththe"TypeI"morphologydescri-
bed here. Erickson (19-15) illustrated C.fremoiitii S. Watson var nehlii
Erickson, and itagrees with "Type 11."
Thisstudywasundertaken theninanticipationthat unrecognizedand
overlooked vegetative features, such as those of the seedling, might
provide clues to the major lines of evolution in the genus that are
ambiguous whenonly floral featuresare used.
MATKRIAI.S AND MFTHC^O.S
Effortsweremadetoobtainseedofspeciesrepresentingall recognized
infragenerictaxainClematisandofseveralcloselyrelatedgenera,following
380
the classihcation ofTamura (1967, see Table 1). According to Tamura,
three genera, Archiclcinatis. Cleniatopsis, and Nanivelni, are distinct from
Cle/i/iitis, but closely related. Each has been included in it by various
previous authors. Therefore, they have been considered in this study,
although 1 thus far have only obtained seed ofCletnatopsis. Altogether,
Tamura's smallest units (subsections and undivided sections), plus the
three relatedgenera, make 26 initial units forsystematicstudy.
Seedlingsof58species,representing20ofthese26units(Table2)were
observed. Seedswereobtainedfromavarietyofsources, includingbotani-
cal givrdens, commercial seed companies, andprivatecollectors. Seedsof
nativeFloridaspeciesandsomeotherswerecollectedbytheauthor. Seed
fromcultivatedsourcesfrequentlyprovetobemisidentihedorofdubious
ormixedancestry. Therefore, greatcarehasbeentakentoassurethatthe
material reported u]X)n has been accurately identified. Identity of all
specimens is being verifiedas theplants becomemature, and specimens
whose identityorinfragcneric placement isstill uncertainarenot inclu-
ded.
Seeds weregerminated inagreenhouseat the USF Botanical Garden,
some only after stratification and/or a long period ofdormancy. Many
plantswerelatertransferred toan outdoorexperimental plot. Allaccess-
ions werephotographed afterthe firstleafappeared andoftenatlaterst-
ages. Seedlingsofmanyspecieswerepreservedandexaminedunderadis-
sectingmicroscope. Voucherspecimensandphotographsarebeingmadeas
each specimen blooms forthe first time.
Tamli 2.Spc'iicscxaminc-i.1(;illculnvarcdaiIJSFHDtannal(iar(.l(.-ii).
'l'ilX(Jll Type US!-Au.#
C.addisoniiliritio[i (Irispac 87-40
(,.alpinaMiliar Arra^t-tu- 87-41
(!.apiilolia1)(^. Viralhac 82-22
(...ansraraR.Br. Aristat.ic- 87-^7
(..haklwiniiTorri-y&A.Ciray (Tispac 86-25
(;.harlxllaraIxitjcw. Hcbacnirhcra 87-139
(;.brachiataKcr,-C'nnvl Vnalliac 87-2
(...buclianianaV>(.. ("onnatac 87-10-t
i..canipaiuilillor.iBrot. Viticclhi 87-33
C^.catcsbyanaFursh Dioicac 85-y,86-35
C;.chincnsLsOsbcck Recrae 88-2
i..chrysDCoina['raiicliL-r ('heiropsis 87-48
381
Tahu:2((AHUinutd)
cirrliosaL. (^heiropsis 1 87-3
cnspa1.. (^rispae U 83-2
Lknncuhit.iVeil. Dioicae I 87-79
drummondiiTorrcy&A.Gray Dioicac I 87-.M
filameiirosaDunn Naraveliopsis I 87-38
flammula1.. Rettae II 87-121
tusc.i'lurcz. Oispae II 87-122
gcnnanoidcsDC;. Aristatae 1 86-28
glaucophyllaSmall Crispae II 87-1^6
grataWallich Vifalbae I 87-105
hcrackitoliaDC. Tuhulosae T 87-3^
hc'xapctalaPall. Angustifoliae 11 87-71
hir.suti.ssimaPursh (!nspae 11 86-30
nitc.gntoliaL. Crispae 11 83-^
inrruaraIkinge Mcclans 1 87-70
kirilowiiMaxim. Rectae II 87-76
lasianrliaNurt. kasiantha 1 87-7
leschenaiilnanaDC7 C!i)nnatae I 87-66
li^yusncifoliaNutt. Dioieae I 87-k86-32
macropc'talaLedcb. Alragene I 86-V^
mandshnncaRupr Rectae II 87-124
micropihyllaDC. J > 87-4^,87-33
napaiilen.sisDC. Behaeantliera I 87-106
oncnralisL. Meclatis I 86-33
orientalIS Meclatis I 87-107
"latlakhiana"
papua.sicaMerr&Perry Papuasicae I 89-1
patensMorr.&Decne Patentes n 87-140
peteraeHand.-Mazz. Vitalbae 1 87-50
pierotnMujuel Pierotianac I 86-37
pitclieriSargent (irispac II 88-33
rantinttiloidesFranehet (a)nn.itae 1 87-49
rectak. Rectae II 86-^9
relidenaiiaCraib Meclatis 1 88-24
retKiilataWalter Crispae II 83-7
serrantoliaRehder Metlatis I 87-123
ttearnmgtulroircaaDK(or^sh MReeccltaateis u[ 8837--673
(asC.paiueulata)
ctteexreniiinsiosraHiDiCtk.lcy CRnesc|tiaaee IIII 8875--^88,87-78
c viornak. (Crispae II 88-^2,87-39
c.vitaihak. Vitalbae 1 86-la,86-42
c.vititellak. Viticella 11 88-39
Cl.F.MAroi'sis
C.villosaDC. 86-43
CkscabiosiloliaViguier&Perrier
vat.kirkii Oliver 86-47
C,anetliitoliaHook. 88-42
^82
iYnFpKu"j\.. 1i.Seleydplein1gsctcycplleisi.iL;A.1)1I('.y'p.i-l-aHiIilsLc\c<iliiihm-ts;hsioiftuCih'Piiiiuirtsihs.hiI)r.aiTkiyjpoeluiIIIsXe^e.dlBi.n,^TyopleCkI-Irsieueiitlnliitii^i'iiiojiltCirliicwDaCl.n
RISULTS
Thespecimensstudiedhillintotwomajorcategorieswithrespecttofour
distinctsetsolcharactersinvolvingnotonlyseedlingmorphology,butalso
aspectsoftheadult foliageandtheachenes. Thefeaturesassociatedwith
each typeofseedling aresummarized inTable .^, anddiscussed mdetail
below. AsummaryofTamura'staxafallmgintothetwocategories,along
with the taxa that have notyet been studied is presented inTable4.
1. Seedlingphyllotaxy
In Type 1 seedlings (Figure 1A,(~), the first several eophylls (seedling
leaves)arealternate,andcloselyspaced,formingasmallrosetteattheapex
ofthehypocotyl. Thisalternatephyllotaxylatergiveswaytotheopposite
383
phyllotaxytypicaloftheadultplants, usuallyatthetimethatinternodal
elongationbegins. Thismayhappenasearlyasthethirdandfourthleaves
insometaxa,butinConnataeandClematopsis,leavesmayremainalternate
throughoutthefirstjuvenileshoot.ThegenusArchklematishasbeensegre-
gatedfromClematisonthebasisofitspermanentlyalternatephyllotaxy.In
sectionMeclatis, thefirsteophyllistypicallyfollowedquicklybyasecond
eophyllwithoutinternodalelongation, givingtheappearanceofopposite
orsuboppositeleaves. InternodalelongationinMedatisbeginsafter2or3
eophylls, while the leavesarestill alternate.
TypeIIseedlings(Figure 1B,D, 2L)contraststronglyinthatleavesare
opposite from the beginning, and several sets ofpaired cataphylls are
producedbeforeanyleaflikeeophyllsareproduced. Internodalelongation
ispresentfromthebeginningalso,evenduringthecatophyllstage,except
that the first pairofcatophyllsmay beproduced immediatelyabove the
cotyledons(e.g. in ClematiscrispaL.).
Taiiii;3-Charactersdistiiit;uishint;TypeIfromType\\CJcmcitis.
ChiiviKter TypeI TypeII
Pliyllotaxyolseedling opposite
Hypoeotyl mostlyelongate suppressed
(exceptinClenuilopsis)
Initialshoot condensedrosette elongate
C'ataphylls absent severalpairspresent
Eophyllmargin toothecl entire
Atliilrfoliage mostoftentoothedand oftenlobedordissectedbut
membranous,orentireami nottoothed,mostly
giossy-coriaceoiis membranous
Regenerativebuds inaerialleafaxilsor(in insubterraneanaxilsof
Clematopsis)insubterranean cotyledonsandsome
axilsofrosetteeophylls cataphylls
CJrowthtorm wootiyvinesorshrubs;many perennialerettherbs,weak-
rootingataerialnodes stemmedvinesorsometimes
woodyvines;theseregenerating
fromsubterraneanbuds
Achenes laterallycompressed,but broad,very(lat
narrow,turgid
384
2. Eophyll and leafmorphology.
InTypeIseedlings, leafshapevariesconsiderably(Figure2C—K), but
eophyllsaretypicallybroad,sometimes3-lobed,withsmallveinsciiverg-
ing from the peripheral region and terminating in marginal teeth. This
patternusuallypersistsintheadultfoliage,andmostofthetaxawithType
I seedlings have conspicuously dentate foliage throughout the plant. In
SectionMeclatisthe firsteophyl—lsarenarrowandlittle-toothed(typically
entiretoirregularly 1-toothed Figure21,J), butsubsequentleavesare
dentate. Section Atragene, considered adistinctgenus by some authors,
dihers from the common form only in that the first eophylls are deeply
divided (Figure 2C).
InTypeIIseedlings,Thefirsteophylls(afterthecataphylls)aremostly
elliptic-ovate and entire, although in C. terniflora the firsr eophylls are
sometimes3-lobedatthetip(Figure ID). Adultfoliagemaybevariously
divided and lobed bur never toothed as in Type I species.
3. Cotyledon, hypocotylorientation, and habit.
InthetermmologyofDukeandPolhill(1981)mostTypeIseedlingsarc
phanerocpigeal,i.e. thecotyledonsandepicotylareelevatedaboveground
byanelongatehypocotyl.Asadults.TypeIplantsaremostlywoodyvines,
orinsubsectionTi/h/dosae, suffrutescentshrubs. Branchingcanoccuronly
from aerial nodes above the hypocotyl. Many species, however, readily
form adventitious roots when aerial shoots touch the ground, and can
spread quiterampantly in thisway.
In the three specieso(Cleniatopsisexamined, whichotherwisehaveall
the characteristics of Type I species, the cotyledons emerge from the
ground, butthehypocotyldoesnotelongateandthecotyledonbases,and
initially the epicotyl, remain below ground (phanerohypogeal). Several
eophylls are produced without internodal elongation, forming a small
rosette,andthesesubterraneannodesformarootcrownwithbudsthatcan
repeatedly regeneratetheplant ifthetopdiesoffduetodrought, fireor
normal seasonal cycles.
TypeIIseedlingsareallhypogeal, asthehypocotyldoesnotelongate,
althoughthebladesofthecotyledonsmayemerge(phanerohypogeal). In
this one respect they are similar ro the species ofClematopsis mentioned
above. However, inTypeIIplants,anelongateshootisproduceddirectly,
withoutformationofarosette. Regenerativebudsareproducedintheaxils
of thecotyledons and someofthe lowestcataphylls.
ThepredominantgrowthforminTypeIIClematis,atleastinsubsections
CrispacandAngNStifoliae,andinClematisrecta, isaperennialherborweak-
stemmed vine, in which stemsdie backto theground each winter. The
385
underground rootcrown established by the seedHngsallows for repeated
renewaloftheplantinsuccessivegrowingseasons.OthertaxawithTypeII
seedlings, suchasClematisternifhraandseveralofitsEurasianrelativesin
sectionRectat,alongwiththesectionsViticellaandPatenteshavepersistent
FIG.2.Variationinfirstseedlingleaf,includingoutgroupcomparisonswithAnmiom(A,B);A-K
representTypeIseedlings,LisTypeII.A.AnemonepiihatillaL.{PulsatillavulgarnMiller).B.Anemo?ie
herUnidienPritzel.(!.C.lemalis(Almi^eni)alpiruiMiller.D.ClematischrysncomaFranchet.F.Ciematnpsis
villiisaDCl.FClenhitisptipiiasicaMerrill&Perry.G.Clematis^entiannidesDC.H.Clematisjilamentosa
Dunn, I.ClematisuricnlalisL,J.ClematislangiitkaKorsh.K.ClematismicrophyllaDG.(oneoftwo
()|Tpositeleaves).L.ClematisfuscaTurcz.(firstancfsecondpairofleavesarenumbered;"b"indicates
positionofbudsinaxilsofcotyledons).
386
Iaiii.I'4.Summaryol'liiimira's(1967)inlra^fiiLTRrax.itlisplayingTypeIantiType-IIiiiDrpliolo^ies
'/)/'('/ '/)'/«'// Viiclilermim-J
Vitalhac Oispae Crassifoliac(prol-). I)
PaTDtinae Rcctac(Eurasiant;ri)up) Rccrac(tropicalAsian)(prob. I)
Dioicae Viticella l-ruticclla(.0
BebacantluTa Patentcs Pterocarpa(pruh, II)
l.asiaiuha An^i^ustifoliac Floridac(prdh. II)
(Jiciropsis Naravelia(pri)h.1)
Arisratae Archicicmatis(prob.I)
Naravciiopsis
Papuasica
Clonnarac
IlibLiiosae
Nk-clacis
Atrai^cne
(.Icmaropsis
woody stems, bur even in well-established plants, new shoots can arise
from thesubterraneanbuds at the baseoftheoriginal shoot.
There is a strong trend toward cryptohypogeal germination in this
group, inwhichthecotyledonsremainwithintheseedcoatbelowground.
ThespecimensstudiedofClenuitisviorna, reticulata,jiisca. texensis.pitcheri.
glancophylla. andpateuswerecryptohypogeal, whileC. mtegrijolia. cnspa.
halclwniii. ternijlora. hexapetalaandkiriloiviiwerephanerohypogeal.
4. Achene shape.
AchenesinType1taxa,althoughlaterallycompressed,tendtobesmall
andturgid, whilethoseinType11taxatendtobeverybroadandflat,and
often havea conspicuously thickened rim.
Ofall the specimens examined, just one appears to be intermediate
betweenTypeIandTypeIIseedlings.SpecimensoiClen/cilisi/mwphyllaDC
from Australia have seedlings with an elongate hypocotyl, with the
eophyllsstrongly ^-lobedandtoothed.Eophyllsarcpairedfromthebegin-
ning, however, and therearebuds in theaxilsofthecotyledons, thein-
ternodcsareelongateafterthefirstpairofleaves,andtheachenesarebroad
and flat. Whether this species is phylogenetically intermediate between
the two types or represents convergence or reversal in some characters
remains tobeelucidated through furtherstudy.