Fossil Evidence for Root Parasites (resembling Balanophoraceae) in a Late Triassic Tropical Rift Basin, Central Pangaea

Bruce Cornet, Ph.D.

Abstract

    The time of angiosperm origin still eludes botanists. During the past four decades several hypotheses have been proposed.  Two became so supported by data and popular among paleobotanists that they were elevated to theories: The Cretaceous Origin and Primary Radiation Theory and the Anthophyte Theory of Angiosperm Origin, which extended angiosperm evolution back to the Early Mesozoic.  Recently molecular biology falsified the Anthophyte Theory, and provided additional support for earlier molecular studies that angiosperms have been independent of extant gymnosperms back to their roots in the Devonian and Carboniferous.  Molecular data have also caused a revolution in the theoretical phylogenetic hierarchy of angiosperms, changing botanical concepts about the most primitive living angiosperms.  Within the new framework fossil plants such as Sanmiguelia lewisii from the Late Triassic of Southwestern United States are enjoying renewed interest, whereas before they were rejected because they conflicted with popular theories and now false evolutionary trees. 

    One enigmatic fossil plant from a paleotropical Late Triassic basin in Virginia went unnoticed for 30 years, because 1) the work of its discoverer was not taken seriously by other paleobotanists, and 2) it was erroneously described as an araucarian conifer, a taxon which is unremarkable in the Mesozoic fossil record.  Root holoparasites such as the pantropical Balanophoraceae are rejected by most botanists as having anything to do with the habits of the earliest angiosperms, and yet they may provide a partial answer to Darwin's "abominable mystery".  Now there is reason to reevaluate the Triassic fossils from a new perspective: evidence for a root parasitic habit on swamp cycadophytes and tree ferns.  Three of Bock's fossil species are redescribed and compared to members of the family Balanophoraceae.  One compares with Langsdorffia in basic inflorescence construction, although outwardly it resembles Ombrophytum and Lathrophytum; the second is compared and contrasted with Lathrophytum, but the third compares so closely with Lophophytum that it could represent an example of convergent evolution.  If these Triassic taxa are indeed basal angiosperms, they would represent the oldest megafossil record yet (~230 mya) of the subdivision Angiospermae, and would add a substantial wrinkle to the habits and habitats of the first angiosperms.

Table of Contents

Introduction
Description and Distribution of Extant Taxa

Primaraucaria wielandii
     Primaraucaria species 2
Triassiflorites grandifolia
Discussion with Comparison
Conclusion
References


Introduction

    Several gymnospermous groups have been proposed as ancestral to the angiosperms: Glossopteridales, Pteridospermales, and Gnetales, but through recent molecular studies, all extant gymnosperms can be excluded, including the Gnetales, which were the latest suspects in the falsified Anthophyte Theory of Angiosperm Origin (Donoghue and Doyle, 2000).  That leaves only those groups of gymnosperms which are extinct: Glossopteridales and Pteridospermales (unrelated to the Cycadales).

    Angiosperm taxonomy is going through a major revision in evolutionary hierarchy based on the falsification of old schemes by molecular data (e.g. Wolfe et al., 1989; Winter et al., 1999; Doyle and Endress, 2000; Sanderson and Doyle, 2001).  The Magnoliales, for example, were once thought to contain basal angiosperms, while the Nymphaeales were thought to be more derived than the Magnoliales.  As recently as a decade ago the Chloranthaceae, Schizandraceae, and Trimeniaceae were thought to contain basal angiosperms, but now hold a more derived status than the Nymphaeaceae.  With the discovery of Archaefructus - an aquatic angiosperm - in possible latest Jurassic strata containing fossils of feathered dinosaurs (Sun et al., 1999; 2002), coupled with the presence of waterlily-like leaves in Barremian-Albian strata of Virginia (Hickey and Doyle, 1977), genetic studies are being taken more seriously by paleobotanists and taxonomists.  As a consequence, phylogenetic trees have changed considerably (e.g. Doyle and Endress, 2000; Doyle, 2001).  And with that change the Triassic and Jurassic data discovered and published by Cornet (1986, 1989a, 1989b, 1996), Cornet and Habit (1992), and Hochuli and Feist-Burkhardt (2004) seem to fit much better than before (see Why.htm).

    On the one hand, recently molecular data have identified Amborella trichopoda as the most primitive living flowering plant (Stephens, 1999).  On the other hand, the molecular relationships between the members of the Balanophoraceae and their pantropical and subtropical world distribution imply that this family arose prior to the complete breakup of Pangea (including Gondwanaland) during the Early Cretaceous.  Nickrent (2003) states under Phylogeny:

"Click HERE to see a tree generated using nuclear small-subunit (18S) rDNA sequences from 11 of the possible 17 genera of Balanophoraceae, with Amborella included as an outgroup. Note the strong biogeographical nature of the tree, with the Neotropical taxa forming one clade that is derived from within the Paleotropical grade. The association of Dactylanthus and Hachettea follows traditional classifications (e.g. Dactylanthaceae sensu Takhtajan 1997), however, the additional association with Mystropetalon (Mystropetalaceae sensu Takhtajan 1997) is surprising. Despite the wide geographic separation (S. Africa, New Zealand, and New Caledonia), these data suggest an ancient southern hemisphere association that traces to ancestors on the Gondwanan landmass." (Nickrent, 2003http://www.science.siu.edu/parasitic-plants/tables/Table-holopars.html

Balanophphylo.gif (11568 bytes)

Image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/images/Balanoph.phylo.gif

    The relationship of the Balanophoraceae (and most parasitic angiosperms) to other angiosperms is more equivocal, however.  See Relationships of Parasitic Flowering Plants at http://www.science.siu.edu/parasitic-plants/Relation-Flowering.html.

    During his investigation into pre-Cretaceous fossils that might have a bearing on the evolution of angiosperms, Cornet came across a group of fossils discovered by Wilhelm Bock, an amateur self-taught paleontologist. His fossils came from a tropical rift basin in Virginia containing a diverse flora of large-leaved pteridosperms, cycadophytes, pteridophytes (including tree ferns), horsetails, and lycopods.  Unfortunately Bock did not have enough botanical training to recognize the uniqueness of these fossils, and he forced them either into the family Cycadales or into the family Araucariaceae.  Because one species had a superficial resemblance to brachyphyll shoots with attached conifer-like cones, and because his specimens were older than previously reported Araucaria species from Gondwanaland, he lumped all the specimens under the name Primaraucaria wielandii Bock.  Bock published on these fossils in several professional papers, the most comprehensive of which is The American Triassic Flora and Global Distribution (Bock, 1969).

    A cursory examination of his numerous photographs will reveal that his fossils have a number of distinctive characteristics in common with the Balanophoraceae.  It is also within the same strata that Cornet discovered the Crinopolles group of angiosperm-like pollen with reticulate-columellate wall structure.  What is interesting about this chronologic and stratigraphic association is that both Crinopolles pollen (Triassic) and Balanochoraceae pollen (extant) have overlapping ranges in morphology and aperture condition (i.e. monosulcate, disulcate, zonasulculate, trichotomosulcate, trisulcate, pentasulcate, tricolpate, and spiraperturate for Crinopolles pollen, and monosulcate, disulcate, trisulcate, pentasulcate, tricolpate, polyporate, and foraminate for Balanophoraceae pollen).

   Four specimens of Primaraucaria were obtained from the Philadelphia Academy of Natural Sciences, where Bock had deposited them.  In his first paper on Sanmiguelia lewisii, Cornet (1986) describes his analyses of Bock's specimens.  He repeats that analysis below with additional comparisons to genera of Balanophoraceae.  Most of the fruiting heads are comprised of unisexual flowers bearing large stalked carpels, but a bisexual flower with latrorse laminar stamens was also identified.  It may contain reticulate pollen of the Crinopolles type.  Small elliptical seeds were found inside the carpels; like the seeds of the Balanophoraceae, they lacked evidence for a testa. 

Description and Distribution of Extant Taxa

    Two internet sources of information are extensively referenced and quoted or linked in this section.  One is from the web page, The Parasitic Plant Connection, by Dan Nickrent at http://www.science.siu.edu/parasitic-plants/index.html, and the other is from the web page, The Families of Flowering Plants, the Balanophoraceae, by L. Watson and M. J. Dallwitz at http://biodiversity.uno.edu/delta/angio/www/balanoph.htm (full reference given below).  Important information and images are reproduced or linked from those websites for focus and convenience, rather than providing only links.  None of the information in this section about extant taxa belongs to the author of this website.

Ombrophytum subterraneum

Ombrophytum.jpg (41732 bytes)

Above image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/images/Ombrophytum.JPEG
Below internet source: Nickrent 2003 at http://www.science.siu.edu/parasitic-plants/Balanophoraceae/

Balanophoraceae

Genera Included: Balanophora, Chlamydophytum, Corynaea, Dactylanthus, Ditepalanthus, Exorhopala, Hachettea, Helosis, Langsdorffia, Lathrophytum, Lophophytum, Mystropetalon, Ombrophytum, Rhopalocnemis, Sarcophyte, Scybalium, Thonningia. Takhtajan (1987) split Balanophoraceae into six families. Among these, molecular evidence supports only the segregation of Cynomoriaceae. Until further evidence exists, I choose to retain the above genera in a single family.
Habit: Fleshy, achlorophyllous holoparasites
Parasitism: Attaching to roots of trees and shrubs (rarely herbaceous plants) by a structure called a tuber which may contain only parasite tissue or mixtures of host and parasite. Plants often accumulating a waxy product called balanophorin.
Roots: The slender rhizomes (roots?) grow from the tuber and form haustorial connections to the host roots they encounter.
Stem: Absent (aerial portions technically an inflorescence)
Leaves: Scaly, without stomata, spirally arranged

ScybaliumDepressum.jpg (55385 bytes)

Image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/images/ScybaliumDepressum.jpg
Inflorescence: Inflorescence bearing "stems" arise endogenously within the tuber. Branches subtended by scaly, reduced, caducous bracts, which in some genera are peltate or in others triangular or clavate.

Langsdorf.jpg (71770 bytes)

Langsdorffia hypogaea (Nee and Whalen 16864). Female (above) and male (below) inflorescences both sectioned longitudinally. Photo by M. Nee taken 7/26/79 6 km west of El Junquito, Venezuela.

CorynaeaCrassa1.jpg (107152 bytes)

Corynaea crassa. Habit of plant showing inflorescence emerging from the large tuberous haustorium. Cloudforest habitat (ca. 10,000 ft.) in the Talamancas, Cuerci biological station, Costa Rica. Photo by Kyle Williams.

MOA-00484_001b.jpg (50890 bytes)

Ombrophytum sp.. Inflorescences. Photograph by Al Gentry (voucher 39680). Links to Missouri Botanical Gardens Tropicos Image Library.
Plant Sex: Plants monoecious or dioecious

Flowers: Often minute and numerous - some of the smallest flowers in the angiosperms. Unisexual, monochlamydous, entomophilous.

Calyx: Staminate flowers diverse with 3-4 (-8) distinct or basally connate, valvate tepals with a stamen opposite each tepal.

Corolla: Absent

Mystro8.jpg (72007 bytes)

Mystropetalon thomii [DLN 4091]. Female (top) and male (bottom) flowers. The ring-shaped, white elaisome that sits below the ovary can be seen enclosesd within bracts of the female flower. (Note: the fruit/elaiosome is upside down). The elaiosome is harvested by ants which disperse the one-seeded fruits. The male flowers contain two rather typical stamens (as compared to other Balanophoraceae!) that are attached to the perianth (tepals). The flower is then subtended by bracts and bracteoles. Photo by D. L. Nickrent.

Androecium: With a tetrasporangiate, dithecal anther opening by longitudinal slits. Stamens often very reduced, monothecal anther opening by a terminal pore, sometimes coalescent to form a synandrium opening irregularly from bilocular, rarely trilocular numerous transverse slits.

Pollen: 3-5 colpate or 3-many-porate or inaperturate, variously binucleate or trinucleate, the binucleate types associated with a wet stigma, the trinucleate ones with a dry one.

Mystro3.jpg (54896 bytes)

Mystropetalon thomii [DLN 4091]. Same plant as above, but excavated to show that all genets arise from the same stem. Note the new shoots being formed. A curious finding was the presence of liquid surounding the central stems. Is this produced by the parasite? What is its function? Photo by D. L. Nickrent.

Gynoecium: Carpellate flowers lacking a perianth or in 2 genera with (2) minute tepals, these hypogynous and united into a cup in Mystropetalon. Gynoecium of 2 or 3 carpels united to form a compound ovary with (2-3) distinct styles or a single trifid style or sometimes the stigma sessile and discoid, or in Balanophora the gynoecium pseudomonomerous and with a single undivided style. Ovary typically solid, without a locule or an obvious placenta or ovule (containing 1 or 2 embryo sacs - ovules very reduced). Early ontogenetic stages of the ovary sometimes showing a massive central placental column that later fuses with the ovary wall.

Ovule: Apparently absent - without recognizable nucellus or integuments.

Embryo, etc.: monosporic or bisporic. Endosperm development cellular. One few-celled embryo develops in the central tissues of the ovary and is surrounded by endosperm and a layer of sclerenchyma at maturity.

Fruit: A tiny, indehiscent, one-seeded achene. In Mystropetalon, surrounded by the swollen perianth tube. Individual fruits sometimes swollen and aggregated into a flesh multiple fruit.
Seed: Solitary with a very small, undifferentiated embryo embedded in the endosperm.
Chromosomes: X = 8, 9, 12 and more.

Distribution

http://www.science.siu.edu/parasitic-plants/Balanophoraceae/Map-Balanophoraceae.gif (6669 bytes)

Image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/

Below internet source: http://biodiversity.uno.edu/delta/angio/www/balanoph.htm

Credit: L. Watson and M. J. Dallwitz (1992 onwards). The Families of Flowering Plants: Descriptions, Illustrations, Identification, and Information Retrieval. Version: 14th December 2000. http://biodiversity.uno.edu/delta/. Dallwitz (1980), Dallwitz, Paine and Zurcher (1993, 1995, 2000), and Watson and Dallwitz (1991) should also be cited (see References).

Balanophoraceae L.C. & A. Rich.
Including Dactylanthaceae (Engler) Takhtajan, Hachettiaceae Van Tiegh., Helosidaceae (Heloseaceae) (Schott & Endlicher) Van Tiegh., Langsdorffiaceae Van Tiegh., Lophophytaceae Horan., Mystropetalaceae Takhtajan, Latraeophilaceae Leandro ex A. St.-Hil., Sarcophytaceae Horan.
Excluding Cynomoriaceae
Habit and leaf form. Herbs. Plants of very peculiar vegetative form; fungoid (the above-ground parts constitute the inflorescence, which is remarkably fungoid in appearance, pallid, brown, pink or purplish, bearing numerous flowers that are among the smallest known. The underground parts, which are attached to the host root, may be the size of a pineapple and are tuber-like in appearance, exhibiting scale-leaves in only one genus. The inflorescence develops within the ‘tuber’, ultimately rupturing it and exhibiting its remains as a ‘volva’ at the base). Leaves much reduced (but subterranean only), or absent. Plants rootless (at least in the normal sense); more or less succulent; totally parasitic. On roots of the host (of trees). Annual to perennial (without chlorophyll). Leaves when present, membranous.
Stem anatomy. Secondary thickening absent. Xylem with vessels, or without vessels. Vessel end-walls simple.
Reproductive type, pollination. Plants monoecious, or dioecious.
Inflorescence, floral, fruit and seed morphology. Inflorescences with densely crowded flowers. Flowers minute.
Perianth sepaline (sometimes, in male flowers), or vestigial to absent; when present, 3–8 (lobed); when present, free, or joined.
Androecium 1–2 (in achlamydeous male flowers), or 3–8 (equalling and opposite P). Androecial members free of one another, or coherent. Androecium exclusively of fertile stamens. Stamens 1–8; often isomerous with the perianth. Anthers cohering, or separate from one another; dehiscing via pores, or dehiscing via short slits; bilocular to four locular to many locular; tetrasporangiate. Anther epidermis persistent. Anther wall with no differentiation of an endothecium; of the ‘dicot’ type. Tapetum probably glandular. Pollen grains aperturate, or nonaperturate; when aperturate, (2–)3–5 aperturate, or 3–4(–5) aperturate; colpate, or porate, or foraminate; 2-celled.
Gynoecium 1–2(–3) carpelled. The pistil 1–2(–3) celled. Gynoecium syncarpous; synovarious; superior to inferior. Ovary 1–2(–3) locular. Gynoecium stylate (usually), or non-stylate. Styles apical. Stigmas 1, or 2. Placentation apical. Ovules 1 per locule; pendulous; without integuments. Embryo-sac development Polygonum-type, or Allium-type. Antipodal cells formed, or not formed; when formed, 1, or 2; not proliferating. Endosperm formation cellular. Endosperm haustoria present. Embryogeny piperad.
Fruit non-fleshy; indehiscent; a drupe, or a nut. The drupes with one stone. Fruit 1 seeded. Seeds endospermic; without a testa. Embryo rudimentary at the time of seed release.
Seedling. Germination type inapplicable — cotyledons lacking.
Physiology, biochemistry. Not cyanogenic. Alkaloids absent (one species).
Geography, cytology. All but one sub-tropical to tropical. Pantropical.
Taxonomy. Subclass Dicotyledonae; Crassinucelli, or Tenuinucelli (?). Dahlgren’s Superorder Balanophoriflorae; Balanophorales. Cronquist’s Subclass Rosidae; Santalales. APG (1998) family of uncertain position at the highest group level. Species 120. Genera 17; Balanophora, Chlamydophytum, Corynaea, Dactylanthus, Ditepalanthus, Exorhopala, Hachettea, Helosis, Langsforffia, Lophophytum, Mystropetalon, Ombrophytum, Rhopalocnemis, Sarcophyte, Scybalium, Thonningia.
Illustrations. • Habit and technical details (Scybalium).

Below internet source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/
Below image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/images/LathrophytumPec.jpg

Lathrophytum - no photos

LathrophytumPec.jpg (97068 bytes)

Lathrophytum peckoltii

Above image caption

Lathrophytum peckoltii. Illustration from Hansen (1980). Legend of Fig. 22. A-H, Peckolt sn 1886 after Hansen (1976), I and K (Pereira 5645) original. A, habit of young specimen, tuber lost, inflorescence covered by peltate parts of bracts X1; B, bract subtending female branch, side view X6; C, the same, front view of pelta X6; D, bract subtending male flower, from below X6; E, male flower, side view X6; F, the same, from above X6; G, female branch, side view X6; H, female flower, side view X17.5; I, habit of flowering specimen with host root, tuber, volva lobes, lower female part of inflorescence showing peltas of branches, upper male part with anthers openeed, some 30 flowers have lost the anthers X1, four male flowers with anthers open, three anthers lost, seen from distal end X2.5.
Lathrophytum peckoltii. Illustration from Hansen (1976). Legend of Figure 1: a: tuber, volva with lobes broken off, and lower part of stem, presumably old specimen (herb. M); b: stem with volva-lobes, inflorescence still covered by bracts, younger specimen (herb. C); c: longitudinal section of young specimen, inflorescence still covered by volva (herb. K); d: same, upper part enlarged, lower part of inflorescence with female-secondary axes, upper part with male-flowers; e: bract supporting male-flower, lateral view slightly from behind; f: same, from below; g: male-flower, from above; h: same, lateral view; i: bract supporting female-secondary axis, lateral view; k: same, from behind; l: same, front view; m: female-secondary axis, lateral view, flowers removed in lower part, still in position in upper part, covered outwards by the enlarged, peltate top part of branch; n: female-flower with 2 styles; o: same, longitudinal section. - Enlargement; a-c: scale 5 cm; d-m: scale 5 mm; n, o: scale 1 mm. - Material: a, b, e-o: PECKOLT s. n., leg. 1886; c, d: GLAZIOU s. n., leg. 1886.

Below internet source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/
Below image source: http://www.science.siu.edu/parasitic-plants/Balanophoraceae/images/Lophophytum2.jpg

Lophophytum2.jpg (216075 bytes)

Above image caption

Lophophytum mirabile. Inflorescence. Photo by Leppard [Leppard No. 445]. Slide no. 11934 archived at Kew.
Lophophytum mirabile and L. leandri. Illustration from Harms (1894). Figure 161 legend, translation from German. A-O Lophophytum mirabile Schott et Endl. A group of young plants in different stages of the development, on a strongly swollen host root (Nw); a = very young tubers; b = somewhat older; c tuber with the beginning of the development of leaves. d = somewhat older stage of a tuber growing into an inflorescence, without cataphylls at the lower part; e = older growing rhizomes with cataphylls covering also basal parts. B longitudinal section through a young inflorescence, showing the shieldlike stalked bracts and the individual spadices of the second order. C flowering plants, in which the bracts have been shed - D part of a female spadix of L. leandri Eichl., showing the bracts of the flowers. - E-K L. mirabile. E male flower from the side and from the front, with p = pistil vestige. F pollen (240/1). G female flower with two staminodia. H ovary in longitudinal section, ov = ovule., skl = sclerenchyma group. J longitudinal section of a somewhat older ovary, showing further advanced development of the upper ovary rim, with ovules completely adhered to the ovary wall .; spt = the septum-like extension of the placenta, es = embryosac. K longitudinal section of a fruit, pt = endocarp, s = seed. (after Eichler.)
Lophophytum weddelllii. Illustration from Hooker (1856). Fig. 1. Portion of section of male inflorescence. Fig. 2. Portion of section of female inflorescence.

Primaraucaria wielandii Bock

This section is by the author, Bruce Cornet.

    If you read what Bock (1969) says about P. wielandii, his description seems as if it were taken from a botany manual on Araucaria.  But when you examine his pictures, they don't agree with what is known about Araucaria, fossil and extant.  For one, the male reproductive structures are not cones, but flowers with perianth parts organized on an elongated inflorescence axis (spike).  Bock assumed that the adnate spirally-arranged bracts on the lower parts of inflorescence axes could be compared to the brachyphyll leaves of conifers, but they are at least three times the size of xerophytic araucarian leaves.  Bock further assumed that silicified tree trunks found in the youngest strata of the basin belonged to Primaraucaria, even though this plant was found only in the oldest strata of the basin (the two horizons are separated by as much as 6,000 feet of strata).  It has since been demonstrated that those tree trunks belonged to Glyptolepis-Pagiophyllum, a common Late Triassic conifer of North America that contributed to the formation of the Petrified Forest of Arizona.  And if you examine actual specimens, dissect them, and prepare macerations of bracts and reproductive organs as I have done, it will become apparent that this was a non-woody herbaceous plant that lived in close association with swamp vegetation, such as Macrotaeniopteris, with which it is commonly associated as a fossil.  Macrotaeniopteris had a leaf and venation that closely resembled a small version of Musa.

    Even after its angiospermous characteristics had been recognized (Cornet, 1986), its rightful place in botany had to wait for the internet and for old concepts of basal angiosperms to give way to new taxonomic hierarchies based on molecular data before such an unusual plant could be compared, let alone accepted, as possibly the oldest (parasitic) angiosperm yet recognized.

    Primaraucaria was first found by Wilhelm Bock in the 1950's, and first named in 1954.  It was found in shales of coal mine dumps at Winterpock, Virginia.  The coals from the Winterpock mine are found near the base of the stratigraphic sequence in the Richmond basin of Carnian (Late Triassic) age (Cornet and Olsen, 1990; Cornet, 1993).  At the time this plant existed, the Richmond basin was located just north of the paleo-equator in the same relative position the Balanophoraceae occur today.

Newark2b.JPG (82032 bytes)

Figure modified from Olsen and Kent (2000).

    Cornet (1986) had the opportunity to study four well-preserved specimens identified by Bock as Primaraucaria.  After careful examination, he discovered that this small collection contained not one, but two distinct species based on reproductive structures.  One species (figs. A-C below) had a unisexual female inflorescence that outwardly resembles the heads of Corynaea, Lathrophytum, and Ombrophytum of the Balanophoraceae, but differed internally.  The second species (fig. D below) had a bisexual inflorescence with apetallous multicarpellate female flowers comprised of pedicelate ascidiate carpels on an elongate receptacle or axis, and laminar stamens located below the female flowers on the inflorescence axis.  Bock also illustrates what may be the male flowers of the first species, which had elongate bracts below an axis bearing male flowers with perianth elements.

Four specimens with labels (A, C, and D also have impressions/compressions of Macrotaeniopteris leaves).

Primar15d.jpg (133919 bytes)

Above specimens from the Bock collection at the Philadelphia Museum of Natural History.

Below from Bock (1969: 313, figs. 534 and 541), showing both female (left) and male (right) inflorescences that may belong to the same species.  A possible second female head can be seen in the lower right corner of figure 534, implying that multiple heads-inflorescences were produced in close proximity to one another.

Bock03b.jpg (149043 bytes)

Another more complete specimen of the male inflorescence on the right (fig. 541) is shown below (Bock, 1969: figure 536) so that the subtending whorl of elongate bracts can be seen (cf. Langsdorffia).

fig536.jpg (20439 bytes)

Plate 9 and caption from Cornet (1986).

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Plate 9, figs. a-i. Zamiostrobus virginiensis Fontaine 1883 or Primaraucaria wielandii Bock 1954 sensu lato, Productive Coal Measures, Richmond Basin, VA. -a. TYPE A fruiting structure, ANSP #200220C (3953). Impression of fruiting head with spiral phyllotaxis of megasporophyll subunits, each showing folded impression of a subtending bract (b2) and an apical scar (st) to a stigma-like process; scale in mm. -b. TYPE A fruiting structure, ANSP #200221 (3961). Compression of a fruiting head (mss) terminating a long reproductive axis, possessing numerous spirally arranged bract-shaped leaves (b1); * indicates position of portion of compression removed for study (see figure 9a for a reconstruction); scale to right in mm: x 2. -c. TYPE A fruiting structure: Paired cuticles of subtending bract from specimen in fig. b (*); x 1,250. -d. TYPE A fruiting structure: Main axis and base to one carpel-like megasporophyll subunit (ms), showing diverging secondary branches (ax2) and possible base to subtending bract (b2?); from * in fig. b (see figure 109); x 3.5. -e. TYPE A fruiting structure: Aborted, 250 um wide, anatropous ovule attached to cuticle of ovary wall; from * in fig. b; x 112. -f. TYPE A fruiting structure: Immature, 2.6 mm long seed removed from an ovary, showing micropyle (mi) adjacent to hilum (hi) and strongly recurved embryo body; from * in fig. b; x 20. -g. TYPE A fruiting structure: Nearly mature, 2.8 mm long seed with a thick wrinkled seed coat, showing only two small pits or depressions at one end and no functional micropyle or obvious hilum scar; from * in fig. b; x 18. -h. TYPE B fruiting structure, ANSP #200220A (3962). Compression of a fruiting head composed of numerous pedicellate carpel-like megasporophyll subunits (ms), collectively subtended by large latrorse laminar stamens (lls); see figures 9b and 10h); scale to left in mm: x 2. -i. TYPE B fruiting structure: Distal end of a megasporophyll in fig. h, showing pore-like opening (st) that may represent the base to a deciduous stigma; x 16.6.

Primaraucaria_spp.jpg (49011 bytes)

Figure 9. a-c. Zamiostrobus virginiensis Fontaine 1883 or Primaraucaria wielandii Bock 1954 sensu lato. Reconstructions of three different types of fruiting heads  and reproductive structures illustrated by Bock (1969) under P. wielandii. -a. TYPE A. -b. TYPE B. -c. TYPE C. See text for further descriptions; scale in cm: x 2. (http://www.sunstar-solutions.com/sunstar/evoltheo/slewisii.htm)


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[8.16.13-16]


Primaraucaria wielandii Bock

See Bock (1969), pages 309-333 at www.sunstar-solutions.com/sunstar/Primarau/Bockindex.htm.

Habit  Fleshy, non-woody (no coalified core as occurs in woody plant compressions), typically found as inflorescence axes with scale bracts terminating in an inflorescence head.

Parasitism  One specimen of an inforescence axis attached to a portion of a tuber - illustrated in Bock (1969: fig. 530).
fig530.jpg (12650 bytes)

Roots  No evidence of roots found or recognized, even though this plant could not have been transported far from where it grew due to its size and shape, and its association with so many large intact Macrotaeniopteris leaves.

Stem  Absent (aerial portions technically part of an inflorescence) based on the fact that attached leaves are largely devoid of stomata, implying a lack of photosynthesis.  One 2.4 cm wide scaly axis was found by Bock (1969: fig. 529) showing a termination without a reproductive structure.  That termination is similar to an immature inflorescence axis of the Balanophoraceae (see Mystropetalon thomii on Nickrent's website) in the process of pushing itself up through the soil before developing a fertile head.
fig529.jpg (8089 bytes)For comparison see an immature inflorescence of Scybalium jamaicense.

Because some axes found by Bock were as long as 14 cm (e.g. his figure 528), he assumed they were fallen branches from a tree.  The scaly axis of Scybalium depressum, for example, grew to 9 cm in length before terminating in a reproductive head.  Some axes of Helosis cayennensis can grow to 10 cm before terminating in a reproductive head.

Leaves  Large, scaly, easily folded or wrinkled, with rare stomata, spirally arranged.  Stomatal structure variable, commonly closed or occluded - nonfunctional. Epidermal hairs reduced or vestigial.
Primar08c.jpg (15520 bytes)Primar09c.jpg (20219 bytes)Primar07c.jpg (15409 bytes)

Inflorescence, floral, fruit, and seed morphology  No evidence of vegetative stems. Inflorescence-bearing axes appear to arise directly from a tuber (see figure 530 above). Axes subtended by large, wide, scaly, flat (as in adnate) bracts.  In male inflorescences a secondary perianth-like development of bracts present below the fertile portion of inflorescence axis - may have functioned as bud scales.

Perianth  Present only in male flowers, 1-2? (lobed); isomerous with and joined to anthers.

Androecium  The number of stamens and petals cannot be accurately determined from Bock's (1969) illustrations, but they appear to be few.  One, possibly two petals can be detected; they conceal the stamens. Bock points out an exposed anther in figure 541c above.  Based on rare pollen found clining to outer carpel cutile, pollen grains are simple monosulcate.

Gynoecium  Unicarpellate. Carpels pedicellate with a swelling or node where pedicel joins carpel, which may have been the attachment point for vestigial perianth parts (see Plate 9 above and image below).  Style and stigma apparently dehiscent at maturity or lost during fossilization, leaving behind a circular aperture at apex of carpel. Carpels 3-4 mm wide, about 9-10 mm long; length of pedicels could not be determined.
Primarcpl2.jpg (29984 bytes)

Ovules 3-4 per locule; pendulous; without integuments; ovule cutile continuous with inner carpel cuticle.
Primar10b.jpg (14672 bytes)

Suggested restoration of pedicellate carpels showing pendulous seeds.
Primarill.JPG (47934 bytes)

Plant sex  Unknown, could be monoecious or dioecious.

Flowers  Unisexual, female naked (possibly reduced monochlamydous).

Fruit  Probably non-fleshy; indehiscent; a compound multiple fruit, like a pineapple. Individual carpels contain 2-3 seeds.  Seeds without testa; only a thickened fleshy cuticle present.  Embryo apparently rudimentary at the time of seed release based on condition found in fruit.  Thin sections through compression fossil show seeds within multiple cuticles of carpels.
Primarslc.JPG (178916 bytes)

Seedling  Germination type unknown — cotyledons apparently lacking as in the Balanophoraceae.

Germinating seed of Dactylanthus taylorii (Balanophoraceae) shown next to a seed of Primaraucaria (right - 2.8 mm)
Dactylseedling.jpg (12953 bytes)Primar04d.jpg (9448 bytes)

Image on left source (Nickrent, 2003): http://www.science.siu.edu/parasitic-plants/Balanophoraceae/

Primaraucaria species 2

The second species is based on only one specimen of a reproductive structure (see labelled figure D above or enlargement below).

Inflorescence and floral morphology  This species differs from P. wielandii in that both male and female reproductive structures are present on the same inflorescence.  Either the inflorescence axis branches (compound inflorescnece), with the secondary branches each bearing numerous unicarpellate flowers, or the flowers are multicarpellate, with pedicellate carpels loosely arranged along an elongate receptacle (depicted as a peltate bract in Sarcophyte sanguinea, Lophophytum mirabile and L. leandri, and Lathrophytum peckoltii).  At least 10 carpels per flower.  Laminar latrorse stamens subtend the ovuliferous part of the inflorescence (based on position and orientation).
Psp2.jpg (68277 bytes)

Flowers  Unisexual, dioecious.

Perianth  Absent or unknown if independent of anthers.

Androecium  At least three laminar stamens preserved on the one specimen on one side of the inflorescence. Anthers elongate, one on each margin of tepaloid lamina; dehiscence slit longitudinal; indications of single chamber at maturity.  Pollen is still present inside the anthers, and awaits extraction, preparation, and study.
lamstamen.jpg (5596 bytes)

Gynoecium  Apocarpous. Carpels pedicellate with a circular aperture at the apex of the carpel.  If existed, the style and stigma apparently dehiscent at maturity or were lost during fossilization. Carpels elliptical in shape; 1 cm long, 5-6 mm wide; pedicels about 1 cm long.  No seeds could be detected within carpels, and no attempt to remove and macerate a specimen was attempted.  Based on morphology and size, the carpels are similar in construction to P. wielandii, and therefore probably contained multiple ovules/seeds.

Triassiflorites grandiflora Bock

    In addition to Primaraucaria, Bock (1969) describes another fossil preserved only as an inflorescence.  Bock relates that over many years of collecting, he was able to recover 12 complete inflorescences of this species and 30 additional fragments.  He was convinced that the close association with Macrotaeniopteris leaves indicated an affinity with that plant, even though Primaraucaria was also intimately associated with Macrotaeniopteris leaves (see above).  As with Primaraucaria, he interpreted Triassiflorites as a gymnosperm, but in this case as a member of the Cycadales.  Strangely, he described the reproductive organs as "flowers" with perianth parts. 

    A close examination of the pictures provided by Bock (1969: 265), however, raise doubts as to its cycadalean affinity.  Instead his pictures reveal remarkable similarities with the Balanophoraceae genus Lophophyton.  Both the anthers and carpels compare remarkably well in size and shape to those illustrated for Lophophyton (see above).  The only significant differences that can be detected are 1) the female secondary branches on a compound bisexual inflorescence retained perianth parts (see Bock, 1969: 273), whereas in Lophophyton they do not, 2) the male secondary branches were longer than those of Lophophyton, and contained many more anthers (naked male flowers), and 3) there may have been more variation in the distribution or number of male and female secondary branches per inflorescence, with some described as being mostly male while others had male and female flowers mixed on the same secondary branch. This is intuitively possible because female flowers were not naked (as in Lophophyton), but were shielded from self-pollination by perianth parts.

    Preservation (or the quality of his illustrations) is not good enough to determine if Bock's interpretation of more than one female flower per secondary branch is correct, or is the result of compaction and distortion of the inflorescence during burial.  Even though Bock distinguished between sterile bracts subtending fertile secondary branches, overlap led him to think that the thousands of biloculate anthers per branch were instead attached to the bracts.  And yet in some of his photographs and reconstructions he provides evidence for their separation and distinction.  In addition, Bock's reconstruction (Fig. 450 below) shows neatly arranged "sporangia" on the anthers, but a close examination of his photographs shows random "bumps", which might instead be remnant pollen grains inside pollen sacs.  Compare Bock's photographic plates below with illustrations of Lophophyton above:

Triassifl03b.jpg (124946 bytes)

From Bock (1969: 271).

Triassifl02b.jpg (173340 bytes)

From Bock (1969: 269).

Discussion with Comparison

   The name Primaraucaria may conflict with some botanists' sensibilities, while giving others who have ulterior motives a reason to reject it as a pre-Cretaceous angiosperm.  There are many examples in paleobotanical and palynological literature of incorrect names applied to new fossils, because the author(s) made incorrect comparisons based on inadequate information.  Early Mesozoic polyplicate pollen possibly belonging to angiosperm ancestors (i.e. stem group angiophytes) were originally thought to be the spores of horsetails; the generic name given to these morphotypes was Equisetosporites.  That epithet must be used even though such palynomorphs are now known to be pollen grains.  The rules of botanical nomenclature were set up for such cases to conserve those names in order to protect the discoverer(s) or author(s) of new species.

    The description of fossils is subject to more interpretation than descriptions of living organisms, which are complete and undegraded.  Being able to associate all preserved organs of fossil plants with one taxon is sometimes difficult if not impossible without organic connection.  In the case of Primaraucaria there are enough specimens in organic connection to allow a reasonable interpretation of this plant, partly because its morphology is so unique in the fossil record.  Hopefully, the evidence given here will be evaluated based on its merits, and not on how well it fits with popular concepts of angiosperm evolution.

For this comparison with the Balanophoraceae, two possible interpretations for the female flowers are considered:

  1. Naked unicarpellate flowers grouped together around a secondary (paniculate) inflorescence axis (e.g. Lothophytum) or bract axis, where bracts are distally expanded to form a peltate head (e.g. Lathrophytum and Ombrophytum).

  2. Apetallous multicarpellate (apocarpous) flowers with an elongate receptacle, which may or may not expand distally to form a peltate head; flowers attached directly to main axis of inflorescence (spike).

In this treatment, the second interpretation is adopted for the following reasons:

Comparison Between Extant Balanophoraceae and Fossil Taxa
extant extant extant Triassic Triassic Triassic
Langsdorffia
hypogaea
Lathrophytum
peckoltii
Lophophytum
mirabile
Primaraucaria
wielandii
Primaraucaria
sp 2
Triassiflorites
grandiflora
inflorescence
unisexual
inflorescence
bisexual,
female flowers located below male flowers
inflorescence
bisexual,
female flowers located below male flowers
inflorescence unisexual inflorescence
bisexual,
female flowers located above male flowers
inflorescence
bisexual,
female flowers located below male flowers
female flowers unicarpellate,
carpels sessile,
no receptacle,
without perianth,
crowded to form dense head,
no bracts
female flowers multicarpellate,
carpels sessile,
on long receptacle,
without perianth,
end of receptacle expanded - peltate,
no bracts
female flowers multicarpellate,
carpels sessile,
on long receptacle,
without perianth,
positioned in axils of primary bracts
female flowers
unicarpellate,
carpels stalked,
no receptacle,
without perianth,
crowded to form
dense head,
no bracts
female flowers multicarpellate,
carpels stalked,
on long receptacle,
without perianth,
end of receptacle not expanded,
no bracts
female flowers
multicarpellate,
carpels sessile,
on long receptacle,
with perianth,
positioned in axils of primary bracts
male flowers
monoclamydous,
2-3 bracts,
long pedicels,
inflorescence subtended by elongate bracts
male flowers
without perianth,
short pedicels,
crowded to form
dense head
male flowers
without perianth,
anthers elongate,
crowded on catkin-like secondary branch
cf. Hedyosmum
male flowers
monoclamydous,
2-3? bracts,
short pedicels, inflorescence subtended by elongate bracts
male flowers
without perianth,
laminar pedicels,
anthers latrorse and embedded in lamina
male flowers
without perianth,
anthers elongate,
crowded on catkin-like secondary branch
cf. Hedyosmum
scale-like leaves
on lower female
inflorescence axis
peltate bracts
on lower
inflorescence axis
elongate bracts
on lower
inflorescence axis
scale-like leaves
on lower female
inflorescence axis
unknown elongate bracts
on lower
inflorescence axis
wet tropical wet tropical wet tropical wet tropical wet tropical wet tropical

    Based on the above comparisons, taking into consideration preservation and missing data, Primaraucaria and Triassiflorites can be favorably compared to the Balanophoraceae.  The existence of trisulcate and pentasulcate aperture types within the Balanophoraceae (Watson and Dallwitz,1992-2000: website) may be a genetic throwback (reversal) to ancestral Crinopolles trisulcate and pentasulcate pollen found in the same strata as Primaraucaria and Triassiflorites.

    Hickey and Doyle (1977: Fig. 65), in their monographic paper on Early-Mid Cretaceous angiosperm leaf evolution, proposed a reduction in leaf size and complexity between an ancestral gymospermous condition (e.g. pteridosperm or cycadopsid) and secondary expansion at the beginning of dicot leaf evolution in the Cretaceous.  However, they proposed a hypothetical xeromorphic intermediate leaf-type during that transformation.  More recently the phylogenetic mapping of functional traits reveals that the basal lineages, Amborella, Austrobaileyales, and some Chloranthaceae, share ecological and physiological traits linked to shady, disturbed, and possibly wet habitats (Feild et al., 2003a; Feild et al., 2003b).  All fossils of possible pre-Cretaceous angiosperms have been found in wet sedimentary facies (habitats) ranging from the margins of freshwater (non-alkaline) lakes and oxbow lakes to coal swamps (Tidwell et al., 1977; Cornet and Traverse, 1975; Cornet,1986; 1989a; 1989b; 1993b; 1996; Cornet and Olsen, 1990; Cornet and Habit, 1992, Hochuli and Feist-Burkhardt, 2004, Kirkland et al., 2002; and Sun et al., 1998; 2002), making it more likely that angiosperms first evolved in a wet habitat rather than a dry one.

    The ecology and physiology of Austrobaileya scandens, for example, is different from earlier hypotheses that the earliest angiosperms were early-successional xeric shrubs, disturbance-loving herbs characterized by high capacity for photosynthesis and water transport, or were aquatic herbs (Feild et al., 2003b).  Instead, basal lineages possess functional characteristics commonly associated with seed plants and ferns adapted to low light, including absence of palisades mesophyll tissue, low leaf photosynthetic rates, and possibly strong reliance on vegetative reproduction for survival (Feild et al., 2003b), which could favor the evolution of parasitism.  Holoparasites are considered highly derived, genetically reduced members of angiosperms with normal genomes (Nickrent, 2002).  They also represent an extreme end member in low light survival, having lost the capability to photosynthesize, opting instead for deriving their energy from other plants.  At least eight families derived from core eudicots and two families from pre-eudicots have semi- and holoparasite members: Lauraceae and Hydnoraceae (magnoliids), Santalales (six families), Balanophoraceae, Cynomoriaceae, Krameriaceae, Rafflesiales (four families), Lennoaceae, Cuscutaceae, and Orobanchaceae (Nickrent, 2002). 

    Although Nickrent (pers. comm., 2004) does not think an angiosperm parasite, once it has lost the genetic ability to photosynthesize, could ever regain that ability (without  intergeneric or interfamily hybridization with a photosynthetic relative: cf. Kellogg and Bennetzen, 2004), other non-parasitic members of the same family or order could have many of the same reproductive characteristics as the parasites.  The existence of those plants or ancestors is implied by the existence of a parasitic seed plant in a wet tropical rain forest.  Because angiosperms have a propensity for evolving parasitic members, even in near basal branches of their phylogenetic tree, it should not be surprising that basal parasitic angiosperms could exist.  Because of their unique habit (i.e. root parasites probably on cycadophytes, gingkophytes, seed ferns, and/or tree ferns, all with giant fronds and leaves: Macrotaeniopteris, Eogingkoites, Taeniopteris, Sphenobaera, Stangerites, etc., which make up the dominant vegetation in sedimentary layers containing Primauraucaria - Cornet and Olsen, 1990; Axsmith et al., 1995), wet habitat (i.e. tropical and subtropical rain forests and swamps), and tropical distribution, their fossil record would be sparce and limited to geologic facies that could preserve them in paleoequatorial regions, such as those found in the Richmond rift basin of Virginia.

    Molecular data indicate that the Balanophoraceae do not represent the phylogenetic root stock of angiosperms (Nickrent, 2002), but probably arose in the nebulous group of angiosperms called "eudicots", which are thought to have first appeared in the Early Cretaceous (Nickrent, pers. comm. 2004).  It is more likely that similarities between the Triassic fossils and some Balanophoraceae are due to convergence rather than to familiar affinity.  It is important to recognize that verification of Sanmiguelia, Primaraucaria, and/or Triassiflorites as crown-group (rather than stem group) angiosperms would not mean that the most current phylogenetic trees based on taxonomic and molecular data are necessarily incorrect (e.g. Fig. 7 in Doyle and Endress, 2000).  It would instead mean that the basal stem branches to the crown groups diverged prior to the Cretaceous and perhaps as early as the Ladinian or Carnian (228-233 mya). 

    Wikström et al. (2001: molecular data) give a conservative age for the origin of angiosperms as Middle Jurassic.  Sanderson and Doyle (2001) also give a Middle Jurassic age (180 mya ± 30 my) based on 18S rDNA data, but show that for 1-2nd rbcL positions the age is basal Jurassic (200 mya ± 40 my).  However, Martin et al. (1992) give an estimated age of 300 mya ± 40 my based on cloned and sequenced cDNAs. Wolfe et al. (1989: molecular data) give a maximum possible age for the monocot-dicot divergence as early Late Triassic (230 mya), consistent with Sanmiguelia (early Norian) in the Chinle Formation and the Crinopolles Group of distinctive angiosperm-like pollen in the Carnian that combines monocot and dicot pollen characteristics.  If the discovery of a water-lily-like leaf (cf. Nuphar) in basal Jurassic lacustrine strata of Utah is that of an angiosperm, the age for origin would be no younger than Late Triassic.  Molecular data has consistently excluded (falsified) the Cretaceous as the time of angiosperm origin.  These estimates are based on an average mutation rate, but rapid evolution during punctuated equilibria indicates that mutation rates may vary considerably depending on the type of genetic alteration.

Conclusion

    As more and more evidence for basal angiosperms has emerged in molecular and paleobotanical fields, the origin of angiosperms has been pushed further back in time from Early Cretaceous to Late Jurassic, then to Middle Jurassic, and now to Early Jurassic, with indications that the age for angiosperm origin might ultimately reach back to the Middle Triassic (Hochuli and Feist-Burkhardt, 2004).  Parasitic plants exist outside the Angiospermae, but they are rare.  For example, Cryptothallus mirabilis is the only parasitic liverwort, while Parasitaxus ustus (Podocaraceae) is the only parasitic conifer.  Neither resembles Primaraucaria or any member of the Balanophoraceae.  Parasitaxus is found on New Caledonia, the same island refuge of Amborella.  Consequently, the presence of a possible basal parasitic angiosperm in the Carnian (early Late Triassic) is not surprising because 1) angiosperms are now thought to have initially evolved in dark (understory) wet habitats rather than in bright dry ones, and 2) the taxonomic distribution of parasitic angiosperms indicates a higher potential for parasitism in angiosperms than in gymnosperms or cryptogams, with 10 parasitic families ranging from pre-eudicots (magnoliids) to asterids (Nickrent, 2002).  The existence of Primaraucaria  implies that non-parasitic relatives also must have existed then in or near the Richmond basin coal swamps.   This interpretation is supported by diverse multiaperturate angiosperm-like pollen found in the same strata (Crinopolles Group: Cornet, 1989a).

References

Arber, A., 1961. Monocotyledons, a morphological study. Reprinted by J. Cramer of Weinheim, Wheldon & Wesley, LTD. and Hafner Publishing Co., New York, 258 p.

Axsmith, B.J., Taylor, T.N., Delevoryas, T., Hope, R.C., 1995. A new species of Eoginkgoites from the Upper Triassic of North Carolina, USA. Rev. Paleobot. Palynol. 85(3): 189-198.

Bock, W, 1969. The American Triassic Flora and Global Distribution. Geological Center, North Wales, Pennsylvania, Research Series. v. 3 & 4: 406 p.

Cornet, B., 1977. The palynostratigraphy and age of the Newark Supergroup. unpublished Ph.D. thesis, The Pennsylvania State University, 505 p.

Cornet, B., 1986. The reproductive structures and leaf venation of a Late Triasic angiosperm, Sanmiguelia lewisii. Evol. Theory 7: 231-309.

Cornet, B., 1989a. Late Triasic angiosperm-like pollen from the Richmond rift basin of Virginia, USA. Palaeontogr. Abt. B 213: 37-87.

Cornet, B., 1989b. The reproductive morphology and biology of Sanmiguelia lewisii, and its bearing on angiosperm evolution in the Late Triassic. Evol. Trends in Plants 3: 25-51.

Cornet, B. and Olsen, P.E., 1990. Early to middle Carnian (Triassic) flora and fauna of the Richmond and Taylorsville basins, Virginia and Maryland, U.S.A. Guidebook No. 1, Virginia Museum of Natural History, Martinsville, VA. 87 p.

Cornet, B., 1993a. Applications and limitations of palynology in age, climatic, and paleoenvironmental analyzes of Triassic sequences in North America. In Lucas, S.G. and Morales, M. (eds.), The Nonmarine Triassic. New Mexico Museum of Natural History & Science Bulletin No. 3: 75-83.

Cornet, B., 1993b. Dicot-like leaf and flowers from the Late Triassic tropical Newark Supergroup rift zone, U.S.A. Mod. Geol. 19: 81-99.

Cornet, B., 1996. A new gnetophyte from the Late Carnian (Late Triassic) of Texas and its bearing on the origin of the angiosperm carpel and stamen. In Taylor, D.W. and Hickey, L.J. (eds.), Flowering Plant Origin, Evolution & Phylogeny. Chapter 3: 32-67. Chapman & Hall, New York.

Cornet, B. and Olsen, P.E., 1990. Early to Middle Carnian (Triassic) flora and fauna of the Richmond and Taylorsville basins, Virginia and Maryland, U.S.A. Virginia Museum of Natural History, Guidebook No. 1, Martinsville, VA.

Cornet, B., and Habib, D., 1992. Angosperm-like pollen from the ammonite-dated Oxfordian (Upper Jurassic) of France. Rev. Palaeobot. Palynol. 71: 269-294.

Cornet, B., and Traverse, A., 1975. Palynological contributions to the chronology and stratigraphy of the Hartford basin in Connecticut and Massachusetts. Geoscience and Man, XI: 1-33.

Donoghue, M.J. and Doyle, J.A., 2000. Seed plant phylogeny: Demise of the anthophyte hypothesis? Current Biology, 10: R106-R109.

Doyle, J.A., 2001. Significance of molecular phylogenetic analyses for paleobotanical investigations on the origin of angiosperms. Palaeobotanist 50: 167-188.

Doyle, J.A. and Donoghue, M.J., 1993. Phylogenies and angiosperm diversification. Paleobiology 19(2): 141-167.

Doyle, J.A. and Endress, P.K., 2000. Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int. J. Plant Sci. 161(6 Suppl.): 5121-5153.

Endress, P.K., 1987. The Chloranthaceae: reproductive structures and phylogenetic position. Bot. Jahrb. Syst., 109(2): 153-226.

Feild, T.S., Arens, N.C., and Dawson, T.E., 2003a. The ancestral ecology of angiosperms: emerging perspectives from extant basal lineages. Int. J. Plant Sci. 164(3 Suppl.):S129-S142.

Feild, T.S., Franks, P.J., and Sage, T.L., 2003b. Ecophysiological shade adaptation in the basal angiosperm, Austrobaileya scandens (Austrobaileyaceae). Int. J. Plant Sci. 164(2): 313-324.

Hickey, L.J. and Doyle, J.A., 1977. Early Cretaceous fossil evidence for angiosperm evolution. Bot. Rev. 43: 3-104.

Hochuli, P. and Feist-Burkhardt, S., 2004. A boreal early cradle of Angiosperms? Angiosperm-like pollen from the Middle Triassic of the Barents Sea (Norway). J. Micropalaeontol. 23(2): 97-104.

Kellogg, E.A. and Bennetzen, J.L., 2004. The evolution of nuclear genome structure in seed plants. Amer. J. Bot. 91(10): 1709-1725.

Kent, D.V. and Olsen, P.E., 2000. Implications of astronomical climate cycles to the chronology of the Triassic. Zbl. Geol. Paläont. I: 1463-1473.

Kirkland, J.I., Lockley, M., and Milner, A.R., 2002. The St. George Dinosaur Tracksite. Survey Notes, Utah Geological Survey, 34(3): 4-5. http://geology.utah.gov/surveynotes/snt34-3.pdf

Martin, W., Gieri, A. and Saedler, H., 1989. Molecular evidence for pre-Cretaceous angiosperm origins. Nature 339(4 May): 46-48.

Martin, W., Lydiate, D., Brinkmann, H., Forkmann, G., Saedler, H., and Cerff, R., 1993. Molecular Phylogenies in Angiosperm Evolution. Mol. Biol. Evol. 10(1): 140-162.

Nickrent, D. L. 2002. Phylogenetic Origins of Parasitic Plants. Chapter 3, pp. 29-56 In J. A. López-Sáez, P. Catalán and L. Sáez [eds.], Parasitic Plants of the Iberian Peninsula and Balearic Islands. Mundi-Prensa, Madrid.

Olsen, P.E. and Kent, D.V., 2000. High-resolution early Mesozoic Pangean climatic transect in lacustrine environments. Zbl. Geol. Paläont. I: 1475-1495.

Olsen, P.E., Kent, D.V., Cornet, B., Witte, W.K., and Schlische, R.W., 1996. High-resolution stratigraphy of the Newark rift basin (early Mesozoic, eastern North America. GSA Bulletin 108: 40-77.

Sanderson, M.J. and Doyle, J.A., 2001. Sources of error and confidence intervals in estimating the age of angiosperms from rbcL and 18S rDNA data. Amer. J. Bot. 88(8): 1499-1516.

Sun, G., Dilcher, D.L., Zheng, Z., and Zhou, Z., 1998. In Search of the First Flower: A Jurassic Angiosperm, Archaefructus, from Northeast China. Science 282: 1692-1695.

Sun, G., Qiang, J., Dilcher, D.L., Zheng, S., Nixon, K.C., and Wang, X., 2002. Archaefructaceae, a new basal angiosperm family. Science 296: 899-904.

Tidwell, W.D., Simper, A.D., and Thayn, G.F., 1977. Additional information concerning the controversial Triassic plant: Sanmiguelia. Palaeontogr. Abt. B 163: 143-151.

Winter, K.U., Becher, A., Münster, T., Kim, J.T., Saedler, H., and Thiessen, G., 1999. MADS-box genes reveal that gnetophytes are more closely related to conifers than to flowering plants. Proc. Natl. Acad. Sci. USA 96: 7342-7347.

Wikström, N., V. Savolainen, and M. Chase, 2001. Evolution of the angiosperms: calibrating the family tree. Proceedings of the Royal Society of London Series B-Biological Sciences 268: 2211-2220.

Wolfe, K.H., M. Gouy, Y.-W. Yang, P.M. Sharp & W.-H. Li., 1989. Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc. Natl. Acad. Sci. U.S.A. 86: 6201-6205.

Glossary

Monochlamydous   Referring to a flower that has only one perianth whorl (the calyx).


This page was created on 13 July 2003; it was last updated on 08/16/2013
© 2003 Bruce Cornet

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