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First published online December 19, 2008; doi:10.3732/ajb.0800202 American Journal of Botany 96: 237-251 (2009) © 2009 Botanical Society of America, Inc. |
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Special Invited Papers |
Department of Ecology and Evolutionary Biology, and Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045-7534 USA
Received for publication 19 June 2008. Accepted for publication 27 October 2008.
ABSTRACT
Five orders of late Paleozoic–Mesozoic seed ferns have, at one time or another, figured in discussions on the origin of angiosperms, even before the application of phylogenetic systematics. These are the Glossopteridales, Peltaspermales, Corystospermales, Caytoniales, and Petriellales. Although vegetative features have been used to suggest homologies, most discussion has focused on ovulate structures, which are generally interpreted as megasporophylls bearing seeds, with the seeds partially to almost completely enclosed by the megasporophyll (or cupule). Here we discuss current information about the reproductive parts of these plants. Since most specimens are impression-compression remains, homologizing the ovulate organs, deriving angiospermous homologues, and defining synapomorphies remain somewhat speculative. Although new specimens have increased the known diversity in these groups, a reconstruction of an entire plant is available only for the corystosperms, and thus hypotheses about phylogenetic position are of limited value. We conclude that, in the case of these seed plants, phylogenetic analysis techniques have surpassed the hard data needed to formulate meaningful phylogenetic hypotheses. Speculation on angiosperm origins and transitional stages in these fossils provides for interesting discussion, but currently it is still speculation, as the role of these groups in the origin of angiospermy continues to be cloaked in Darwin’s mystery.
Key Words: angiosperm ancestors • caytonialeans • corystosperms • fossil plants • glossopterids • Mesozoic • peltasperms • Permian • seed plant phylogeny
The Permian glossopterids, along with the three major groups of late Paleozoic–Mesozoic seed ferns (peltasperms, corystosperms, caytonialeans), all represent gymnosperms that have historically figured prominently in discussions on the origin of angiosperms (e.g., Krassilov, 1977b
). The Glossopteridales are considered to represent a monophyletic group, and all members have similar foliage, i.e., Glossopteris Brongniart and Gangamopteris McCoy, although more recent work suggests some diversity in reproductive organs (e.g., Taylor et al., 2007; Prevec et al., 2008). They represent the dominant elements in Permian floras from the supercontinent of Gondwana (including Antarctica, Australia-New Zealand, parts of Africa and South America, and peninsular India) and appear to have gone extinct around the Permo–Triassic boundary (McManus et al., 2002). The other, post-Carboniferous seed ferns, however, were widespread from the Permian to the Cretaceous, and unlike the Carboniferous forms, appear to have few morphological characters in common. Rather, they are included as a collection of either orders or families in which the relationships among the various taxa are uncertain (Taylor et al., 2006). In most seed plant phylogenies, each of these groups is included as a single terminal branch, often a composite terminal. Although a few of these seed plants are known from anatomically preserved specimens, most are represented by impression and compression fossils and therefore are not understood with the same degree of resolution as the late Paleozoic pteridosperms, many of which are understood, at least in part, in anatomical detail. Nevertheless, some of these "younger" seed ferns possess morphological features that have been used to suggest affinities with some of the Paleozoic seed ferns (Petriella, 1981). As research has continued, our knowledge of the diversity within some of these groups has increased, which often makes it difficult to define the group according to its original concept. Nevertheless, this additional diversity needs to be accommodated in seed plant phylogenies.
Historically, and for obvious reasons, many of these gymnosperms have been the subject of considerable interest as potential angiosperm progenitors. These assumptions have been based on a number of features, most notably the enclosure of the ovules in some type of leaflike structure that has generally been termed a cupule. In the sections that follow, we provide a discussion of several seed fern groups and offer our perspective on the relationships of these fossil groups and possible homologies with the angiosperms.
The general concept of the seed ferns was proposed by Oliver and Scott (1904) for Paleozoic (Carboniferous) plants that possessed fernlike foliage, but with seeds and pollen sacs, rather than sporangia, attached to the leaves. The initial concept of the Pteridospermae was based on structurally preserved organs of the Carboniferous lyginopterids, but was subsequently expanded to other Carboniferous–Permian orders, and today also includes the late Paleozoic Glossopteridales. In Mesozoic rocks, four groups have been delimited. One of these, the Corystospermales (Upper Permian–Cretaceous), is known in some detail, based on permineralized and compression fossils from several continents. The Peltaspermales (Pennsylvanian–Triassic) and the Caytoniales (Triassic–Cretaceous) are known only from impression and compression specimens; both structurally preserved and compressed fossils have been assigned to the Petriellales (Triassic). Although foliage and other vegetative parts of these seed plants are known, we have limited the discussion that follows to the reproductive parts of these plants because they have served as the focal point in discussions linking them to the flowering plants.
GLOSSOPTERIDALES
There is a considerable body of literature on the Glossopteridales, beginning with the description of the vegetative leaf Glossopteris by Adolphe Brongniart in 1828. Today, the group is known from stem, root, and leaf genera (Fig. 1), that are preserved in a variety of modes. The reproductive organs of the glossopterids, however, have remained a continuing source of controversy since the first report of "linear sori" on some Glossopteris leaves (Feistmantel, 1886).
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), with additional ones continually being reported or reexamined (e.g., Adendorff, 2005; Prevec et al., 2008). A few reproductive organs have been found attached to the parent plant in association with vegetative leaves (Fig. 2) (e.g., Pant and Singh, 1974). Other reproductive organs are attributed to the group based on venation patterns of the megasporophyll that are similar to those of the vegetative leaves and on co-occurrence at the same locality. One of the major obstacles in the interpretation of glossopterid reproductive organs has been the fact that most are preserved as impression-compression (e.g., Fig. 3) or mold-cast specimens and thus, interpreting the homology of these organs has been controversial. In attempting to document diversity, some authors have used an artificial system of morphofamilies based on macromorphological features (e.g., Arberiaceae, Dictyopteridiaceae, Lidgettoniaceae, Rigbyaceae) to classify and categorize these structures (see Adendorff, 2005, for a history of glossopterid classification). Others have used different names for higher-level taxonomy in the mistaken belief that families of fossil plants should be named after an ovulate organ rather than the oldest validly published genus in the group.
Plumstead (1956) initially described the ovulate fructifications of the glossopterids and thus demonstrated that they were gymnosperms and not ferns. She erected the genus Hirsutum Plumstead for shield-shaped, "bivalvate" structures that she interpreted as bisexual (Plumstead, 1956, 1958). Plumstead suggested that the fructifications produced hairlike, pollen-producing organs on one of the two valves. She also interpreted flat, bractlike structures in Scutum Plumstead (Fig. 4) as pollen bearing (for details, see Prevec et al., 2008). Thus far, no glossopterid reproductive organs have been conclusively demonstrated as containing both pollen and seeds (Pant, 1987). Despite the numerous ovulate structures attributed to the glossopterids, many represent variations on a basic theme. These consist of a megasporophyll bearing seeds; the megasporophyll has been variously termed a capitulum, cupule, fertiliger, or cladode. In instances where the reproductive structure is attached to the parent plant, it appears in an axillary position (e.g., Holmes, 1987) or fused or adpressed to the petiole or lamina of a Glossopteris leaf.
Perhaps the most important discovery contributing to understanding the homology of the glossopterid ovulate reproductive organs is the report of Gould and Delevoryas (1977) of anatomically preserved Glossopteris megasporophylls with attached ovules (Fig. 5). Although the megasporophylls were not found organically attached to axes or leaves, anatomical similarities between of the megasporophylls and vegetative leaves of Glossopteris suggest that they were borne on the same plant (see Nishida et al., 2007). Attached to one surface of the fleshy megasporophyll are numerous ovoid seeds with the edges of the megasporophyll slightly enrolled and partially covering the seeds. Now named Homevaleia gouldii Nishida et al. (2007), the megasporophyll lacks the sclerenchymatous hypodermal fibers found in the vegetative leaf of G. homevalensis. Each orthotropous ovule is 1.2–1.3 mm long by 0.8–0.9 mm wide and attached by a small stalk to the adaxial surface of the megasporophyll, based on the anatomy. The integument is thickened in the micropylar region, and the outer layer (sarcotesta) extends out from the ovules to form a meshwork of filaments between the seeds. Gould and Delevoryas (1977) suggested that this meshwork may have been involved in some way in directing pollen flow, possibly aided by a pollination droplet. Another suggestion is that perhaps the spongy meshwork served to insulate the ovules in the cool, temperate environment in which this plant lived (Nishida et al., 2007). Many of the ovules contain well-preserved megagametophytes, each with a single archegonium (Fig. 6). Bisaccate pollen of the Protohaploxypinus Samoilovitch type (Fig. 7) has been reported in the pollen chambers of these ovules (Gould and Delevoryas, 1977; Nishida et al., 2004). Especially significant is the report of pollen tubes in various stages of releasing flagellated sperm in the region of the archegonium (Nishida et al., 2003). Sperm are top shaped (Fig. 8), small (
12 µm in diameter), and characterized by spiral bands of dark dots at one end that are interpreted as corresponding to the positions of the basal bodies of numerous flagella aligned along a multilayered structure (MLS). Interestingly, the glossopterid sperm are morphologically like those of cycads and Ginkgo, but much smaller (Nishida et al., 2007). In general organization, the Homevaleia megasporophyll shows some similarities to the impression-compression ovulate structures Dictyopteridium Feistmantel ex Zeiller or Plumsteadia Rigby (Fig. 9), in part based on the arrangement of ovules in the permineralized and compressed forms (Nishida et al., 2007).
Anatomically preserved glossopterid megasporophylls with attached ovules are also known from permineralized peat in the Late Permian Buckley Formation of Antarctica (Taylor and Taylor, 1992; Taylor et al., 2007). One of these is 6.0 mm wide and 1.0 mm thick and is thought to have been produced by the same plant that bore Glossopteris schopfii Pigg (1990a) leaves, based on similar anatomy (Taylor and Taylor, 1992). The seeds are attached to the adaxial surface of the megasporophyll (Fig. 10) (Taylor and Taylor, 1992). This character is based on the position of the tissues that make up the vascular bundles and contrasts with the suggested abaxial attachment of ovules described from impression fossils (Adendorff, 2005).
Another permineralized specimen from the Late Permian of Antarctica shows some similarity to several of the so-called cupulate glossopterid reproductive structures (Surange and Chandra, 1975), such as Arberia White or Rigbya Lacey et al. (Fig. 4). A preliminary analysis suggests that it is a branching structure bearing at least four uniovulate cupules. Each cupule is 3.0 mm long and contains a sessile ovule with two flattened wings extending from the integument. The stalk at the base of the organ contains a C-shaped vascular strand like that produced in some leaves (Taylor et al., 2007).
Dispersed ovules that show details of embryo development have been described from the Antarctic permineralized peat. Although they occur in close association with Glossopteris leaves, none have been found attached. They are considered to represent glossopterid seeds based on the overwhelming dominance of this group in the peat and in nearby floras of comparable age (e.g., Cúneo et al., 1993). Seeds of Plectilospermum Taylor and Taylor are 5.0 mm long and platyspermic with the nucellus and integument attached only at the base (Taylor and Taylor, 1987). Many seeds have a cellular megagametophyte with two archegonia, each showing evidence of a multicellular embryo, confirming the existence of polyembryony (Fig. 11). Development had progressed in some embryos so that the presence of a suspensor could be distinguished (Smoot and Taylor, 1986).
As noted, one of the problems in discussing the ovulate structures in the glossopterids is the use of nonstandard terms to describe their morphology. Schopf (1976) suggested the term fertiliger for the megasporophyll, a designation that Pant (1987) also used. Schopf (1976) proposed that the ovulate complex in the glossopterids represented an axillary shoot and suggested a distant relationship with the cordaites, an idea that was termed the cladode concept by Retallack and Dilcher (1981) . Permineralized reproductive structures that have been described to date, however, clearly indicate that the ovules are borne on the adaxial surface of a megasporophyll, although reconstructions based on impression fossils suggest attachment was abaxial. What remains to be determined is whether the megasporophyll is attached to a reduced and modified axillary branch system or to the base of the subtending vegetative or scale leaf (Pigg and Trivett, 1994). It is also possible that the structures that make up the glossopterid ovulate complex do not involve the same homologies in every case. This hypothesis is further strengthened by the variety of morphologic forms, including those that have multiple ovules (Fig. 12) and those with apparently solitary ovules. Seed morphology is also variable, with both radially and bilaterally symmetrical forms known. The presence or absence of wings on some ovules may be related to dispersal syndromes. Moreover, some glossopterid ovules have only a single archegonium, while in others, two are present. The situation may in part parallel the extraordinary variation demonstrated among the seeds of Paleozoic seed ferns, which were produced on leaves, in cupules, and on naked branching systems. Thus, the glossopterids, despite the evident uniformity of their vegetative organs, apparently represent a rather diverse group of late Paleozoic seed ferns that may ultimately rival the Carboniferous taxa in the variability of their ovulate reproductive structures. Because the group dominated Gondwana for more than 30 Myr, perhaps it is not surprising that the glossopterids are more diverse than their vegetative morphology would suggest. While at least some of the glossopterid ovulate structures are homologous with a megasporophyll, with ovules attached to the adaxial surface, we echo the comments of others who have examined and discussed the glossopterid reproductive structures in noting that additional permineralized specimens will be critical in understanding the homologies of these unusual reproductive organs.
One interesting feature is the apparent absence of any wing-like structure on the megasporophyll in the permineralized specimens, a structure that is commonly found in impression-compression forms (Fig. 4). It is doubtful that the enrolled edges of the megasporophyll of Homevaleia gouldii could create such a structure if compressed. The absence of the wing may reflect a developmental stage of the megasporophyll or a difference in taxa between South Africa and Australia. The presence of this structure on many of the impression specimens suggests that there is some function for the wing. Protection of the developing ovules may be one obvious adaptation. Another might involve dispersal, with the entire megasporophyll being shed as a unit (Adendorff et al., 2002), although this is unlikely because most impression-compression specimens appear to have already shed their seeds. The presence of some dispersed seeds with integumentary wings is also not consistent with the idea of the entire unit being shed.
Pollen organs
Unlike the ovulate organs, there is little variability in the pollen organs of the Glossopteridales. The two most common genera are Glossotheca Surange and Maheshwari (1970) and Eretmonia Du Toit (1932), although it has been suggested that they actually represent a single taxon (Pant, 1987). In both, clusters of pollen sacs are borne on two stalks, which are attached to a subtending leaf. In Eretmonia, which is more completely known, the pollen sacs are elongate (1.0 mm long), and the subtending leaf is small and rhombohedral. Arberiella Pant et Nautiyal is used for isolated pollen sacs similar to those of Glossotheca Surange and Maheshwari. Pollen of the glossopterids is bisaccate and striate (taeniate). It has generally been compared to the sporae dispersae genus Protohaploxypinus, although Lindström et al. (1997) found four different morphogenera within a single pollen sac of Arberiella.
CAYTONIALES
The Caytoniales are a small group of Triassic–Cretaceous seed ferns (Krassilov, 1977a) that was erected in 1925 by the British paleobotanist H. H. Thomas, based on compression specimens from the Middle Jurassic plant-bearing beds along the coast of Cayton Bay in Yorkshire, Great Britain. These plants possessed such interesting features that Thomas regarded them as a new group of angiosperms in his initial description (Thomas, 1925). Since that time, the seed-bearing structure Caytonia Thomas has captured the imagination of paleobotanists and has been variously used as a link to the angiosperm carpel (e.g., Gaussen, 1946; Doyle, 1978, 1996, 2006). As a result, the Caytoniales have figured prominently in a number of phylogenetic analyses, despite the fact that they continue to be one of the most poorly known groups of Mesozoic seed ferns.
Ovulate organs
Caytonia consists of an axis 5.0 cm long bearing stalked, multiovulate cupules in subopposite pairs (Fig. 13) (Thomas, 1925; Harris, 1964). This structure, which has been interpreted as a megasporophyll, bears scars along the surface, suggesting that the cupules were shed at maturity. Each cupule is compressed to be nearly circular in outline (Fig. 14) and recurved with a liplike projection directed toward the point of attachment (Harris, 1940). A single cupule contains from 8–30 seeds, depending on the species, and each seed is attached by a delicate stalk in an orthotropous position (Fig. 15). Seeds are 2.0 mm long and radially symmetrical with an integument composed of an outer, uniseriate epidermis that covers a row of radially aligned, thick-walled cells (e.g., Harris, 1958). Harris (1951) suggested that perhaps the outer portion of the integument was fleshy.
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termed the stigmatic flap or region. This was no doubt the principal reason that the cupule was described as an angiospermous fruit containing numerous seeds. According to this interpretation, fertilization would have taken place via a pollen tube that grew from the pollen grain on the stigmatic surface to the pollen chamber of an ovule. Fine strands of cuticle that extended from the cupule to the seeds were interpreted as the remnants of pollen tubes or as extensions of the seed micropyles. Later research, however, revealed that pollen grains were actually present inside the cupule, perhaps drawn in by pollination droplets that originated at the micropylar end of each seed. The next step in elucidating the reproductive biology of Caytonia was provided by Maria Reymanówna (1973) . Her detailed work indicated that each seed was associated with an elongate canal extending from the seed micropyle to the outer lip of the cupule and that the number of these canals was equal to the number of seeds produced in each cupule. Today, Caytonia is interpreted as a multiovulate cupule and not an angiospermous fruit as originally thought.
Caytonia demonstrates at least one method in which seeds became enclosed and in this feature parallels the morphology, although not the function, of an angiosperm carpel (Krassilov, 1977a). Doyle (1978, 2006) has supported the idea, proposed earlier by Gaussen (1946), that the Caytoniales represent some grade of angiosperm ancestors. According to this theory, there is a reduction in the number of ovules in Caytonia to one per cupule. The cupule wall would be homologous with the second integument in an angiosperm ovule and the cupule-bearing axis would develop to grow over and enclose the cupule and is thus homologous with the carpel. This idea requires that the main Caytonia axis develop into a flattened, dorsiventral structure, and cuticular differences on the upper and lower sides of the axis have been used to support this scenario. Because all caytonialean fossils represent flattened compressions and no internal anatomy is known, however, it is difficult to extrapolate the three-dimensional morphology of the reproductive structures. In addition, in some specimens of Caytonia, the ovules are borne on long stalks (e.g., Fig. 13), a configuration which would presumably make it difficult for overgrowth of the stalk.
Pollen organs
Caytonanthus Harris (originally Antholithus) is a pollen-bearing structure that was also found in the Middle Jurassic Yorkshire flora in association with Caytonia cupules and foliage of Sagenopteris Presl in Sternberg. Thomas included it in the Caytoniales on the basis of the pollen, which was identical to that found in Caytonia. Caytonanthus consists of a slender axis bearing flattened, pinnate lateral branches (Fig. 16); each branch bears from 1–3 elongate synangia (Osborn, 1994). Synangia are about 1.0 cm long, pointed at the distal end (Fig. 17), and contain 1–4 pollen sacs (originally termed locules) that are arranged around a central zone of tissue (Harris, 1941). These structures (which have been termed anthers in some treatments) are circular in cross section, with dehiscence taking place toward the center of each synangium. The epidermis is composed of delicate fusiform cells, perhaps with thicker-walled fibrous cells beneath.
Pollen grains of Caytonanthus are small and bisaccate, and if found dispersed would be included in Vitreisporites Leschik. Grains are 25–40 µm in diameter and contain endoreticulations lining the interior of the sacci, thus making these grains eusaccate (Zavada and Crepet, 1986; Osborn, 1994). Another interpretation is that the grains are protosaccate and the endoreticulations are continuous between the saccus wall and surface of the corpus (Pedersen and Friis, 1986). The ultrastructure of the exine suggests that the sexine is alveolate, and there is a conspicuous sulcus on the distal surface (Zavada and Crepet, 1986).
CORYSTOSPERMALES
The Corystospermales have a worldwide distribution based on foliage and, in many cases, reproductive structures. In Gondwana, foliage of Dicroidium Gothan is often the dominant element in Middle–Late Triassic floras, and the genus is known from localities in Antarctica, South Africa, Australia, Argentina, Tasmania, and India. In Laurasia, foliage of Pachypteris Brongniart (Harris, 1964) and Thinnfeldia von Ettingshausen is assigned to the corystosperms. Umkomasia Thomas and Pteruchus Thomas are known from the Jurassic of Europe associated with Thinnfeldia foliage (Kirchner and Müller, 1992). Recently, three species of Dicroidium leaves have been described from the Upper Permian of Jordan (Abu Hamad et al., 2008), suggesting that the group may have originated in the late Paleozoic and spread into Gondwana through Africa. The family was established by Thomas in 1933 to include Dicroidium foliage, Umkomasia (and other) ovulate organs, and Pteruchus pollen organs, with the familial name based on the characteristic helmet shape of the uniovulate cupules. Based on the morphological diversity within the corystosperms, Archangelsky (1996) suggests that they were a diverse and rapidly evolving group during the Triassic. The plants were probably small to large woody shrubs and trees and bore pinnate leaves with open dichotomous venation. Although the various plant parts have not been found attached, their consistent occurrence in the same beds, similarity in epidermal anatomy, and identical pollen found in both pollen organs and seeds have been used to indirectly associate the various organs (Petriella, 1983). When permineralized, the plants have been reconstructed based on the occurrence of unique secretory cells in the various organs (Taylor, 1996).
Ovulate organs
One of the interesting aspects of the corystosperms is that the reproductive organs are morphologically consistent within the group. The most common seed-containing structure is Umkomasia (Fig. 18) (Thomas 1933), which is known widely from Gondwanan deposits (Taylor, 1996), but is also known from Europe (Kirchner and Müller, 1992) and China (Figs. 19, 20) (Zan et al., 2008). It consists of a fertile branch, more than 15 cm long in some taxa, e.g., U. quadripartita Anderson and Anderson (2003), which produces laterals. Each lateral bears one to several pairs of recurved, helmet-like, generally uniovulate cupules. Some specimens have a pair of subtending bracts at the base of the branch (Fig. 21); in others, they are not present and may have been shed (Holmes, 1987).
The branching in Umkomasia was originally interpreted to be flattened in a single plane (Thomas, 1933), but permineralized specimens from the Middle Triassic of Antarctica indicate that the cupulate branch has stem-like anatomy and produces paired traces to the laterals. The cupule-bearing branches of U. resinosa Klavins et al. (2002) are helically arranged and cupules contain either one or two ovules attached to the abaxial surface (Fig. 22) of the cupule wall. Ovules of this species are small, possess a single integument, and are characterized by a bifid micropylar extension at the distal end.
Cupules preserved as compressions and impressions often appear urn-like in morphology with two prominent lobes (Fig. 19). The surface of the cupule is wrinkled, suggesting that it may have been fleshy (Thomas, 1933). On well-preserved specimens, stomata are present on both surfaces of the cupule. The seeds of U. macleanii are small (5.0 mm long) and borne either singly or in pairs in each cupule (Thomas, 1933). Compressed cupules have also been found attached to short shoots, which in turn arise from longer branches bearing D. odontopteroides leaves (Fig. 23) (Axsmith et al., 2000). Cupules of U. uniramia Axsmith et al. (2000) are borne in whorls of five to eight. The cupules attached to short shoots (Fig. 24) and leaves attached to long shoots from the Upper Triassic of Antarctica has perplexed some who challenge whether long shoots would retain leaves (e.g., Artabe and Brea, 2003; Holmes and Anderson, 2005). In modern Ginkgo L., however, leaves are borne on relatively large stems as well as on short shoots (Axsmith et al., 2007). It is also important to note that this Dicroidium plant grew at high polar latitudes, and thus the parameters affecting growth were no doubt much different than they are in temperate regions today (Axsmith et al., 2007). The report of Umkomasia cupules (Figs. 19, 20) in association with Thinnfeldia-type foliage from the Upper Triassic of China (Zan et al., 2008) further expands the diversity within the corystosperms. Umkomasia has also recently been described from the Upper Permian of India (Chandra et al., 2008), providing some support for the idea that the corystosperms arose in the late Paleozoic (Kerp et al., 2006; Abu Hamad et al., 2008).
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, Pilophorosperma Thomas (1933) (Fig. 25), and Karibacarpon Lacey (1976) . Judging from the number of species described, Pilophorosperma is perhaps the most common seed-producing member of this group (Thomas, 1933). Some cupules are less hemispherical in outline than are those in Umkomasia. Specimens of P. granulatum have three cupules at the end of each branch, while two are common in P. gracile. On the outer surface of the cupule are short papillae, and the inner surface is covered with long, pointed hairs. In P. crassum the cupules are borne in an overlapping fashion along the axis so that the fertile branch appears compact. Holmes (1987) places Pilophorosperma and Karibacarpon in the genus Umkomasia. On the basis of consistent co-occurrence in the Middle Triassic of eastern Australia, he suggests that U. feistmantelii was the cupulate organ of the plant that produced Dicroidium zuberi foliage.
Some seeds of the corystosperms possessed a slightly curved, bifid micropylar canal, which often extended beyond the cupule margin (Fig. 25) (Thomas, 1933). Macerations suggest that the integument contained no fibrous cells and that the seed epidermis was covered with a thick cuticle. Embedded in the pollen chambers are numerous saccate pollen grains similar to those found in the pollen-producing organ Pteruchus (Townrow, 1962).
Pollen organs
The most common pollen organ attributed to the Corystospermales is Pteruchus (Thomas, 1933) (Fig. 26). The genus is known throughout Gondwana (Townrow, 1962; Taylor, 1996), but there are also scattered reports from Laurasia, e.g., P. septentrionalis from the Rhaeto–Liassic (Late Triassic–Early Jurassic) of Germany (Kirchner and Müller, 1992). Most specimens have alternately arranged microsporophylls attached to an axis about 4.0 cm long (Thomas, 1933; Townrow, 1962), although in P. indicus the microsporophylls appear to be helically arranged (Pant and Basu, 1973). Each microsporophyll terminates in a flattened head (Fig. 27) that bears numerous, elongate pollen sacs on the abaxial surface; these are partially protected by the tissue of the head. The number of sacs per head is variable (20–200), and dehiscence is longitudinal. The cuticle on all parts shows epidermal cells with slightly undulate margins and few stomata (Townrow, 1962).
Permineralized specimens of Pteruchus are known from peat deposits from the lower Middle Triassic of Antarctica (Yao et al., 1995). Pteruchus fremouwensis Yao et al. (1995) consists of a branch bearing helically arranged microsporophylls (Fig. 28). Each microsporophyll has a flattened head bearing 20 elongate, sessile, unilocular pollen sacs. Pollen sacs are 
2.0 mm long and possess walls that contain secretory cells (Fig. 29) like those in the leaves of D. fremouwensis (Pigg, 1990b) from the same peat deposit (Pigg and Taylor, 1990). If found dispersed, the pollen of Pteruchus would be assigned to Alisporites Daugherty, Pteruchipollenites Couper, or Falcisporites Leschik. Pollen is bisaccate, with the sacci slightly inclined and partially covering the distal sulcus. Pollen of P. dubius ranges from 80–115 µm in the primary plane (Taylor et al., 1984). The sacci have endoreticulations on their inner surfaces, but the outer surfaces are smooth (Zavada and Crepet, 1985).
Another pollen organ believed to belong to the corystosperms is Pteroma Harris. Pteroma is known to date only from the Middle Jurassic of Yorkshire, where it is associated with Pachypteris foliage (Harris, 1964). In Pteroma thomasii, the microsporophyll is flattened and bears two rows of pollen sacs from what is interpreted as the lower surface. Each head is shield-shaped, with the pollen sacs partially embedded in the tissue. Pollen is bisaccate and up to 107 µm long. It is not known whether these grains are protosaccate or eusaccate like those of Pteruchus (Osborn and Taylor, 1993). Other putative corystosperm pollen organs include Nidiostrobus from India (Bose and Srivastava, 1973) and Kachchhia from India and Antarctica (Bose and Banerji, 1984; Gee, 1989).
PETRIELLALES
This order of seed ferns was defined based on a single genus of permineralized cupule containing seeds from the lower Middle Triassic of Antarctica (Taylor et al., 1994). A new family, Kannaskoppiaceae, based on impression-compression specimens, was later included in the order (Anderson and Anderson, 2003).
Ovulate organs
Cupules of Petriellaea Taylor et al. (1994) are bilateral, elongate, and borne in clusters on a dichotomizing axis (Fig. 30). A vascular bundle extends along the midrib of the cupule with a trace given off to each ovule. The cupule wall is thin, but there is no evidence of a preformed suture. Each cupule contains from 2–6 small (1.0 mm in diameter), triangular ovules (Fig. 31), each attached to the adaxial surface of the cupule surface at differing levels (Fig. 32). Ovules are orthotropous with the integument thickened only in the corners; extending from the distal end of the seed is a short micropylar tube.
Morphologically, there is some superficial similarity between the cupules of Petriellaea and those of Caytonia. While the structure of the Caytonia cupules remains unknown, in Petriellaea the organization suggests that the cupule has evolved by a proximal-distal folding of the megasporophyll (Fig. 32) (Taylor et al., 1994), rather than by enrolling or folding laterally along the midrib, the hypothesized ancestral conduplicate carpel organization sometimes attributed to the earliest angiosperms. Nothing is known about pollen organs that were associated with the Petriellaea cupules.
The Kannaskoppiaceae includes impression fossils of pollen organs (Kannaskoppianthus), ovulate structures (Kannaskoppia) (Fig. 33), and foliage (Kannaskoppifolia) from the Upper Triassic Molteno Formation of South Africa (Anderson and Anderson, 2003). Leaves are cuneate to flabellate and lack a petiole; the lamina is entire to deeply divided into segments with anastomosing venation. Similar leaves from the Upper Triassic of Argentina and Chile have been described as Rochipteris by Herbst et al. (2001) . The seed-bearing organs Kannaskoppia are termed strobili with each 2.0 cm long and are attached in groups of two or three in the axils of the leaves. Each consists of a short, proximal axis segment, which then forks to form two secondary axes. Each of these bears two rows of megasporophylls, with each sporophyll containing a single cupulate ovule (Fig. 33); at maturity, the cupule splits into three lobes. The pollen organ Kannaskoppianthus is up to 45 mm long and constructed of two rows of microsporophylls arising from a forked axis, each with five recurved, longitudinal pollen sacs in a distal concavity protected by an operculum.
PELTASPERMALES
The peltasperms were initially described from the Upper Triassic of Greenland and South Africa based on associated foliage (Lepidopteris Schimper), pollen organs (Antevsia Harris), and seed-bearing organs (Peltaspermum Harris) (Thomas, 1933; Harris, 1937). As defined by Townrow (1960), the group included bipinnate foliage of Lepidopteris, peltate, ovulate reproductive structures of Peltaspermum, and pinnately branched pollen organs of Antevsia, which bore small, oval pollen grains. Townrow (1960) was able to put the three parts together because L. ottonis Schimper, A. zeilleri (Nathorst) Harris, and P. rotula Harris all bore characteristic blisters on the epidermis and had the same stomatal structure. A unique feature of the foliage of the peltasperms is the presence of intercalary pinnules on the rachis, termed Zwischerfiedern. Because of the peltate megasporophylls, the group was at one time thought to be morphologically isolated from other seed ferns. Today, however, the order encompasses a much wider range of morphologies and reproductive biologies than in the original concept. The geographic and geologic range of the group has also expanded, and peltasperms are now known from North America, Europe (Kerp, 1988; Kerp et al., 2001), and the Russian platform (Gomankov and Meyen, 1986; Naugolnykh and Kerp, 1996), and from the Pennsylvanian (Kerp et al., 2001) into the Triassic. As currently circumscribed, the group was probably more widespread during the Permian than the Triassic.
Ovulate organs
The ovulate organs of the peltasperms demonstrate a wide range of morphological variability. Those from the Rotliegend (Upper Pennsylvanian–Lower Permian) of Europe are unlike the structures for which the group was erected. Based on repeated co-occurrences of material from the Rotliegend of central Europe, the well-known foliage type Callipteris conferta (Sternberg) Brongniart and the ovule-bearing reproductive organ Autunia Krasser (Fig. 34) were combined into Autunia conferta (Sternberg) Kerp (Kerp, 1982, 1988). Autunia was originally introduced for strobili with helically arranged, fan-shaped megasporophylls, each bearing one or two ovules on the lower surface (Figs. 35, 36). Pollen-producing organs of Arnhardtia (Zeiller) Haubold et Kerp are believed to belong to A. conferta and consist of 5–9 pollen sacs borne on a peltate microsporophyll (Barthel, 2006). Unlike previously described peltasperms, however, these pollen sacs contain monosaccate grains assignable to Vesicaspora Schemel; grains are up to 50 µm in diameter.
|
) that consist of elliptical to radial, peltate, umbrellalike discs (Figs. 37, 38), which are sometimes termed peltoids (e.g., Meyen 1984; Naugolnykh, 2001). The discs (megasporophylls) are up to 1.0 cm in diameter and helically arranged into simple linear-cylindrical strobili (Fig. 39); ovules are borne in a ring on the lower surface of the megasporophylls (Townrow, 1960). The number of ovules per disc is variable.
Based on association, a concept which was expanded by Meyen (1987) and termed assemblage genera, Poort and Kerp (1990) emended the genus Peltaspermum, so that foliage and ovulate structures are both circumscribed by the "natural" genus Peltaspermum. "Natural" taxon concepts similar to the one suggested for A. conferta have been proposed for several other Early Permian taxa, including Autunia naumannii (Gutbier) Kerp (ovulate organs), Rhachiphyllum schenkii (Heyer) Kerp (foliage), and Arnhardtia scheibei (Gothan) Haubold et Kerp (pollen organs) (e.g., Kerp, 1988; Kerp and Haubold, 1988; Barthel, 2001, 2006). Peltaspermum reproductive organs, described from a site in Morocco, have certain features, i.e., resinous bodies, that also occur on Rhachiphyllum Kerp foliage from the same site (Kerp et al., 2001).
Peltaspermopsis polyspermis Gomankov is a natural genus concept used for Late Permian peltasperms from Russia. The plant includes vegetative stems, some with conspicuous nodes, which are interpreted as evidence of seasonal growth interruptions. Lanceolate leaves assigned to Pursongia Zalessky are also considered to be part of the same plant, along with reproductive organs in the form of seed-bearing discs and their "racemose" aggregations (Fig. 40) (Naugolnykh, 2001).
The genus Meyenopteris Poort et Kerp has also been suggested to be a "natural" genus of peltasperms (but see Karasev and Krassilov, 2007), using the concept of Poort and Kerp (1990), and includes the form taxa Lepidopteris natalensis and Peltaspermum thomasii. Lepidopteris natalensis foliage is typically bipinnate, with small blister-like swellings on the axes and intercalary pinnules (Zwischerfiedern), characters that are diagnostic for the genus. The blister-like swellings also occur on the ovule-bearing organs of P. thomasii, which made it possible to connect the two plant parts. In this species, two ovules (3.0 mm long) occur on the lower surface of each disc-shaped megasporophyll. Lopadangium Zhao et al. emend. Gomankov et Meyen is used for peltaspermaceous ovulate organs that cannot be correlated with foliage or other organs.
Pollen organs
In the Mesozoic forms, such as Antevsia, pollen sacs are borne on branches. Antevsia includes branched axes that bear lateral groups of 4–12 elongate pollen sacs at their distal tips (Fig. 41). Townrow (1960) described Antevsia as pinnate, with the main axis bearing alternate laterals in one plane and secondary branches produced irregularly. Although these branches are described as microsporophylls, the branches are not expanded at their tips (Fig. 42). Branches show the characteristic blister-like swellings that also occur on Lepidopteris fronds. Pollen sacs are up to 5 mm long and dehisce longitudinally. Like the majority of the Mesozoic Gondwanan peltasperms, pollen grains are small (23–40 µm) and oval, with a distal sulcus; if dispersed, these grains would be assigned to Cycadopites Wodehouse ex Wilson and Webster.
In the Late Pennsylvanian–Early Permian peltasperms, the pollen organs are not known in great detail. Perhaps the best-known form is Callipterianthus arnhardtii Roselt (1962) from the Rotliegend (Pennsylvanian–Early Permian) of Germany. This fossil has a frond-like (pinnate) organization with pollen sacs attached to reduced pinnules in the distal part of the frond. Sterile pinnae occur in the proximal portion of the frond, and intercalary pinnules are present on the rachis. Although the specimen is partially sterile, a correlation with sterile foliage is difficult. Callipterianthus arnhardtii has been suggested to represent the pollen-producing organ of either Autunia naumannii or Arnhardtia scheibei (see Kerp, 1996). Barthel (2006), however, assigned pollen organs of the Pterispermostrobus type, which is composed of elongate pollen sacs attached to a peltate microsporophyll, to Arnhardtia scheibei.
DISCUSSION
We have provided information about the reproductive parts of the glossopterids and the major groups of late Paleozoic–Mesozoic seed ferns so as to provide base-level data that can be used in discussing either real or inferred relationships with the angiosperms. Although there are, of course, still gaps in our knowledge of these groups, a large amount of data has been gathered in the last ten years, especially for the peltasperms and the corystosperms. Except for the Petriellales, these groups have been considered as possible angiosperm ancestors because all have ovules attached to a more or less leaflike megasporophyll. Some groups have cupules that partially enclose their ovules, i.e., the corystosperms, Petriellales, and caytonialeans. Others, such as the peltasperms, do not have enclosed ovules. Nevertheless, at one time or another, taxa in all of these groups have been suggested as demonstrating morphological stages of angiospermy based on the implied homologies of the reproductive organs or as showing some intermediate stage in the transformation of an angiosperm organ, usually a carpel. Space does not permit a discussion of what does or does not constitute a unique angiosperm feature, and all are familiar with the limitations imposed on defining such a feature in the fossil record. The problem of real or implied homology using fossils is exacerbated by the absence of structurally preserved fossils in some of the groups and by the use of composite terminals in some phylogenetic analyses, rather than whole plants reconstructed on the basis of attachment, shared anatomical characters, or consistent and exclusive co-occurrence.
Like many other Paleozoic and Mesozoic pteridosperms, the glossopterids have been suggested as possible ancestors to the angiosperms. Perhaps the earliest advocate of this relationship was Plumstead (1956), who interpreted the glossopterid ovulate organs as bisexual. The glossopterid-angiosperm connection has periodically gained support as additional information about the ovulate organs has been published and hypotheses advanced that attempt to homologize these organs with those of other seed plants (e.g., Melville, 1983). For example, Retallack and Dilcher (1981) championed the idea initially suggested by Stebbins (1974) of the glossopterids as flowering plant progenitors. They proposed a transformational series in which the number of ovules on the megasporophyll is reduced to one. The megasporophyll would then enclose the ovule to form a second integument, and the subtending leaf would be transformed into the carpel. Doyle (2006) also discussed this idea as a way to evolve the angiosperm carpel, with perhaps Caytonia as an intermediate. Geologic time remains an obstacle to the acceptance of glossopterids as angiosperm ancestors, however, because the glossopterids disappeared around the Permian–Triassic boundary (251 million years ago [Ma]), while the first recognizable angiosperm megafossils do not occur until the Lower Cretaceous (Barremian–Aptian, 145 Ma; Friis et al., 2006).
Phylogenetic analyses have treated the glossopterids as a single, composite terminal, reconstructed of various organs, often from different sites, thus providing little resolution of the group’s diversity in the analysis (e.g., Nixon et al., 1994; Doyle, 2006; Hilton and Bateman, 2006). There has been some attempt to relate isolated organs based on associations and anatomy, and in some cases, the vegetative parts of plants have been reconstructed, e.g., Glossopteris schopfii Pigg and G. skaarensis Pigg from Antarctica (Pigg and Taylor, 1993) and G. homevalensis Pigg et McLoughlin from Australia (Pigg and Nishida, 2006). A permineralized ovulate structure from the Late Permian of Antarctica could be attributed to G. schopfii leaves based on similar anatomy (Taylor and Taylor, 1992), and Nishida et al. (2007) suggested that Homevaleia gouldii ovulate organs belong to leaves of G. homevalensis. These studies represent a first step in taking what may be a heterogeneous group and developing a framework that can be used to test subsequent hypotheses of relationships, not only within the glossopterids, but with other seed plants. Until homologies can be established, there is currently insufficient evidence to link the glossopterids with any other major group of plants, either as progenitors or descendants.
The late Paleozoic–Mesozoic seed ferns have never represented a natural group, and whether each of the four orders discussed represents a monophyletic group is also far from settled, because no complete phylogeny has been presented for any of these plants. It is clear from our current state of knowledge of these groups that the discovery of additional specimens, especially those in different modes of preservation, and research that focuses directly on these groups is what is needed in the years ahead if more robust relationships are to be fully realized. In almost all phylogenetic analyses of seed plants published to date, each of these seed fern orders has been treated as a clade and is often represented as a single, composite terminal, even when reconstructions have been based only on association. Some reconstructions of "whole" plants have used organs from different continents! In the case of the corystosperms, which currently represent the best-known group overall, the remarkable uniformity of both pollen and ovulate organs throughout Gondwana suggests that at least the Gondwanan representatives may constitute a single clade. Artabe and Brea (2003) conclude that the group is not a natural one, but their analysis was based primarily on stem anatomy, a character that is variable and may simply reflect habitat. It is interesting to note that the Dicroidium plants reconstructed from South America and Antarctica suggest the presence of two quite different growth architectures (based on stem anatomy), although their reproductive organs and foliage are very similar (Petriella, 1978; Taylor, 1996).
The Caytoniales are perhaps the most poorly known of the Mesozoic seed ferns, yet it is the cupule-bearing megasporophyll of Caytonia that has received the greatest amount of attention in scenarios leading to the origin of the angiosperm carpel and seeds with two integuments (e.g., Doyle, 2006). While important details about the reproductive biology of the Caytoniales are known, there is nothing to suggest that they possessed anything other than a distinctly gymnospermous seed-plant reproductive system. As is the case with some of the peltasperms, the Caytoniales produced saccate pollen, a morphological character state that both groups share with the Paleozoic callistophytalean seed ferns. It is important to point out that prior to the recognition of the Pennsylvanian Callistophytales, pollen of this morphotype would have implied affinities with some conifer or cordaite seed-plant group. If in fact any of these groups are distant progenitors of flowering plants, then the fact that many possess saccate pollen may simply reflect that the pollination syndrome did not keep pace with developmental changes in the function of the mature microgametophyte. The primitive nature of the male gametophyte is also underscored by the discovery of flagellated sperm in the glossopterid Homevaleia that, aside from their reduced size, morphologically resemble the male gametes of cycads and Ginkgo.
At the present time, the Peltaspermales are perhaps the most perplexing of all of these late Paleozoic–Mesozoic seed plants. The morphology of the Autunia ovulate organ is distinct from that of the Peltaspermum known from numerous other sites, including Siberia and Gondwana; however, the absence of any anatomical features significantly impedes progress in resolving this seed-plant group. This is also the case for the Petriellales, although structurally preserved cupules and seeds are known, no other plant parts have been found to date. These isolated organs are included within the assemblage known as seed ferns both for convenience and necessity, because all produce ovules on a modified, leaflike structure.
We have noted earlier that many of the ideas regarding the origin of the flowering plants have been based on scenarios in which megasporophylls become transformed so that the lamina covers the ovule(s), and this stage has been cited as a precursor to the evolution of a carpel. Although this was the original concept of Thomas when he described the Caytoniales, subsequent theories have used the cupule to form a second integument of the seeds, and other tissue to derive the carpel. All these scenarios suggest that megasporophyll closure is longitudinal, a theoretical basis that is supported by conduplicate folding in certain extant flowering plants and even in some Early Cretaceous angiosperms (e.g., Archaeanthus Dilcher et Crane, Lesqueria Crane et Dilcher, Protomonimia Nishida et Nishida). What is interesting about Petriellaea is that megasporophyll closure may have proceeded in a different pattern in which the tip of the megasporophyll is bent back toward the base or petiole (Taylor et al., 1994). This may also represent the pattern in Caytonia.
Beginning in the late Paleozoic and continuing into the Mesozoic, almost all seed-plant groups demonstrate increasing levels of cupule and megasporophyll closure. Historically, this has been interpreted as a response to predation or other selective advantages associated with ovule protection. While this structure–function relationship may have some validity, another hypothesis suggests that intercalating sterile tissue between ovules and pollen was a key physiological innovation in the transition from gymnospermy to angiospermy (Zavada and Taylor, 1986a). In this context, closure of the megasporophyll was directly linked to the evolution of self incompatibility and a change from postzygotic to prezygotic selection. There would have been strong selective pressure on pollen to develop alternative mechanisms to insure compatibility with the stigma in angiosperms. More efficient pollen transfer, the evolution of accessory floral parts to influence potential pollinator behavior, and the loss of sacci may have been some of the evolutionary stimuli in the transition to angiospermy. Interestingly, to the extent where pollen for a group is known, all the late Paleozoic–Mesozoic seed ferns, including the glossopterids, possess saccate pollen, with the exception of Cycadopites grains recovered from the peltasperm Antevsia (Townrow, 1960). This is in contrast to the situation in angiosperms where sacci are found only in the extant genus Lactoris Philippi (Zavada and Taylor, 1986b)
While the morphological features showing a transition to the angiosperm carpel may be difficult to resolve based on fossils, the fossil record can sometimes offer another dimension—the gametophyte phase—in deciphering the transition from gymnospermy to angiospermy. The discovery of male gametes similar to those in cycads and Ginkgo in the glossopterid Homevaleia (Nishida et al., 2003) contributes important details about one group of plants thought to represent potential flowering plant progenitors. The inclusion of this character state in a data matrix may suggest glossopterid affinities with the cycads and Ginkgo—a conclusion that is predictable, but may not be correct if the glossopterids are more heterogeneous than previously thought.
We believe that our understanding of all these fossil groups will significantly advance when anatomically preserved specimens are found and when there are better reconstructions that either combine organs unique to a site or that link organs based on distinctive synapomorphies (Taylor et al., 2006). With the exception of the Petriellales and Corystospermales, which are known from permineralized and compressed fossils, we know a great deal about the morphology and even the epidermal anatomy of some groups like the Caytoniales and Peltaspermales, but nothing about the internal anatomy. These data will be critical in characterizing homologies with other seed plant groups. In addition, details about where the reproductive organs are produced, how they are attached, and how much diversity they demonstrate within each group are important areas that require additional attention. This is especially true of the Glossopteridales. As to the question posed in the title of this paper—the same question that has been addressed countless times since Darwin’s declaration regarding the "abominably perplexing" problem of angiosperm origins (Crepet, 2000)—from our perspective, the mystery remains intact. We would offer one caveat, however. In our opinion, it will be more productive to attempt to solve Darwin’s mystery if there were greater attention directed at mining the rock record in the hope of discovering more informative and new specimens, than to continue to construct new phylogenies using the same, often ambiguous characters.
FOOTNOTES
1 The authors thank the following colleagues for kindly supplying figures: J. M. Anderson, C. P. Daghlian, H. Kerp, S. McLoughlin, H. Nishida, P. Ryberg, and M. Zavada, as well as students and postdoctoral scholars in our laboratory who contributed to this work. This research was partially supported by the National Science Foundation (OPP-0229877, ANT-0635477). 
2 E-mail: etaylor{at}ku.edu; tntaylor{at}ku.edu
LITERATURE CITED
Abu Hamad, A., H. Kerp, B. Vörding, AND K. Bandel. 2008. A Late Permian flora with Dicroidium from the Dead Sea region, Jordan. Review of Palaeobotany and Palynology 149: 85–130.[CrossRef][Web of Science]
Adendorff, R. 2005. A revision of the ovuliferous fructifications of glossopterids from the Permian of South Africa. Ph.D. dissertation, University of the Witwatersrand, Johannesburg, South Africa.
Adendorff, R., S. McLoughlin, AND M. K. Bamford. 2002. A new genus of ovuliferous glossopterid fructifications from South Africa. Palaeontologia Africana 38: 1–17.
Anderson, J. M., AND H. M. Anderson. 2003. Heyday of the Gymnosperms: Systematics and Biodiversity of the Late Triassic Molteno fructifications (Strelitzia 15). South African National Botanical Institute, Pretoria, South Africa.
Archangelsky, S. 1996. Aspects of Gondwana paleobotany: Gymnosperms of the Paleozoic–Mesozoic transition. Review of Palaeobotany and Palynology 90: 287–302.[CrossRef][Web of Science]
Artabe, A., AND M. Brea. 2003. A new approach to Corystospermales based on Triassic permineralized stems from Argentina. Alcheringa 27: 209–229.[Web of Science]
Axsmith, B. J., E. L. Taylor, AND T. N. Taylor. 2007. The "new approach to Corystospermales" and the Antarctic fossil record: A critique. Ameghiniana 44: 223–230.[Web of Science]
Axsmith, B. J., E. L. Taylor, T. N. Taylor, AND N. R. Cúneo. 2000. New perspectives on the Mesozoic seed fern order Corystospermales based on attached organs from the Triassic of Antarctica. American Journal of Botany 87: 757–768.
Barthel, M. 2001. Arnhardtia scheibei (Gothan) Haubold & Kerp und andere Rotliegend-Peltaspermaceen. Wege und Irrwege ihrer Erforschung. Hallesches Jahrbuch für Geowissenschaften 23: 1–8.
Barthel, M. 2006. Makroflora und zugehörige "in situ" Sporen. In W. Reichel, and M. Schauer [eds.], Das Döhlener Becken bei Dresden—Geologie und Bergbau, (Bergbau in Sachsen 12), 28–40. Sächsisches Landesamt für Umwelt und Geologie (LfUG), Dresden, Germany.
Bose, M. N., AND J. Banerji. 1984. The fossil floras of Kachchh. I. Mesozoic megafossils. Palaeobotanist 33: 1–189.
Bose, M. N., AND S. C. Srivastava. 1973. Some micro- and megastrobili from the Lower Triassic of Gopad River Valley, Nidpur. Geophytology 3: 69–80.
Brongniart, A. T. 1828. Prodrome d’une histoire des végétaux fossiles. Dictionnaire des Sciences Naturelles 57: 16–212.
Chandra, S., K. J. Singh, AND N. Jha. 2008. First report of the fertile plant genus Umkomasia from Late Permian Beds in India and its biostratigraphic significance. Palaeontology 51: 817–826.[CrossRef][Web of Science]
Crane, P. R. 1985. Phylogenetic analysis of seed plants and the origin of angiosperms. Annals of the Missouri Botanical Garden 72: 716–793.[CrossRef][Web of Science]
Crepet, W. L. 2000. Progress in understanding angiosperm history, success, and relationships: Darwin’s "abominably perplexing phenomenon". Proceedings of the National Academy of Sciences, USA 97: 12939–12941.
Cúneo, N. R., J. Isbell, E. L. Taylor, AND T. N. Taylor. 1993. The Glossopteris flora from Antarctica: Taphonomy and paleoecology. In S. Archangelsky [ed.], Compte Rendu, Congrès International de Géologie du Carbonifère-Permian, Buenos Aires, Argentina, vol. 2, 13–40.
Dilcher, D. L. 1979. Early angiosperm reproduction: An introductory report. Review of Palaeobotany and Palynology 27: 291–328.[CrossRef][Web of Science]
Doyle, J. A. 1978. Origin of angiosperms. Annual Review of Ecology and Systematics 9: 365–392.[CrossRef][Web of Science]
Doyle, J. A. 1996. Seed plant phylogeny and the relationships of Gnetales. International Journal of Plant Sciences 157 (6 Supplement): S3–S39.[CrossRef][Web of Science]
Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133: 169–209.
Du Toit, A. L. 1932. Some fossil plants from the Karroo System of South Africa. Annals of the South African Museum 28: 369–393.
Feistmantel, O. 1886. The fossil flora of the Gondwana System. Part 2. The fossil flora of some of the coal fields in western Bengal. Memoirs of the Geological Survey of India: Palaeontologia Indica, 12th series, 4: 1–71.
Friis, E. M., K. Raunsgaard Pedersen, AND P. R. Crane. 2006. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232: 251–293.[CrossRef]
Gaussen, H. 1946. V: Les autres cycadophytes. L’origine cycadophytique des angiospermes. Travaux du Laboratoire Forestier de Toulouse, Tome II, Etudes dendrologiques, Première section, Les gymnospermes genéralités, vol. I, Les gymnospermes actuelles et fossiles, partie 2, fascicule 3, chapitre 5: 1–26.
Gee, C. T. 1989. Revision of the Late Jurassic/Early Cretaceous flora from Hope Bay, Antarctica. Palaeontographica 213B: 149–214.
Gomankov, A. V., AND S. V. Meyen. 1986. Tatarina-flora (composition and distribution in the Late Permian of Eurasia). Akademii Nauk SSSR. Ordena Trudovogo Krasnogo Znameni Geologicheskii Institut 401: 1–174.
Gould, R. E., AND T. Delevoryas. 1977. The biology of Glossopteris: Evidence from petrified seed-bearing and pollen-bearing organs. Alcheringa 1: 387–399.
Harris, T.M. 1937. The fossil flora of Scoresby Sound East Greenland. Part 5: Stratigraphic relations of the plant beds. Meddelelser om Grønland 112(2): 1–114.
Harris, T. M. 1940. Caytonia. Annals of Botany 4: 713–734.
Harris, T. M. 1941. Caytonanthus, the microsporophyll of Caytonia. Annals of Botany 5: 47–58.
Harris, T. M. 1951. The relationships of the Caytoniales. Phytomorphology 1: 29–39.
Harris, T. M. 1958. The seed of Caytonia. Palaeobotanist 7: 93–106.
Harris, T. M. 1964. The Yorkshire Jurassic flora. II. Caytoniales, Cycadales and pteridosperms. British Museum (Natural History), London, UK.
Herbst, R., A. Troncoso, AND S. Gnaedinger. 2001. Rochipteris nov. gen., hojas incertae sedis (= Chiropteris pro parte) del Triásico superior de Argentina y Chile. Ameghiniana 38: 257–269.[Web of Science]
Hilton, J., AND R. M. Bateman. 2006. Pteridosperms are the backbone of seed-plant phylogeny. Journal of the Torrey Botanical Society 133: 119–168.
Holmes, W. B. K. 1987. New corystosperm ovulate fructifications from the Middle Triassic of eastern Australia. Alcheringa 11: 165–173.[CrossRef][Web of Science]
Holmes, W. B. K., AND H. M. Anderson. 2005. The Middle Triassic megafossil flora of the Basin Creek Formation, Nymboida Coal Measures, New South Wales, Australia, part 4, Umkomasiaceae. Dicroidium and affiliated fructifications. Proceedings of the Linnean Society of New South Wales 126: 1–37.[Web of Science]
Karasev, E. V., AND V. A. Krassilov. 2007. Late Permian phylloclades of the new genus Permophyllocladus and problems of the evolutionary morphology of peltasperms. Paleontological Journal 41: 198–206.[CrossRef][Web of Science]
Kerp, H. 1996. Post-Variscan late Palaeozoic Northern Hemisphere gymnosperms: The onset to the Mesozoic. Review of Palaeobotany and Palynology 90: 263–285.[CrossRef][Web of Science]
Kerp, H., A. Abu Hamad, B. Vörding, AND K. Bandel. 2006. Typical Triassic Gondwanan floral elements in the Upper Permian of the paleotropics. Geology 34: 265–268.
Kerp, H., J. Broutin, S. Lausberg, AND H. Aassoumi. 2001. Discovery of latest Carboniferous–Early Permian radially symmetrical peltaspermaceous megasporophylls from Europe and North Africa. Comptes Rendus de l’Académie des Sciences. Sciences de la Terre 332: 513–519.
Kerp, J. H. F. 1982. Aspects of Permian palaeobotany and palynology. II. On the presence of the ovuliferous organ Autunia milleryensis (Renault) Krasser (Peltaspermaceae) in the Lower Permian of the Nahe area (F.G.R.) and its relationship to Callipteris conferta (Sternberg) Brongniart. Acta Botanica Neerlandica 31: 417–427.[Web of Science]
Kerp, J. H. F. 1988. Aspects of Permian palaeobotany and palynology. X. The west- and central European species of the genus Autunia Krasser emend. Kerp (Peltaspermaceae) and the form-genus Rhachiphyllum Kerp (callipterid foliage). Review of Palaeobotany and Palynology 54: 249–360.[CrossRef][Web of Science]
Kerp, J. H. F., AND H. Haubold. 1988. Aspects of Permian palaeobotany and palynology. VIII. On the reclassification of the west- and central European species of the form-genus Callipteris Brongniart 1849. Review of Palaeobotany and Palynology 54: 135–150.[CrossRef][Web of Science]
Kirchner, M., AND A. Müller. 1992. Umkomasia franconica n. sp. und Pteruchus septentrionalis n. sp., Fruktifikationen von Thinnfeldia Ettingshausen. Palaeontographica 224B: 63–73.
Klavins, S. D., T. N. Taylor, AND E. L. Taylor. 2002. Anatomy of Umkomasia (Corystospermales) from the Triassic of Antarctica. American Journal of Botany 89: 664–676.
Krassilov, V. A. 1977a. Contributions to the knowledge of the Caytoniales. Review of Palaeobotany and Palynology 24: 155–178.[Web of Science]
Krassilov, V. A. 1977b. The origin of angiosperms. Botanical Review 43: 143–176.[CrossRef]
Lacey, W. S. 1976. Further observations on the Molteno flora of Rhodesia. Arnoldia Rhodesia 7: 1–14.
Lindström, S., S. McLoughlin, AND A. N. Drinnan. 1997. Intraspecific variation of taeniate bisaccate pollen within Permian glossopterid sporangia, from the Prince Charles Mountains, Antarctica. International Journal of Plant Sciences 158: 673–684.[CrossRef][Web of Science]
McLoughlin, S. 1990. Some Permian glossopterid fructifications and leaves from the Bowen Basin, Queensland, Australia. Review of Palaeobotany and Palynology 62: 11–40.[CrossRef][Web of Science]
McManus, H. A., E. L. Taylor, T. N. Taylor, AND J. W. Collinson. 2002. A petrified Glossopteris flora from Collinson Ridge, Central Transantarctic Mountains: Late Permian or Early Triassic? Review of Palaeobotany and Palynology 120: 233–246.[CrossRef][Web of Science]
Melville, R. 1983. Glossopteridae, Angiospermidae and the evidence for angiosperm origin. Botanical Journal of the Linnean Society 86: 279–323.[CrossRef][Web of Science]
Meyen, S. V. 1984. Basic features of gymnosperm systematics and phylogeny as evidenced by the fossil record. Botanical Review 50: 1–111.[CrossRef]
Meyen, S. V. 1987. Fundamentals of palaeobotany. Chapman & Hall, New York, New York, USA.
Naugolnykh, S. V. 2001. A new peltaspermaceous pteridosperm from the Upper Permian of the Russian Platform. Palaeobotanist 50: 189–205.
Naugolnykh, S. V., AND H. Kerp. 1996. Aspects of Permian palaeobotany and palynology. XV. On the oldest known peltasperms with radially symmetrical ovuliferous discs from the Kungurian (uppermost Lower Permian) of the fore-Urals (Russia). Review of Palaeobotany and Palynology 91: 35–62.[CrossRef][Web of Science]
Nishida, H., K. B. Pigg, K. Kudo, AND J. F. Rigby. 2004. Zooidogamy in the Late Permian genus Glossopteris. Journal of Plant Research 117: 323–328.[CrossRef][Web of Science][Medline]
Nishida, H., K. B. Pigg, K. Kudo, AND J. F. Rigby. 2007. New evidence of reproductive organs of Glossopteris based on permineralized fossils from Queensland, Australia. I. Ovulate organ Homevaleia gen. nov. Journal of Plant Research 120: 539–549.[CrossRef][Web of Science][Medline]
Nishida, H., K. B. Pigg, AND J. F. Rigby. 2003. Swimming sperm in an extinct Gondwanan plant. Nature 422: 396–397.[CrossRef][Web of Science][Medline]
Nixon, K. C., W. L. Crepet, D. Stevenson, AND E. M. Friis. 1994. A reevaluation of seed plant phylogeny. Annals of the Missouri Botanical Garden 81: 484–533.[CrossRef][Web of Science]
Oliver, F. W., AND D. H. Scott. 1904. On the structure of the Palaeozoic seed Lagenostoma lomaxi, with a statement of the evidence upon which it is referred to Lyginodendron. Philosophical Transactions of the Royal Society of London 197B: 193–247.[Web of Science]
Osborn, J. M. 1994. The morphology and ultrastructure of Caytonanthus. Canadian Journal of Botany 72: 1519–1527.[CrossRef]
Osborn, J. M., AND T. N. Taylor. 1993. Pollen morphology and ultrastructure of the Corystospermales: Permineralized in situ grains from the Triassic of Antarctica. Review of Palaeobotany and Palynology 79: 205–219.[CrossRef][Web of Science]
Pant, D. D. 1987. Reproductive biology of the glossopterids and their affinities. Bulletin de la Société Botanique de France. Actualités Botaniques 134: 77–93.
Pant, D. D., AND N. Basu. 1973. Pteruchus indicus sp. nov. from the Triassic of Nidpur, India. Palaeontographica 144B: 11–24.
Pant, D. D., AND D. D. Nautiyal. 1984. On the morphology and structure of Ottokaria zeilleri sp. nov.—A female fructification of Glossopteris. Palaeontographica 193B: 127–152.
Pant, D. D., AND R. S. Singh. 1974. On the stem and attachment of Glossopteris and Gangamopteris leaves. Part II. Structural features. Palaeontographica 147B: 42–73.
Pedersen, K. R., AND E. M. Friis. 1986. Caytonanthus pollen from the Lower and Middle Jurassic. In J. T. Møller [ed.], Twenty-five years of geology in Aarhus, Department of Geology, Aarhus University, Aarhus, Denmark. GeoSkrifter 24: 225–267.
Petriella, B. 1978. La reconstrucción de Dicroidium (Pteridospermopsida, Corystospermaceae). Obra del Centenario del Museo de la Plata 5: 107–110.
Petriella, B. 1981. Sistemática y vinculaciones de las Corystospermaceae H. Thomas. Ameghiniana 18: 221–234.
Petriella, B. 1983. Sinopsis de las Corystospermaceae (Corystospermales, Pteridospermophyta) de la Argentina. III. Troncos y chrono-stratigrafía. Ameghiniana 20: 41–46.
Pigg, K. B. 1990a. Anatomically preserved Glossopteris foliage from the central Transantarctic Mountains. Review of Palaeobotany and Palynology 66: 105–127.[CrossRef][Web of Science]
Pigg, K. B. 1990b. Anatomically preserved Dicroidium foliage from the central Transantarctic Mountains. Review of Palaeobotany and Palynology 66: 129–145.[CrossRef][Web of Science]
Pigg, K. B., AND H. Nishida. 2006. The significance of silicified plant remains to the understanding of Glossopteris-bearing plants: An historical review. Journal of the Torrey Botanical Society 133: 46–61.
Pigg, K. B., AND T. N. Taylor. 1990. Permineralized Glossopteris and Dicroidium from Antarctica. In T. N. Taylor, and E. L. Taylor [eds.], Antarctic paleobiology—Its role in the reconstruction of Gondwana, 164–172. Springer-Verlag, New York, New York, USA.
Pigg, K. B., AND T. N. Taylor. 1993. Anatomically preserved Glossopteris stems with attached leaves from the central Transantarctic Mountains, Antarctica. American Journal of Botany 80: 500–516.[CrossRef][Web of Science]
Pigg, K. B., AND M. L. Trivett. 1994. Evolution of the glossopterid gymnosperms from Permian Gondwana. Journal of Plant Research 107: 461–477.[CrossRef][Web of Science]
Plumstead, E. P. 1956. Bisexual fructifications borne on Glossopteris leaves from South America. Palaeontographica 100B: 1–25.
Plumstead, E. P. 1958. Further fructifications of the Glossopteridae and a provisional classification based on them. Transactions of the Geological Society of South Africa 61: 52–79.
Poort, R. J., AND J. H. F. Kerp. 1990. Aspects of Permian palaeobotany and palynology. XI. On the recognition of true peltasperms in the Upper Permian of Western and Central Europe and a reclassification of species formerly included in Peltaspermum Harris. Review of Palaeobotany and Palynology 63: 197–225.[CrossRef][Web of Science]
Prevec, R., S. McLoughlin, AND M. K. Bamford. 2008. Novel double wing morphology in a South African ovuliferous glossopterid fructification. Bifariala intermittens (Plumstead 1958) comb. nov. Review of Palaeobotany and Palynology 150: 22–36.[CrossRef][Web of Science]
Retallack, G. J., AND D. L. Dilcher. 1981. Arguments for a glossopterid ancestry of angiosperms. Paleobiology 7: 54–67.[Abstract]
Reymanówna, M. 1973. The Jurassic flora from Grojec near Kraków in Poland. Part II. Caytoniales and anatomy of Caytonia. Acta Palaeobotanica 14: 46–87.
Roselt, G. 1962. Untersuchungen zur Gattung Callipteris. I. Callipteris scheibei Gothan, Aufbau und Habitus des ganzen Gewächses sowie stratigraphisches und geographisches Vorkommen. II. Callipterianthus arnhardtii n. g., n. sp., die erste durch Zusammenhang erwiesene Callipteris- Fruktifikation. Freiberger Forschungshefte, serie C 131: 1–81.
Schopf, J. M. 1976. Morphologic interpretation of fertile structures in glossopterid gymnosperms. Review of Palaeobotany and Palynology 21: 25–64.[CrossRef][Web of Science]
Smoot, E. L., AND T. N. Taylor. 1986. Evidence of simple polyembryony in Permian seeds from Antarctica. American Journal of Botany 73: 1079–1081.[CrossRef][Web of Science]
Stebbins, G. L. 1974. Flowering plants: Evolution above the species level. Belknap Press of Harvard University Press, Cambridge, Massachusetts, USA.
Surange, K. R., AND S. Chandra. 1975. Morphology of the gymnospermous fructifications of the Glossopteris flora and their relationships. Palaeontographica 149B: 153–180.
Surange, K. R., AND H. K. Maheshwari. 1970. Some male and female fructifications of Glossopteridales from India. Palaeontographica 129B: 178–192.
Taylor, E. L. 1996. Enigmatic gymnosperms? Structurally preserved Permian and Triassic seed ferns from Antarctica. Review of Palaeobotany and Palynology 90: 303–318.[CrossRef][Web of Science]
Taylor, E. L., AND T. N. Taylor. 1992. Reproductive biology of the Permian Glossopteridales and their suggested relationship to flowering plants. Proceedings of the National Academy of Sciences, USA 89: 11495–11497.
Taylor, E. L., T. N. Taylor, H. Kerp, AND E. J. Hermsen. 2006. Mesozoic seed ferns: Old paradigms, new discoveries. Journal of the Torrey Botanical Society 133: 62–82.
Taylor, E. L., T. N. Taylor, AND P. E. Ryberg. 2007. Ovule-bearing reproductive organs of the glossopterid seed ferns from the Late Permian of the Beardmore Glacier region, Antarctica. USGS Open-File Reports 2007-1047(082): 1–4.
Taylor, T. N., M. A. Cichan, AND A. M. Baldoni. 1984. The ultrastructure of Mesozoic pollen: Pteruchus dubius (Thomas) Townrow. Review of Palaeobotany and Palynology 41: 319–327.[CrossRef][Web of Science]
Taylor, T. N., G. M. del Fueyo, AND E. L. Taylor. 1994. Permineralized seed fern cupules from the Triassic of Antarctica: Implications for cupule and carpel evolution. American Journal of Botany 81: 666–677.[CrossRef][Web of Science]
Taylor, T. N., AND E. L. Taylor. 1987. Structurally preserved fossil plants from Antarctica. III. Permian seeds. American Journal of Botany 74: 904–913.[CrossRef][Web of Science]
Thomas, H. H. 1925. The Caytoniales, a new group of angiospermous plants from the Jurassic rocks of Yorkshire. Philosophical Transactions of the Royal Society of London, B 213: 299–363.[CrossRef]
Thomas, H. H. 1933. On some pteridospermous plants from the Mesozoic rocks of South Africa. Philosophical Transactions of the Royal Society of London, B 222: 193–265.[CrossRef]
Townrow, J. A. 1960. The Peltaspermaceae, a pteridosperm family of Permian and Triassic age. Palaeontology 3: 333–361.
Townrow, J. A. 1962. On Pteruchus, a microsporophyll of the Corystospermaceae. Bulletin of the British Museum (Natural History), Geology 6: 289–320.
Yao, X., T. N. Taylor, AND E. L. Taylor. 1995. The corystosperm pollen organ Pteruchus from the Triassic of Antarctica. American Journal of Botany 82: 535–546.[CrossRef][Web of Science]
Zan, S.-Q.B., J. Axsmith, N. C. Fraser, F.-X. Liu, AND D. Xing 2008. New evidence for Laurasian corystosperms: Umkomasia from the Upper Triassic of Northern China. Review of Palaeobotany and Palynology 149: 202–207.[CrossRef][Web of Science]
Zavada, M. S., AND W. L. Crepet. 1985. Pollen wall ultrastructure of the type material of Pteruchus africanus, P. dubius and P. papillatus. Pollen et Spores 27: 271–276.
Zavada, M. S., AND W. L. Crepet. 1986. Pollen wall structure of Caytonanthus. Plant Systematics and Evolution 153: 259–264.[CrossRef][Web of Science]
Zavada, M. S., AND T. N. Taylor. 1986a. The role of self-incompatibility and sexual selection in the gymnosperm–angiosperm transition: A hypothesis. American Naturalist 128: 538–550.[CrossRef][Web of Science]
Zavada, M. S., AND T. N. Taylor. 1986b. Pollen morphology of Lactoridaceae. Plant Systematics and Evolution 154: 31–39.[CrossRef][Web of Science]
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