a minute mid-cretaceous flower from siberia and...

Click here to load reader

Post on 06-Mar-2018

225 views

Category:

Documents

4 download

Embed Size (px)

TRANSCRIPT

  • 5GEODIVERSITAS 2004 26 (1) Publications Scientifiques du Musum national dHistoire naturelle, Paris. www.geodiversitas.com

    A minute mid-Cretaceous flower from Siberia and implications for the problem of basal angiosperms

    Valentin A. KRASSILOVInstitute of Evolution, University of Haifa,

    Mount Carmel, Haifa, 31905 (Israel)and Palaeontological Institute, 123 Profsojusnaya,

    Moscow 117647 (Russia)[email protected]

    [email protected]

    Lena B. GOLOVNEVABotanical Institute, 2 Popova, St. Petersburg (Russia)

    [email protected]

    Krassilov V. A. & Golovneva L. B. 2004. A minute mid-Cretaceous flower from Siberiaand implications for the problem of basal angiosperms. Geodiversitas 26 (1) : 5-15.

    ABSTRACTA new taxon of fossil angiosperms, Callicrypta chlamydea n. gen., n. sp., isestablished for a minute pistillate flower less than 2 mm wide from the mid-Cretaceous (Cenomanian) of East Siberia. It is preserved as compression,showing under SEM a calyx of six sepals, a biserrate corolla and an apocar-pous gynoecium. Pollen grains adhering to the perianth are like in Freyantha,a staminate flower from contemporaneous deposits. These floral structuresare compared with the Amborellaceae and Menispermaceae suggesting a pos-sible link between these families, with implications for the current concept ofbasal angiosperms.

    RSUMDcouverte dune petite fleur dans le Crtac moyen de Sibrie et ses implicationsdans le problme des angiospermes basaux. Un nouveau taxon dangiosperme fossile, Callicrypta chlamydea n. gen., n. sp.,du Crtac moyen de Sibrie orientale, est dcrit. Le matriel qui lui est rap-port se compose dune petite fleur carpellaire de moins de 2 mm de largeur.Lexamen au SEM montre un calice six spales, une double corolle et ungynce apocarpe. Des grains de pollen sont galement conservs et associs la fleur carpellaire, une disposition qui est dj connue chez Freyantha. Cesfleurs sont compares avec celles des Amborellaceae et des Menispermaceae,elles partagent certaines caractristiques qui indiqueraient une parentpossible avec ces familles. Le concept dangiosperme basal est discut.

    KEY WORDS Plant morphology,

    flower, basal angiosperms,

    ranunculids, pollination ecology,

    Cretaceous, Cenomanian,

    Siberia, new genus,

    new species.

    MOTS CLSMorphologie vgtale,

    fleur, angiospermes basaux,

    ranunculides, cologie de la pollinisation,

    Crtac, Cnomanien,

    Sibrie, nouveau genre,

    nouvelle espce.

  • INTRODUCTION

    We describe a new fossil flower that is the smallestof the hitherto found, yet showing a high degree ofmorphological accomplishment of its miniatureparts and having a certain bearing on the problemof basal angiosperms (Mathews & Donoghue1999; Qiu et al. 1999; Sampson 2000; Endress2001; Hesse 2001). This find supports our earlierview that small size and dicliny are primitivewhereas large perfect flowers are derived (Krassilov1984, 1997). It contributes to a diversity of earlyranunculids comprising forms related to the pres-ent-day Ranunculaceae, Menispermaceae,Sargentodoxaceae and even Paeoniaceae as a linkto the Dilleniales, hence fairly differentiated in themid-Cretaceous already (Vakhrameev & Krassilov1979; Krassilov et al. 1983; Krassilov 1984;Krassilov & Golovneva 2001).

    MATERIAL AND METHODS

    The material was obtained by bulk macerationof a slab from the plant-bearing clay horizon inthe lower part of Timerdyakhskaya Formation(Cenomanian) in the middle reaches of theTyung River about 200 km upstream of itsconfluence with the Vilyuy River, easternSiberia. The locality has been described inVakhrameev (1958) and the recent finds ofhamamelid remains are reported in Maslova &Golovneva (2000). The flower was picked fromamong the mesofossil debris, cleaned from theremaining rock matrix with hydrofluoric acid,cleansed in distilled water, photographed withstereomicroscope, mounted on SEM stub andcoated with gold. No parts were removed. Thepollen grains sticking to the perianth andcarpels were noticed when scanning the flowerwith CAMSCAN.

    MORPHOLOGICAL DESCRIPTION

    The flower is preserved as a compression withparts radially spreading in four overlapping

    whorls (Figs 1A; 2). It appears somewhat zygo-morphic, the longer axis 1.8 mm, shorter axis1.4 mm. However the original symmetrymight have been distorted by a slightly obliquecompression. Hence the flower is describedlater on as actinomorphic or slightly zygomor-phic. The receptacle is not preserved, leaving ahole 0.4 mm wide in the center. Since it israther large in comparison with the carpels itmight have been expanded with divergence ofthe latter. The flower shows three cycles of perianth and anincomplete apocarpous gynoecium inside. Theoutermost perianth members are thin membran-ous sepals, apparently in a single whorl of six, ofwhich five are preserved and the sixth one (bot-tom right in Fig. 1) is required by the symmetry.They are c. 0.6 mm long, elliptical, apicallysmoothly rounded, flat, apparently brittle, with aconspicuous epidermis cell pattern.The next perianth cycle is turned about 25clockwise against the calyx, its members alternat-ing with the sepals and readily distinguishable bybeing shorter, 0.55 mm long, thicker, ovate inoutline, proximally concave, with involute mar-gins and narrow blunt apex. They are slightlyimbricate basally, but apparently distinct(Figs 1C; 2).The innermost perianth segments are clasped bythe outer petals, although they appear slightlydisplaced clockwise (Fig. 1C). The inner petalsare considerably smaller than the outer ones,0.35-0.40 mm long, membranous, roundedovate, flat or only slightly concave, notched at theapex. A better preserved inner petal shows apapillate body at the apical notch that can be anectary (Fig. 1E). The body is thick with distinctborders, of irregular outline, 87 m long, coveredwith dense relatively large hollow papillae that areelongate, apically depressed, leaving ellipticalscars when detached.One of the outer petals (bottom left in Fig. 1A)clasps a tubular appendage 0.24 mm long,0.08 mm thick that appears as a filament of astaminode the distal part of which is squashed(Fig. 1D). Two pollen grains were found stick-ing among the fragments of the distal part,

    Krassilov V. A. & Golovneva L. B.

    6 GEODIVERSITAS 2004 26 (1)

  • A new mid-Cretaceous flower from Siberia

    7GEODIVERSITAS 2004 26 (1)

    A B

    C D

    E F

    S

    C

    Po

    Pin

    FIG. 1. Callicrypta chlamydea n. gen., n. sp. from the Cenomanian of Vilyuy Basin, Siberia, SEM photographs; A, holotype, a pistil-late flower with a calyx, biseriate corolla, and apocarpous gynoecium (see Fig. 2 for interpretation); B, carpel with a short style, ab-axial aspect; C, radial sequence of sepal (S), outer petal (Po), inner petal (Pi) and carpel (C), the carpel is split in the median planeshowing the locule, the position of papillate gland on the inner petal is marked as n; D, tubular structure (staminode?) clasped atbase by the inner petal; E, papillate gland (nectary?) below the apical notch of an inner petal (see n); F, carpel, lateral view, stylemissing. Scale bars: A, 300 m; B, 120 m; C, 90 m; D, 40 m; E, 21 m; F, 70 m.

  • which can be a mere coincidence, although sta-minodes sometimes produce some amount ofsterile pollen.The carpels facing the observer are in a singlewhorl, widely separated, opposite to the innerpetals or only slightly displaced against them.A carpel in posterior view (Fig. 1B) is ovatewith a broad base, broadly rounded distally,0.4 mm long, with a single style 50 m long. Itshows a median keel and thin striation corres-ponding to longitudinal rows of large epi-dermal cells. The style is filled with a spongytissue, distally slightly expanded and notched,perhaps at the base of stigma that is not pre-served. A carpel in lateral view (Fig. 1F) isgibbose, with an apical notch where the stylewas broken off. It appears incompletely sealednear the apex, but this may be owing to lateralcompression. Still another carpel (Fig. 1C) issplit, showing a single locule. Ovules are notpreserved.

    The surface of sepals appears granular owing tothe slightly bulging polygonal epidermal cells dis-posed in longitudinal files. The outer petals aresmooth, with a faint longitudinal striation overthe margins. The inner petals are marked by irre-gularly scattered rounded pits. The carpels areabaxially pubescent, with dense hair bases andoccasionally preserved unicellular hairs c. 10-15 mlong.The pollen grains found sticking to the petals andcarpels are all of the same morphotype, slightlyoblate, tricolpate, reticulate, equatorial aspectrounded-elliptical, polar aspect trilobate, withdeeply incised lobes, equatorial diameter 18-20 m, polar axis 16-18 m. The colpi are slit-like, slightly invaginate, long, nearly reaching thepoles. The surface reticulum is polygonal, scarce-ly differentiated on the colpi margins, with thickmuri and relatively narrow lumina of rounded,elliptical, triangular, elongate, arcuate or irregularshapes (Fig. 3).

    Krassilov V. A. & Golovneva L. B.

    8 GEODIVERSITAS 2004 26 (1)

    FIG. 2. Callicrypta chlamydea n. gen., n. sp., a flower from the Cenomanian of Vilyuy Basin, Siberia, outline of the holotype (seeFig. 1A) showing interpretation of the floral parts. Abbreviations: C, carpel; Pi, inner petal; Po, outer petal; S, sepal; St , staminode?.Scale bar: 150 m.

  • SYSTEMATICS

    Our material is fairly different from all hithertodescribed fossil flowers in combining very smallsize with dicliny, hexamerous structure, well dif-ferentiated perianth and apocarpous gynoeciumof many carpels. Most early (mid-Cretaceous)flowers are considerably larger, pentamerous withbracteate perianth of undifferentiated tepals andvariously connate carpels (reviewed in Friis &Crepet 1987; Krassilov 1997). The comparisonsbased on surveys of angiosperm families(Hutchinson 1926; Takhtajan 1966; Heywood1978; Cronquist 1981; Goldberg 1986;Zomlefer 1994) have revealed the closest affini-ties with the Menispermaceae, in which the flow-ers are minute diclinous, with staminodes in thepistillate ones, hypogynous and basically trimer-ous, with a calyx of typically six sepals and a bise-riate to triseriate corolla of distinct (rarelyconnate) petals. The petals are smaller than sepals(indistinguishable in the tribes Coscineae andAnomospermae) and often valvate, without nec-taries in this family but nectariferous in the close-ly allied Sargentodoxaceae and Lardizabalaceae.The gynoecium is apocarpous of six (rarely more)free carpels in a single whorl. The carpels are asci-diform, gibbose, with a short style or sessile stig-mas, unilocular, producing two ovules initially,but uniovulate at maturity (Imkhanitskaya 1980;Thanikaimoni 1986). Most features are sharedalso with the Sargentodoxaceae in which, how-ever, the carpels are spiral and more numerous. The monotypic Amborellaceae is similar inhaving minute pistillate flowers only 3-5 mm indiameter, with five or six gibbose pubescent uni-locular carpels and often with a solitary stamino-de, yet the floral organs appear more distinctlyspiral in mature flowers (Endress 2001).Kingdonia, a ranunculoid genus included in theCircaeasteraceae or sometimes considered asrepresenting a monotypic family Kingdoniaceae(Foster 1961; Cronquist 1981), is similar in thegeneral aspect of flowers, morphology of gynoe-cium and petaloid sepals. The nectariferous sta-minodes of Kingdonia are perhaps homologous tonectariferous petals of the fossil flower, yet the

    A new mid-Cretaceous flower from Siberia

    9GEODIVERSITAS 2004 26 (1)

    A

    B

    C

    FIG. 3. Pollen grains adhering to the petals and carpels ofCall icrypta n. gen., n. sp., a pisti l late f lower from theCenomanian of Vilyuy Basin, Siberia; A, polar aspect; B, obliqueequatoriopolar aspect; C, lateral aspect. Scale bars: 3 m.

  • petals are formally lacking in the former genusand the flowers are monoclinous. The tricolpatepollen grains of Kingdonia are like those foundadhering to the fossil flower (Nowicke & Skvarla1982; Savitsky 1982).The adhering pollen grains are too numerous tobe just occasional. They might come from thesame plant (or adjacent plant with staminateflowers, if dioecious). Remarkably, the pollengrains are similar to those produced by staminateflowers Freyantha sibirica Krassilov et Golovneva(2001) in the shape and dimensions, as well as inconfiguration of the surface reticulum and thelong slit-like invaginate colpi nearly reaching thepoles. Freyantha sibirica came from approximate-ly the same stratigraphic horizon, but from a dif-ferent sedimentary basin within the broadgeographic region. It is represented by a racemoseinflorescence with minute prophylls bearing theshortly pedicellate staminate flowers of five or sixhemispiral (transitional from spiral to circular:Weberling 1989) stamens the anterior of whichconstantly forms a basally connate group of three,subtended by three calyptrate bracts with promi-nent abaxial glands (Figure 4 gives a better idea ofthe structure than the original black and whiteillustrations).The affinities of Freyantha have been sought withthe Menispermaceae and Sargentodoxaceae, thusit might have been actually related to the newform, which explains the similarity of pollengrains. The flowers are minute in both, but atleast twice larger in Freyantha than in the newform. In the Menispermaceae, the staminate flow-ers are sometimes larger than the pistillate ones,yet the distinctions in the perianth structures,bracteate in Freyantha vs. differentiated into calyxand corolla in the new form, indicates that theybelonged to different genera within the group.Fossil menisperms are represented by peltateleaves (Menispermites) that are not easily distin-guishable from those of the Nymphaeaceae,Piperaceae (Peperomia), Platanaceae, etc., there-fore not reliable as evidence of the family. Thefairly distinctive curved and sculptured endocarpsof menisperms have not been found until thePalaeocene. A peculiar extinct genus Nordenskioldia

    is based on the pistillate inflorescences bearingflowers with a calyptrate perianth of connatebracts and an apocarpous gynoecium.Nordenskioldia has been traditionally assigned tothe Trochodendraceae (Kryshtofovich 1958;Crane et al. 1991; Pigg et al. 2001) although itbetter complies with the Menispermaceae onaccount of perianth and the apocarpy (in Tro-chodendron the carpels are proximally connate toabout half their length) and to the Illiciaceae onaccount of floral axis protruding beyond thegynoecium (Krassilov in Krassilov & Fotyanova1995). It is readily distinguishable from the newform in the perianth structure and the morenumerous carpels. Other supposed ranunculids include Caspiocarpuswith small unicarpellate flowers (Vakhrameev &Krassilov 1979; Krassilov 1984) and Hyrcanthawith relatively large monoclinous pentamerousflowers of an inconspicuous undifferentiatedperianth and the urn-shaped carpels topped bythe broad sessile stigmas (Krassilov et al. 1983).Neither of these genera is matching the new format the generic level. It is therefore considered hereas representing a new genus.

    Genus Callicrypta n. gen.

    TYPE AND ONLY SPECIES. Callicrypta chlamydean. sp.

    ETYMOLOGY. From kallos (Greek) = beauty, andkrypte (Greek) = to hide.

    DIAGNOSIS. Pistillate flower minute actinomorphicor slightly zygomorphic, hypogynous, with a calyx of sixsepals, a biseriate corolla and an apocarpous gynoeciumof six carpels. A single or few staminodes might havebeen present. The sepals are membranous, brittle, largerthan petals. The outer petals are relatively thick, valvate.The inner petals are much smaller, with apical glands,supposedly nectariferous. The carpels are ascidiform,unilocular, with a short style, densely pubescent.

    Callicrypta chlamydea n. sp.(Figs 1-3)

    HOLOTYPE. Komarov Botanical Institute, St.Petersburg, No. 1181-3-585(1), a flower from theCenomanian (Timerdyakhskaya Formation) of the

    Krassilov V. A. & Golovneva L. B.

    10 GEODIVERSITAS 2004 26 (1)

  • A new mid-Cretaceous flower from Siberia

    11GEODIVERSITAS 2004 26 (1)

    TABLE 1. Morphological comparison of Cretaceous ranunculids with the Amborellaceae, Menispermaceae and allied families.

    Characters Amborellaceae Menispermaceae and Freyantha related families Callicrypta n. gen.

    Growth habit Small scrambling tree or shrub Diverse, commonly smallscrambling trees or shrubsas is also the monotypicSargentodoxaceae

    Unknown, yet a slenderaxis and minute prophyllsof Freyantha suggest adiminutive habit

    Leaves Alternate, entire or rarely lobed Alternate, entire or rarelylobed, occasionally peltate

    In Freyantha lobbed ofLiriodendropsis type

    Sex allocation Dioecious Commonly dioecious Unknown, probablydioecious since and came from different localities

    Inflorescence Axillary cyme Axillary or supra-axillarycymes or racemes

    Supra-axillary raceme inFreyantha

    Prophylls Small scales on peduncle Occasionally conspicuousin Menispermaceae(Cissampelos), scaly inLardizabalaceae andSargentodoxa

    Small scales on pedunclein (Freyantha)

    Flower symmetry Actinomorphic, hypogynous orslightly perigynous

    Actinomorphic, or somewhatzygomorphic hypogynous

    Actinomorphic or slightlyzygomorphic, hypogynous

    Flower morphology

    Minute, 3-5 mm in diameterfunctionally diclinous, with 1-2staminodes in pistillate flower

    Minute, diclinous withrudimentary organs ofopposite sex

    Minute, diclinous with asingle staminode inpistillate flower

    Perianth Of variable numbers of distincttepals, sepals and petalsindistinguishable

    Of variable number,commonly 6, distinct,occasionally connatesepals and smaller valvatebiseriate petals(indistinguishable in thetribes Coscineae andAnomospermae),nectariferous inSargentodoxaceae andLardizabalaceae

    Perygonal of bracteate,calyptral nectariferoustepals in Freyantha,heterochlamydeous ofdistinct mebranous sepalsand valvate biseriatenectariferous petals inCallicrypta n. gen.

    Floral receptacle Expanded, cuplike in bud Somewhat expanded inMenispermaceae, elongatein Sargentodoxaceae

    Elongate in Freyantha,broad relative to carpels,apparently expanded inCallicrypta n. gen.

    Floral phyllotaxis Spiral in mature flowers, atearly stages indistinguishable

    Bi- to multiseriate, inSargentodoxaceaehemicyclic (transitionalfrom spiral to cyclic)

    Transitional from spiral tocyclic in Freyantha, cyclic(petals bicyclic) inCallicrypta n. gen.

    Pollination Mixed anemo- or entomophilous Anemo- or entomophilous Supposedly entomophilous

    Staminate flowers

    With 9-11 tepals and a morenumerous, 12-21, stamens inseveral cycles, bearing arudimentary gynophore

    With 6, rarely fewer or morenumerous biseriatestamens mostly oppositethe petals

    With 3 bracteate tepals and6 stamens, hemicyclic,indistinctly biseriate

  • Krassilov V. A. & Golovneva L. B.

    12 GEODIVERSITAS 2004 26 (1)

    Stamens Basally adnate to inner tepals,with a short filament,connective protruding, anthers bithecate introrse

    Free to variously connate,connective occasionallyinflated, sometimesprotruding(Chondrodendron), anthers bithecate, mostlyintrorse, with a shortfilament and a broadprotruding connective inSargentodoxaceae, someLardizabalaceae(Decaisnea) andBerberidaceae (Nandina)

    Free or the anterior slightlyconnate, with a shortfilament and protrudingconnective, anthersbithecate, apparentlyintrorse

    Characters Amborellaceae Menispermaceae and Freyantha related families Callicrypta n. gen.

    Anther opening By longitudinal slit By longitudinal slit By longitudinal slit

    Pollen grains Monoporate operculateor inaperturate

    Of diverse apertural types more commonlytricolpate, tricolporate,porate or inaperturate.Tricolpate irregularlyreticulate with long slit-likeinvaginate colpi inSargentodoxaceae

    Tricolpate irregularlyreticulate with long slit-likeinvaginate colpi inFreyantha and dispersedadhering to Callicryptan. gen.

    Pistillate flowers Smaller than the staminate,with 1-2 staminodes

    Commonly withstaminodes

    Smaller than Freyantha,with a single staminode

    Gynoecium Apocarpous Apocarpous, often on agynophore, with carpelswidely diverging in theLardizabalaceae

    Apocarpous, with widelydiverging carpels

    Carpels In a single whorl, mostly 5-6,minute, gibbose, ascidiform,shortly stipitate, unilocular

    Commonly 6 (1-3 to 30) inone or more cycles,gibbose, unilocular,unsealed inLardizabalaceae

    6 in a single whorl, minute,distinct, sessile, gibbose, incompletely sealed,unilocular

    Stigma Sessile, bilobed, withmulticellular papillae

    Sessile or on a very shortstyle

    On a short style

    Ovule In mature carpels solitary,hemitropous (or described asorthotropous curved at base),bitegmic

    Initially 2, but in maturecarpels single, mostly bitegmic. In Sargentodoxasolitary hemianatropous

    Unknown

    Endosperm Abundant Scanty in Menispermaceae, yet abundant inSargentodoxaceae andLardizabalaceae

    Unknown

    Fruit Drupaceous Aggregates of drupes ornutlets

    Aggregates of nutlets in association withFreyantha

  • middle reaches of Tyung River about 200 kmupstream of its confluence with the Vilyuy River,eastern Siberia.

    ETYMOLOGY. Chlamidea (from Greek) with a man-tle (perianth).

    DIAGNOSIS. As for the genus.

    DISCUSSIONCallicrypta chlamydea n. gen., n. sp. is similar toAmborellaceae in general aspect of the minutediclinous oligomerous flowers of free parts, withone or few staminodes and with a single whorl offive or six gibbose ascidiform carpels. At the sametime, it shares with the Menispermaceae and/orthe allied ranunculid families Sargentodoxaceae,Lardizabalaceae and Kingdoniaceae such diagnos-tic features of floral morphology as the calyx ofpetaloid sepals, corolla of more numerous biseri-ate nectariferous petals which are smaller thansepals, imbricate and valvate, clasping the stami-nodes, and the apocarpous gynoecium of sixcarpels with a short style. Callicrypta chlamydean. gen., n. sp., thus, indicates an affinity between

    the Amborellaceae and Menispermaceae, whichcan be reinforced by involving in the comparisonthe staminate flowers of the Cretaceous ranuncu-lid Freyantha sibirica which produced pollen ofthe same type as found attached to Callicryptachlamydea n. gen., n. sp. The morphological comparison (Table 1) placesboth these Cretaceous species in the plexus ofarchaic ranunculids the present day survivors ofwhich form the monotypic families Sargen-todoxaceae, Kingdoniaceae, Circaeasteraceae,Glaucidiaceae and the closely allied Amborellaceae.A traditional assignment of Amborella to theLaurales (Monimiaceae) is based mainly on asingle feature in common, the inflated floralreceptacle (Cronquist 1981) that occurs, althoughin a less conspicuous form, in the Menisper-maceae also. A recently advocated link to theNymphaeales (Mathews & Donoghue 1999; Qiuet al. 1999), an order of aquatic angiosperms, isscarcely justified by a few homoplastic featuresin common, such as the porose vessels (Schneider& Carlquist 1996) or a spiral floral phyllotaxis,

    A new mid-Cretaceous flower from Siberia

    13GEODIVERSITAS 2004 26 (1)

    FIG. 4. Freyantha sibirica Krassilov et Golovneva (2001), from the Cenomanian of Tschulymo-Yenisey Basin, Siberia, inflorescenceof staminate flowers subtended by calyptrate bracts with a prominent nectar gland (n). Scale bar: 1.5 mm.

    n

  • widely scattered among the angiosperm orders.The tracheary elements in Amborella with smallpores in pit membranes or altogether lacking pitmembranes are unlike those in Nymphaeaceaewith large pores (Field et al. 2000). The morestrictly diagnostic features of the flower topology,gynoecium, ovules, fruit, pollen grains, etc., areso disparate that a detailed comparison does notmake much sense. Basic nymphaeaceous floralstructure has been fairly distinct in the mid-Cretaceous already (Krassilov & Bacchia 2000). We emphasize the extreme diminution of the flower in Callicrypta n. gen. not only because itcounters once popular idea of primitiveness, butalso because dimensions are important in pollina-tion ecology. Our studies of gut contents of fossilinsects have revealed a widespread Palaeozoic andMesozoic pollen feeding by various relatively largeinsects, such as hypoperlids, booklice, katydidsand xyelids (Krassilov & Rasnitsyn 1998). Floralorgans of proangiosperms might have been visitedfor pollen primarily, as in the case of Preflosella, anEarly Cretaceous pre-flower foraged by two xyelidspecies (Krassilov & Rasnitsyn 1998). Co-adapta-tion of plants and pollinivorous insects implied acertain robustness of floral organs. A miniaturization of floral parts accompanied by adevelopment of secreting structures (glands on thebracteate tepals in Freyantha sibirica and on theinner petals in Callicrypta chlamidea n. gen., n. sp.)suggests a major innovation in pollination ecologyinvolving new groups of insects coming for nectarand capable of gently handling the flower. This lineof co-evolution might have led to a diversificationof forms related to the present-day ranunculids.The finds of such forms in the mid-Cretaceous ofSiberia and northern Kazakhstan (Caspiocarpus:Vakhrameev & Krassilov 1979; Krassilov 1984;Hyrcantha: Krassilov et al. 1983) suggest a diversifi-cation center in the northern temperate realm.

    AcknowledgementsWe thank the reviewers, W. L. Crepet and an ano-nymous one, for their valuable comments. Thiswork was supported by the Russian Foundationof Basic Research, grant 03-05-64794.

    REFERENCES

    CRANE P. R., MANCHESTER S. R. & DILCHER D. L.1991. Reproductive and vegetative structure ofNordenskioldia (Trochodendraceae), a vessellessdicotyledon from the early Tertiary of the NorthernHemisphere. American Journal of Botany 78:1311-1334.

    CRONQUIST A. 1981. An Integrated System ofClassification of Flowering Plants. ColumbiaUniversity Press, New York, 1262 p.

    ENDRESS P. K. 2001. The flowers in extant basalangiosperms and inferences on ancestral flowers.International Journal of Plant Science 162: 1111-1140.

    FIELD T. S., ZWEINIECKI M. A., BRODRIBB T., JAFFRT., DONOGHUE M. J. & HOLBROOK N. M.2000. Structure and function of tracheary ele-ments in Amborella trichopoda. International Journalof Plant Science 161: 705-712.

    FOSTER A. S. 1961. The floral morphology andrelationships of Kingdonia uniflora. Journal ArnoldArboretum 42: 397-415.

    FRIIS E. M. & CREPET W. L. 1987. Time ofappearance of floral features, in FRIIS E. M.,CHALONER W. C. & CRANE P. R. (eds), TheOrigins of Angiosperms and their MorphologicalConsequences . Cambridge University Press,Cambridge: 145-180.

    GOLDBERG A. 1986. Classification, evolution andphylogeny of the families of dicotyledons.Smithsonian Contributions to Botany 58: 1-314.

    HESSE M. 2001. Pollen characters of Amborellatrichopoda (Amborellaceae): a reinvestigation.International Journal of Plant Science 162: 201-208.

    HEYWOOD V. H. (ed.) 1978. Flowering Plants of theWorld. Oxford University Press, Oxford, 335 p.

    HUTCHINSON J. 1926. The Families of FloweringPlants, 1. Dicotyledons. MacMillan, London, 328 p.

    IMKHANITSKAYA N. N. 1980. [Family Meni-spermaceae], in TAKHTAJAN A. L. (ed.), Plant Life 5,Flowering Plants. Prosvescheniya, Moscow: 198-205(in Russian).

    KRASSILOV V. A. 1984. New paleobotanical data onorigin and early evolution of angiospermy. Annals ofMissouri Botanical Garden 71: 577-592.

    KRASSILOV V. A. 1997. Angiosperm Origins:Morphological and Ecological Aspects. Pensoft, Sofia,270 p.

    KRASSILOV V. A. & BACCHIA F. 2000. Cenomanianflorule of Nammoura, Lebanon. Cretaceous Research21: 785-799.

    KRASSILOV V. A. & FOTYANOVA L. I. 1995. Newhamamelid fructification from the Paleocene ofKamchatka, with comments on Trochodendrocarpusand Nordenskioldia. Paleontological Journal 29 (A):87-95.

    KRASSILOV V. A. & RASNITSYN A. P. 1998. Plantremains from the guts of fossil insects: evolutionaryand palaeoecological inferences. Proceedings of the

    Krassilov V. A. & Golovneva L. B.

    14 GEODIVERSITAS 2004 26 (1)

  • 1st International Palaeoentomological Conference,Moscow, AMBA Projects AM/PFICM-98/1.99:65-72.

    KRASSILOV V. A. & GOLOVNEVA L. B. 2001. Inflorescence with tricolpate pollen grains from theCenomanian of Tschulymo-Yenisey Basin, WestSiberia. Review of Palaeobotany and Palynology 115:99-106.

    KRASSILOV V. A., SHILIN P. V. & VAKHRAMEEV V. A.1983. Cretaceous flowers from Kazakhstan.Review of Palaeobotany and Palynology 40: 91-113.

    KRYSHTOFOVICH A. N. 1958. [The Cretaceousflora of Anadyrland]. Transactions of BotanicalInstitute Series 8, Palaeobotany 3: 9-70 (in Russian).

    MASLOVA N. P. & GOLOVNEVA L. B. 2000. Ahamamelid inflorescence with in situ pollen grainsfrom the Cenomanian of Eastern Siberia. Paleon-tological Journal 34 (Supplement 1): 40-49.

    MATHEWS S. & DONOGHUE M. J. 1999. The rootof angiosperm phylogeny inferred from duplicatephytochrome genes. Science 286: 947-950.

    NOWICKE J. & SKVARLA J. 1982. Pollen morpholo-gy and the relationship of Circaeaster, of Kingdonia,and of Sargentodoxa to the Ranunculales. AmericanJournal of Botany 69: 990-998.

    PIGG K. B., WEHR W. C. & ICKERT-BOND S. M.2001. Trochodendron and Nordenskioldia(Trochodendraceae) from the Middle Eocene ofWashington State, USA. International Journal ofPlant Science 162: 1187-1198.

    QIU Y.-L., LEE J., BERNASCONI-QUADRONI F., SOLTISD. E., SOLTIS P. S., ZANIS M., ZIMMER Z. A.,

    CHEN Z., SOVALAINEN V. & CHASE M. V. 1999. The earliest angiosperms: evidence from mitochon-drial, plastid and nuclear genomes. Nature 402:404-407.

    SAVITSKY V. D. 1982. [Morphology, Classificationand Pollen Evolution in the Family Ranunculaceae].Naukova Dumka, Kiev, 124 p. (in Russian).

    SAMPSON F. B. 2000. Pollen diversity in somemodern magnoliids. International Journal of PlantScience 161: 193-210.

    SCHNEIDER E. L. & CARLQUIST S. 1996. Vessel originin Cabomba. Nordic Journal of Botany 16: 637-641.

    TAKHTAJAN A. L. 1966. [System and Phylogeny ofFlowering Plants]. Nauka, Moscow; Leningrad,611 p. (in Russian).

    THANIKAIMONI G. 1986. Evolution of Meni-spermaceae. Canadian Journal of Botany 64:3130-3133.

    VAKHRAMEEV V. A. 1958. [Stratigraphy and FossilFlora of the Jurassic and Cretaceous Deposits in theVilyuy Depression and the Adjacent Part ofPriverhoyansk Trough]. USSR Academy of SciencePress, Moscow, 138 p. (in Russian).

    VAKHRAMEEV V. A. & KRASSILOV V. A. 1979. Reproductive organs of angiosperms from theAlbian of Kazakhstan. Palaeontological Journal,Moscow 1: 121-128.

    WEBERLING F. 1989. Morphology of Flower.Cambridge University Press, Cambridge, 405 p.

    ZOMLEFER W. B. 1994. Guide to Flowering PlantFamilies. University of North Carolina Press,Chapel Hill, 430 p.

    Submitted on 14 November 2002;accepted on 2 June 2003.

    A new mid-Cretaceous flower from Siberia

    15GEODIVERSITAS 2004 26 (1)