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First published online December 24, 2008; doi:10.3732/ajb.0800193 American Journal of Botany 96: 284-295 (2009) © 2009 Botanical Society of America, Inc. |
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Special Invited Papers |
2 Department of the Geophysical Sciences, The University of Chicago, 5734 S. Ellis Avenue, Chicago, Illinois 60637 USA 3 Chicago Botanic Garden, 1000 Lake Cook Road, Glencoe, Illinois 60022 USA
Received for publication 13 June 2008. Accepted for publication 12 November 2008.
ABSTRACT
Middle Jurassic fossil plants from the Grisethorpe Bed at Cayton Bay and Grisethorpe Bay, Yorkshire, UK, are preserved in a soft claystone, and plant mesofossils recovered by sieving reveal excellent details of external structure. Studies of these mesofossils complement previous work on macrofossils from the Grisethorpe Bed and allow the plant fossils in this classic flora to be studied in a similar way to those preserved in Cretaceous mesofloras. Bennettitales, a key group in discussions of how angiosperms may be related to other seed plants, are especially well represented among mesofossils from the Grisethorpe Bed. Abundant bennettitalean leaves, scale leaves, and fragments of pollen and ovulate organs provide new information on these extinct plants. In particular, a specimen of Williamsoniella coronata (presumed aborted) shows only weak differentiation between interseminal scales and ovules and provides further evidence of homology between these structures.
Key Words: Bennettitales • fossils • Middle Jurassic • paleobotany • Williamsoniella coronata • Williamsonia leckenbyi • Yorkshire
The fossil plant bed (the Grisethorpe Bed) exposed on the foreshore of Cayton Bay and Grisethorpe Bay, just south of Scarborough, Yorkshire in the United Kingdom, is one of the most extensively collected and most intensively studied of all plant fossil assemblages. Fossil plants from the Grisethorpe Bed have been investigated for more than 180 years, including by some of the most important figures in the history of paleobotany (e.g., Phillips, Williamson, Lindley and Hutton, Carruthers, Nathorst, Thomas, Florin, Harris; see review in Thomas and Batten, 2001
) and more than 100 species have been named. The Grisethorpe Bed is the richest of more than 500 sites in Yorkshire that have yielded fossil plants (Thomas and Batten, 2001), and together, the more than 300 species described so far (Harris, 1961, 1964, 1969, 1979; Harris et al., 1974) are the benchmark against which Jurassic floras from around the world are compared.
The importance of the flora from the Grisethorpe Bed derives from the diversity of plant fossils preserved and the quality of their preservation. The plant bed is also readily accessible and well exposed over a large area. The fossils are preserved as coherent coaly compressions in a relatively soft claystone matrix and yield excellent details of cuticles, as well as in situ pollen and spores, with conventional acid–alkali maceration techniques. As a result, many plant fossils from the Grisethorpe Bed have been described in detail and have played a key role in developing our understanding of Mesozoic seed plants. For example, Cayton Bay is the type locality of the Caytoniales (Thomas, 1925), and fossils from the Grisethorpe Bed have provided most of what we know about this interesting group of extinct seed plants. Similarly, through the work of W. Carruthers, A. G. Nathorst, H. H. Thomas, and T. M. Harris, fossil plants from the Grisethorpe Bed have provided key insights into the structure and biology of the Bennettitales (see summary in Harris, 1969), including through reconstructions of "whole bennettitalean fossil plants" that have linked vegetative and reproductive organs (Table 1). Such reconstructed Bennettitales and Caytoniales have figured prominently in analyses and discussions of how angiosperms may be related to other groups of seed plants (e.g., Crane, 1985; Doyle, 2006; Hilton and Bateman, 2006, and references cited therein).
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). Based on this approach, we review knowledge of Bennettitales from the Grisethorpe Bed and provide new information, especially on the different organs of the Williamsoniella coronata plant. The mesofossils recovered provide improved documentation of the structure of Middle Jurassic Bennettitales, as well as new information, and they also suggest new avenues for future research. Studies of other fossil plants from the Grisethorpe Bed, including Caytonia Thomas, will be the focus of subsequent papers. MATERIALS AND METHODS
Bulk samples (
200 kg) were collected from the Grisethorpe Bed in the summer of 2003. The Bed occurs near the base of the Grisethorpe Member in the Cloughton Formation and is of Middle Jurassic (Lower Bajocian) age (Thomas and Batten, 2001; van Konijnenburg-van Cittert and Morgans, 1999). Plant fossils occur as well-preserved compressions and fragments in a soft gray-white claystone, 0.5 m thick, which is interpreted as an abandoned channel deposit (Livera and Leeder, 1981). In Cayton Bay, the Grisethorpe Bed is exposed on the foreshore below the high water mark. At Yon’s Nab, at the eastern limit of Cayton Bay, the plant bed occurs in the base of the cliff and can be traced laterally westward for more than 300 m below Red Cliff (UK Grid Reference TA 083842; 54°14'34''N, 0°20'31''E). In earlier times, important material was also collected from the Grisethorpe Bed exposed in Grisethorpe Bay to the southeast (Thomas and Batten, 2001).
The fossil flora of the Grisethorpe Bed comprises 103 species (Thomas and Batten, 2001). These include three species of liverwort (assigned to Hepaticites Walton), two species of horsetail (Equisteum L.), a lycopod (Lycopodites falcatus Lindley & Hutton), and 21 species of ferns, including Dicksoniaceae, Dipteridaceae, Matoniaceae, Osmundaceae, Schizaeaceae, and probable Polypodiaceae (Harris, 1961). The seed plant component of the flora includes cycads (14 species), conifers (16 species), and Ginkgoales (five species) (Harris et al., 1974; Harris, 1979). There is also extensive representation of extinct groups of seed plants, including Caytoniales (seven species), Czekanowskiales (four species), and "pteridosperms" (six species) (Harris, 1964). Bennettitales are among the most diverse and abundant of all the plant groups represented in the Grisethorpe Bed with 16 named species based on dispersed leaves (Table 1).
Samples were dried in the laboratory, disaggregated in water, and cleaned in hydrofluoric and hydrochloric acid according to standard mesofossil preparation techniques (e.g., Herendeen et al., 1999). Mesofossil residues were then thoroughly washed in water, dried in air, and examined under a dissecting microscope. Specimens selected for scanning electron microscopy were mounted on stubs, coated with gold-palladium using a Denton (Moorestown, New Jersey, USA) sputter coater, and examined with a Leo scanning electron microscope (Cambridge, UK) at 5–10 kV. All specimens are deposited in the paleobotanical collections at the Field Museum, Chicago (PP).
MESOFOSSILS AND THEIR PRESERVATION IN THE GRISETHORPE BED
Sieving and cleaning of samples from the Grisethorpe Bed yields large quantities of plant fragments, each typically less than a few millimeters in maximum dimension, which are easily sorted under a dissecting microscope. Especially abundant are leaf fragments of Bennettitales and other plant groups, as well as large numbers of Caytonia cupules and seeds. Less common are a variety of parts of different kinds of ferns and seed plants (e.g., leaves with attached sporangia, seeds of cycads, pollen organs of the Caytonia plant), as well as the fragments of bennettitalean reproductive structures described here.
Mesofossils are well preserved and include organs that would not survive standard acid maceration (e.g., fern leaves). Many leaf fragments, as well as many Caytonia cupules, have cuticles with excellent external anatomical details (e.g., hairs, stomata) that are easily studied with scanning electron microscopy. Internal tissues have been transformed into hard black coal often with conchoidal fracture. This preservation is an important difference from Cretaceous mesofloras in which the plant fragments are typically charcoalified or lignified. Nevertheless, in the Grisethorpe mesofossils especially resistant structures (e.g., pollen grains, spores) or membranes (e.g., megaspore membranes, certain internal seed cuticles) are preserved within the coal and can be released by standard acid–alkali maceration. This is the method that has been used most widely for the study of fossils from the Jurassic of Yorkshire (e.g., Harris, 1961, 1964, 1969, 1979; Harris et al., 1974). Here we took a different approach and used scanning electron microscopy to study external surfaces. An important challenge for future studies, as more abundant material becomes available, will be to integrate these two approaches while also developing new and less destructive maceration techniques that allow more delicate internal structures to be studied (see for example the techniques of Thomas, 1925).
BENNETTITALES IN THE GRISETHORPE BED
Based on the compilation of named species from the Grisethorpe Bed by Thomas and Batten (2001), a maximum of about 16 "whole plant species" of Bennettitales are potentially present in the flora (Table 1). Eight are known only from leaves (Table 1, leaf species 3, 7–13). Others are based on more than one organ that have been linked together, with varying degrees of certainty, using different lines of evidence from several localities by Harris (1969). In the case of leaves of Otozamites beanii (Lindley & Hutton) Brongniart, Otozamites gramineus (Phillips) Phillips and Zamites gigas (Lindley & Hutton) Morris the likely corresponding reproductive structures (based on inferences by Harris, 1969) have been identified at other localities in the Jurassic of Yorkshire, but are not known from the Grisethorpe Bed (Table 1, leaf species 5, 6, 16). Ptilophyllum pectinoides (Phillips) Morris has been linked with the pollen-producing structures of Weltrichia whitbiensis (Nathorst) Harris and ovulate reproductive structures of Williamsonia hildae Harris, but only the corresponding stems (Bucklandia pustulosa Harris) are recorded from the Grisethorpe Bed (Table 1, leaf species 15). This species of stem has also been linked with ovulate reproductive structures of Williamsonia leckenbyi Nathorst (discussed later).
Four species of Bennettitales are known from the Grisethorpe Bed based on leaves as well as some of their corresponding reproductive structures (Table 1, leaf species 1, 2, 4, 14). These are referred to here as the Williamsoniella coronata plant, based on bisexual reproductive structures of Williamsoniella coronata Thomas and leaves of Nilssoniopteris vittata (Brongniart) Florin (Table 1, leaf species 4); the Williamsoniella papillosa plant, based on bisexual reproductive structures of Williamsoniella papillosa Cridland and leaves of Nilssoniopteris major (Lindley & Hutton) Florin (Table 1, leaf species 2); the Williamsonia leckenbyi plant, based on ovulate reproductive structures of Williamsonia leckenbyi Nathorst, scale leaves of Cycadolepis nitens Harris, pollen-producing structures of Weltrichia pecten (Leckenby) Halle, leaves of Ptilophyllum pecten (Phillips) Harris (Table 1, leaf species 14) and stems of Bucklandia pustulosa Harris; and the Bennettites diodon plant, based on the ovulate reproductive structures of Bennettites diodon Harris, scale leaves of Cycadolepis stenopus Harris, and leaves of Anomozamites nilssonii (Phillips) Seward (Table 1, leaf species 1).
Leaves of the Williamsoniella coronata plant (Nilssoniopteris vittata) are "abundant" (Harris, 1969), while leaves of the Williamsonia leckenbyi plant (Ptilophyllum pecten) are "locally frequent" (Harris, 1969). Leaves of the Williamsoniella papillosa (Nilssonopteris major) plant are "occasional," and those of the Bennetticarpus diodon plant (Anomozamites nilssonii) are "frequent at certain points" (Harris, 1969). These observations are also consistent with the relative abundance of macrofossils of the corresponding bennettitalean reproductive structures in the Grisethorpe Bed (Harris, 1969). Williamsoniella coronata is described as "frequent" and is represented by numerous specimens. In contrast, Williamsonia leckenbyi is based mainly on specimens from Cloughton Wyke, and the occurrence of the species at Cayton Bay is only mentioned in passing (Harris, 1969). Only one large pollen organ of Williamsoniella papillosa and four ovulate structures of Bennetticarpus diodon are reported from the Grisethorpe Bed. Based on these assessments, fragments of the ovulate structures of Williamsonia coronata are likely to be most abundant among the Grisethorpe Bed mesofossil assemblage. Williamsonia leckenbyi, Williamsoniella papillosa, and Bennetticarpus diodon may also be present, perhaps along with other bennettitalean ovulate structures not yet recorded as macrofossils.
The genus Williamsoniella Thomas
Williamsoniella coronata, the type species of the genus, was first described by Thomas (1915) based largely on material collected from the Grisethorpe Bed at Cayton Bay. Thomas recognized the bisexual organization of the reproductive structure, the ovules, and interseminal scales and how they are borne, and the general form of the pollen-producing organs. He also linked the bisexual structure with leaves of Taeniopteris vittata Brogniart (now Nilssoniopteris vittata) and suggested that both were borne on slender branched stems. Subsequently, Zimmermann (1933) figured a specimen showing a slender branched stem with probable attached reproductive structures and Nilssoniopteris leaves. Harris (1944) clarified the structure of the pollen-producing organs and showed that the flowers were surrounded by scale leaves of the kind now referred to Cycadolepis. A second species of Williamsoniella (W. papillosa) was described by Cridland (1957) and Harris (1969) based largely on three ovulate structures and associated detached pollen-producing organs from the Whitby Plant Bed (see Thomas and Batten, 2001). A single specimen of W. papillosa is known from the Grisethorpe Bed (Harris, 1969). Williamsoniella papillosa is mainly distinguished from W. coronata by its larger size (seed-bearing axis 33 mm long vs. 8 mm; apical projection of the seed-bearing axis 4–7 mm long vs. 2 mm; Harris, 1969).
BENNETTITALES AS MESOFOSSILS IN THE GRISETHORPE BED
Some of the bennettitalean mesofossils can be assigned securely to previously described macrofossils, but the assignment of others is more problematic. Here we focus on material that can be attributed to Williamsoniella coronata, Williamsonia leckenbyi, species of Cycadolepis and Nilssoniopteris vittata, as well as several fragments of ovulate structures that are of uncertain affinity within Bennettitales. The material was collected mainly from part of the exposure where leaves of N. vittata were abundant, although bennettitalean reproductive structures were not observed on any of the blocks collected.
Williamsoniella coronata
Fragments of ovulate structures include a single well-preserved specimen that can be attributed securely to W. coronata based on its size and the distinctive form of the apical projection of the axis that bears the ovules and interseminal scales ("corona"; Fig. 1). The specimen is 6.8 mm long from the tip of the corona to the lowermost interseminal scales. An extrapolation from previously described material indicates that the complete ovulate portion of the bisexual reproductive structure at the time of preservation was probably about 9–10 mm from the tip of the corona to the attachment of the pollen-producing organs. At the apex, the corona forms a short, more or less conical projection 1 mm long and 2.3 mm in diameter. Immediately below are 10–12, more or less rectangular, facets. These facets (only five visible in Fig. 1), arranged in a whorl, were probably formed by the apices of the pollen-producing organs surrounding the corona early in its development (Thomas, 1915). Their number is consistent with the number of pollen-producing organs observed in buds of W. coronata (Thomas, 1915).
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1440 interseminal scales and 250 seeds. The ratio of seeds (judged by micropyles) to interseminal scales is roughly 1:6. The shape of the interseminal scales varies from the base of the specimen toward the apex, but at both levels the interseminal scales and micropyles are not strongly differentiated. Toward the apex, the heads of the interseminal scales have a rounded outline and micropyles can be difficult to recognize (Fig. 2). Toward the base, the heads of the interseminal scales typically have a five- to six-angled outline. At this level, micropyles are more clearly differentiated. In both cases, the interseminal scales are 120–180 µm in diameter, while the micropyles are smaller, typically 100 µm in diameter. Especially in the upper part of the ovulate structure, the heads of the interseminal scales often have a small depression in the center (Fig. 4) sometimes surrounded by a ring of tissue (Fig. 5).
Scattered on the surface of the ovulate structure are common, small, psilate, apparently monocolpate pollen grains (Figs. 4, 6, 7). Each is 45–50 µm in maximum dimension. Frequently, they are located in the grooves that separate adjacent interseminal scales and micropyles. No pollen grains have been observed on top of, or within, the micropyles.
Pollen grains have not previously been observed on the surface of the "gynoecium" of W. coronata. These grains are all of the same kind and sufficiently common that we think it unlikely that they are derived accidentally from an unrelated plant. However, they are larger than the pollen described previously from W. coronata, and additional material will be needed to determine conclusively that they were produced by Williamsoniella pollen organs.
Probable Williamsoniella coronata
In addition to the specimen referred to as W. coronata, other fragments of ovulate structures (Figs. 8–10) also show facets on the lower portion of the corona (Fig. 10), but there is no conical projection at the apex (Figs. 8–10). In these specimens, differentiation between ovules and interseminal scales is more pronounced. Interseminal scales are flat-topped, angular in outline, and separated by distinct grooves. They range in shape from elongate (130–270 µm) to more or less isodiametric (174–195 µm), but they are only slightly larger than the interseminal scales in the more complete, presumed immature, specimen (Figs. 2, 3; 174–195 µm vs. 140–180 µm). Micropyles are of similar size to those in the presumed immature specimen, but they protrude well above the heads of the interseminal scales (Fig. 14) and are much more pronounced (Figs. 12, 13). Despite a careful search, no pollen grains were observed either in any of the micropyles or on the surface of these fragments.
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, text, figs. 2, 17) and Harris (1944, fig. 4B). Interseminal scales of both "immature" and "mature specimens" do not differ greatly in size, suggesting that at this stage of development maturation of the ovulate structure resulted from tissue differentiation rather than tissue expansion. "Mature specimens" have a corona in which the number of facets and their size is similar to that of "immature specimens," but in these cases the corona has a flat top. Thomas (1915, p. 124) notes that in some specimens the apical projection (Fig. 1) "though present, is not quite so well defined."
Williamsonia leckenbyi Nathorst
Several specimens were recovered (Fig. 11) that are similar to the corona of Williamsonia leckenbyi figured by Harris (1969, fig. 58A). Each is 2.4–3.2 mm in diameter, and the facets are both more slender (typically 470–560 µm) and more numerous (typically 16–17 µm) than in Williamsoniella coronata. In these unisexual reproductive structures, the facets were presumably formed by the scale leaves rather than by pollen-producing organs. Proximally, very little of the "gynoecium" is preserved, but a few flat-topped interseminal scales are clearly present. The most distinctive feature of these coronas is their strongly concave, warty apex. In Williamsoniella coronata, the corona is smooth and either conical or shallowly concave. The facets are also more rectangular.
Other fragments of bennettitalean ovulate structures
A few fragments of bennettitalean ovulate reproductive structures were recovered that appear to be more mature specimens (Figs. 15–19). They are similar to material illustrated and attributed to Williamsoniella coronata by Harris (1944, fig. 4D; compare with Fig. 15), but because our material is fragmentary we are not confident that it can be assigned to that species. We leave open the possibility that these pieces are fragments of mature specimens, perhaps even from more than one species given their differences (compare Figs. 15, 19).
In one specimen (Fig. 18), the interseminal scales (800–1000 µm in maximum dimension) have a papillate surface and come to an obtuse-pointed apex. The micropyle of the corresponding ovules is very long (Fig. 19). In another specimen (Fig. 15), the center of each interseminal scale is elongated into a very pronounced and central "boss" up to 330 µm long, which is very distinctive and shiny under light microscopy. Some of these bosses show stomata on their flanks (Fig. 17). The interseminal scales are strongly angular in outline and 460–555 µm in maximum dimension. The corresponding micropyles are very elongated, up to 460 µm long.
Pollen-producing organs of Williamsoniella coronata
A few fragments of pollen-producing organs were recovered from the mesofossil assemblage. Usually, these are the distal portions of what Thomas (1915) and Harris (1944, 1969) termed microsporophylls, but whether these structures are leaf homologs in Bennettitales is not certain. They are recognizable by their shape and size, but also by their characteristic "pimply" surface (fig. 22) (Harris, 1969). A single pollen-producing organ is more complete and is preserved as a flattened, largely cuticular, compression (Figs. 20, 21). This specimen (Figs. 20, 21) shows the distinctive lobes first described by Harris (1944) and also two elongated, presumed synangia. Like many of the pollen-producing organs described by Thomas (1915) and Harris (1944), the synangia appear immature. Their bivalved construction and their internal septae are not visible. There are also no pollen grains associated with the specimen.
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, fig. 2D–I). However, in view of the fact that four different kinds of bennettitalean reproductive structures are known from the Grisethorpe Bed (Table 1), we refrain from assigning them to particular "whole plant" species. The scale leaves vary considerably in size and shape. Frequently, they have trichomes on the margin and the presumed outer (abaxial) surface.
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, in fig. 22 caption) described similar "bract-like structures" bearing "a much reduced lamina of the Taeniopteris vittata type" on a hand specimen of Williamsoniella coronata.
Associated Nilssoniopteris vittata leaves
Leaves of Nilssoniopteris vittata are abundant among the macrofossils from the Grisethorpe Bed and were common on the many blocks from which the mesofossils were recovered. In the mesofossil assemblage large fragments of leaf lamina attached to the midrib, and numerous distinctive leaf apices, are also common. As noted by Thomas (1915), leaf apices are typically retuse (Figs. 32, 33) but with a small apical projection formed by the slightly extended pointed tip of the midrib (Fig. 34). The leaf lamina is more or less continuous over the adaxial surface of the midrib (Fig. 32). On the abaxial surface, the midrib is much more prominent (Fig. 36). Small, perhaps less well-developed leaves have numerous papillae on the abaxial leaf surface, both over the midrib and on the lamina (Fig. 35). The papillae are much more sparse in larger, perhaps more mature leaves (Fig. 37) and are sometimes ruptured (compare Figs. 38–40).
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Advantages and disadvantages of the mesofossil approach
Mesofossils recovered from a relatively well-understood macrofossil flora, such as that from the Grisethorpe Bed, often yield specimens that improve documentation and understanding of larger structures. For example, new information on ovules and interseminal scales at what appear to be different stages of maturity extend the information gleaned previously from macrofossils. But on the other hand, mesofossils can be difficult to assign to species recognized based on macrofossils, and it may not be possible to retrieve key aspects of structure that can only be seen in larger specimens. For example, it would have been impossible, based on the mesofossils discovered so far, to recognize the bisexual construction of Williamsoniella coronata. The mesofossil approach is therefore a useful supplementary technique for the study of suitably preserved fossil floras that can provide valuable information complementary to that derived from macrofossils.
Pollination and dispersal biology
Mesofossils recovered from the Grisethorpe Bed provide further evidence of certain aspects of reproductive biology in Bennettitales inferred from previous studies. Based on macrofossils of Williamsoniella coronata of different sizes in which interseminal scales and ovules were developed to different extents, Harris (1944) inferred a developmental series for the "flowers" in which he recognized six stages (summarized in Table 2). The most complete mesofossil specimen (Fig. 1) corresponds to a stage 2 ovulate structure in which both interseminal scales and micropyles are visible, but the interseminal scales have rounded heads and the micropyles do not project. The fragments with more mature interseminal scales (Figs. 10–12) were probably from an ovulate structure at stage 3.
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in Williamsoniella coronata (Table 2) is the apparently weak developmental integration among the different parts of the bisexual reproductive structure. For example, the scale leaves may be either shed or retained at both relatively early and relatively late stages of floral development (Table 2), whereas in a typical angiosperm flower the perianth is retained at least until anthesis. This observation suggests that the scale leaves may have had more to do with protection during early development than attraction for pollinators. Similarly, while the pollen-producing structures enclose (and may protect) the developing ovules and interseminal scales in bud (see Thomas, 1915, figs. 9, 10; Harris, 1944, fig. 9) and are always shed at a relatively early stage before the ovules and interseminal scales reach maturity (Harris, 1944), very often the pollen is immature and retained within the pollen sacs (Harris, 1944). Early dropping of the pollen organs is also consistent with observations of bisexual flowers of Cycadeoidea in which specimens that have well-preserved pollen-producing structures have poorly differentiated ovules and interseminal scales (Crepet, 1972).
Based on the observations of Harris (1944) and also on the differences in the development of interseminal scales and micropyles on different mesofossil fragments, it seems that within a single flower maturation of the ovules followed early shedding of the pollen-producing organs. Judged from the development of more prominent micropyles, the ovules became receptive only at this later stage. By analogy with extant gymnosperms, each may have produced a pollination drop. However, it is interesting that we did not observe pollen grains in any of the micropyles (as has been possible in other fossil seed plants using SEM, e.g., Rydin et al., 2006). Harris (1944) also failed to find pollen in any of the preparations he made using acid–alkali maceration even though they are "easy to find in various other Bennettitalean seeds" (Harris, 1944, p. 325). Based on studies of permineralized Williamsonia, Stockey and Rothwell (2003, p. 260) suggest that "pollination brought grains into only the distal-most part of the micropylar canal in most Bennettitales" and that this may have been followed by invasive growth of the pollen tubes into the interior of the ovule. This and other possibilities for the mechanism of pollination in Bennettitales need further study.
A striking feature of the mesofossil assemblage from the Grisethorpe Bed is the absence of dispersed bennettitalean seeds. As recognized by Harris (1944), this absence is strange considering the potentially large number of seeds produced by each ovulate structure and that plant parts that are presumed to be much more delicate (e.g., fragments of fern leaf with attached sporangia) are frequently encountered. Dispersed seeds of the Caytonia plant are also extremely abundant.
Summarizing the evidence from previous work (Thomas, 1915; Harris, 1944), as well as the evidence from mesofossils, it appears that the developing bisexual reproductive structure of Williamsonia coronata was protected initially by Cycadolepis scale leaves that were then shed or persisted in an irregular way during the rest of development (see specimens figured by Thomas, 1915; Harris, 1944). Subsequently, protection of the developing ovulate structure may have been afforded by the surrounding tightly packed pollen-producing organs, which may also have been involved in the attraction of pollinators. Maturation and shedding of pollen probably took place before receptivity of the ovules, but in many cases, pollen organs were shed precociously before the pollen matured. For the bisexual reproductive structure as a whole, maturation of the different organs seems to have taken place in acropetal order, but in general, development seems much less well coordinated than in a typical angiosperm flower (Harris, 1944).
Structural and phylogenetic considerations
The similarity in shape, size, and texture of the apices of the interseminal scales and micropyles, especially in the less well-developed parts of the ovulate structure (Figs. 2, 3) suggests similar early development and is consistent with the interpretation that the interseminal scales are aborted ovules (Thomas, 1915). This has also been inferred from other studies of bennettitalean ovulate reproductive structures (e.g., Harris, 1932; Crane, 1988; Pedersen et al., 1989) and is also supported by similarities in the vascular supply to ovules and interseminal scales in permineralized bennettitalean ovulate reproductive structures (Rothwell and Stockey, 2002). Seemingly delayed growth in the center of some interseminal scales was noted by Thomas (1915), and this is further supported by our SEM observations of interseminal scales that show a distinct ring of tissue surrounding a depression (Fig. 5). Consistent with Thomas’ inference, it seems likely that the outer layers of the interseminal scales formed first, perhaps from a ring of tissue, while growth in the center was retarded. The slight differences in the form of the interseminal scales in the upper and lower part of the "gynoecium" are consistent with the suggestion of Thomas (1915) that the ovules may have matured in acropetal succession.
Ovules of Bennettitales have usually been interpreted as having the nucellus surrounded by a single integument (e.g., Lignier, 1894; Stopes, 1918; Watson and Sincock, 1992; Rothwell and Stockey, 2002; Stockey and Rothwell, 2003). Recently, the previously discussed possibility (Solms-Laubach, 1891; Berridge, 1911) that the Bennettitales have the nucellus surrounded by two layers (an inner, true, integument, and an outer envelope) have been revived (Friis et al., 2007, 2009, pp. 252–283 in this issue). Under this interpretation, the interseminal scales may be ovules in which the outer envelope is relatively well-developed but in which growth of both the nucellus and integument is retarded. There is also an interesting resemblance between the four-angled, wrinkled interseminal scales seen in some mesofossil specimens (Fig. 18) and the form of some seeds attributed to the Bennettitales-Erdtmanithecales-Gnetales group (see Friis et al., 2009, pp. 252–283).
Recognition of two coverings around the nucellus in bennettitalean ovules (Friis et al., 2009, pp. 252–283) also raises questions about whether the structures described here as micropyles (e.g., Figs. 2–4, 13) are true micropyles formed by the integument or are formed by the outer envelope. In many of the presumed youngest micropyles, the ovule tip appears more complicated than a single layer (Figs. 2–4), but at the stage where the micropylar tips are prominent, they seem to be a single structure (Fig. 13). Whether this robust tube is formed by the envelope or the integument is not clear from our material. Further research is needed to determine exactly how these ovules and the complex reproductive structures of which they are part should be compared with the diversity of reproductive structures in other extinct seed plants.
FOOTNOTES
1 The authors thank E. M. Friis and two anonymous reviewers for helpful comments on the manuscript. P.R.C. is also grateful to H. van Konijnenburg-van Cittert for advice concerning the Yorkshire Jurassic flora. 
4 Author for correspondence (e-mail: p.crane{at}geosci.uchicago.edu)
LITERATURE CITED
Berridge, E. M. 1911. On some points of resemblance between Gnetalean and Bennettitalean seeds. New Phytologist 10: 140–144.[CrossRef]
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]
Crane, P. R. 1988. Major clades and relationships in the "higher" gymnosperms. In C. B. Beck [ed.], Origin and evolution of gymnosperms, 218–272. Columbia University Press, New York, New York, USA.
Crane, P. R., P. S. Herendeen, AND E. M. Friis. 2004. Fossils and plant phylogeny. American Journal of Botany 91: 1683–1699.
Crepet, W. L. 1972. Investigations of North American cycadeoids: Pollination mechanisms in Cycadeoidea. American Journal of Botany 59: 1048–1056.[CrossRef][Web of Science]
Cridland, A. A. 1957. Williamsoniella papillosa, a new species of bennettitalean flower. Annals and Magazine of Natural History, series 12, 10: 383–388.
Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133: 169–209.
Friis, E. M., P. R. Crane, K. R. Pedersen, S. Bengston, P. C. J. Donoghue, G. W. Grimm, AND M. Stapanoni. 2007. Phase-contrast X-ray microtomography links Cretaceous seeds with Gnetales and Bennettitales. Nature 450: 549–551.[CrossRef][Web of Science][Medline]
Friis, E. M., K. R. Pedersen, AND P. R. Crane. 2006. Cretaceous angiosperm flowers: Innovation and evolution in plant reproduction. Paleogeography, Paleoclimatology, Paleoecology 232: 251–293.[CrossRef]
Friis, E. M., K. R. Pedersen, AND P. R. Crane. 2009. Early Cretaceous mesofossils from Portugal and eastern North America related to the Bennettitales-Erdtmanithecales-Gnetales group. American Journal of Botany 96: 252–283.
Harris, T. M. 1932. The fossil flora of Scoresby Sound, East Greenland, part 3, Caytoniales and Bennettitales. Meddelelser om Grønland 85: 1–133.
Harris, T. M. 1944. A revision of Williamsoniella. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 231: 39–328, plates 25, 26.
Harris, T. M. 1961. The Yorkshire Jurassic flora. I. Thallophyta-Pteridophyta. British Museum (Natural History), London, UK.
Harris, T. M. 1964. The Yorkshire Jurassic flora. II. Caytoniales, Cycadales and pteridosperms. British Museum (Natural History), London, UK.
Harris, T. M. 1969. The Yorkshire Jurassic flora. III. Bennettitales. British Museum (Natural History), London, UK.
Harris, T. M. 1979. The Yorkshire Jurassic flora. V. Coniferales. British Museum (Natural History), London, UK.
Harris, T. M., W. Millington, AND J. Miller. 1974. The Yorkshire Jurassic flora. IV. British Museum (Natural History), London, UK.
Herendeen, P. S., S. Magallón-Puebla, R. Lupia, P. R. Crane, AND J. Kobylinskya. 1999. A preliminary conspectus of the Allon flora from the Late Cretaceous (late Santonian) of central Georgia, U.S.A. Annals of the Missouri Botanical Garden 86: 407–471.[CrossRef][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.
Lignier, O. 1894. Structure et affinités du Bennettites morierei Sap. & Mar. (sp.). E. Lanier, Caen, France.
Livera, S. E., AND M. R. Leeder. 1981. The Middle Jurassic Ravenscar Group (‘Deltaic Series’) of Yorkshire: Recent sedimentological studies as demonstrated during a field meeting, 2–3 May 1980. Proceedings of the Geologists’ Association 92: 241–250.
Pedersen, K. R., P. R. Crane, AND E. M. Friis. 1989. Morphology and phylogenetic significance of Vardekloeftia Harris (Bennettitales). Review of Palaeobotany and Palynology 60: 7–24.[CrossRef][Web of Science]
Rothwell, G. W., AND R. A. Stockey. 2002. Anatomically preserved Cycadeoidea (Cycadeoidaceae), with a reevaluation of systematic characters for the seed cones of Bennettitales. American Journal of Botany 89: 1447–1458.
Rydin, C., K. R. Pedersen, P. R. Crane, AND E. M. Friis. 2006. Former diversity of Ephedra (Gnetales): Evidence from Early Cretaceous seeds from Portugal and North America. Annals of Botany 98: 123–140.
Solms-Laubach, H. 1891. On the fructification of Bennettites gibsonianus, Carr. Annals of Botany 5: 419–454.
Stockey, R. A., AND G. W. Rothwell. 2003. Anatomically preserved Williamsonia (Williamsoniaceae): Evidence for bennettitalean reproduction in the Late Cretaceous of western North America. International Journal of Plant Sciences 164: 251–262.[CrossRef][Web of Science]
Stopes, M. C. 1918. New bennettitean cones from the British Cretaceous. Philosophical Transactions of the Royal Society, B, Biological Sciences 208: 389–440.[CrossRef]
Thomas, B. A., AND D. J. Batten. 2001. The Jurassic palaeobotany of Yorkshire. In C. J. Cleal, B. A. Thomas, D. J. Batten, and M. E. Collinson [eds.], Mesozoic and Tertiary palaeobotany of Great Britain, 29–96. Joint Nature Conservation Committee, Peterborough, UK.
Thomas, H. H. 1915. On Williamsoniella, a new type of bennettitalean flower. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 207: 113–148, pl. 12–14.[CrossRef]
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, Biological Sciences 213: 299–363.[CrossRef]
van Konijnenburg-van Cittert, J. H. A., AND H. S. Morgans. 1999. The Jurassic flora of Yorkshire. Palaeontological Association, London, UK.
Watson, J., AND C. A. Sincock. 1992. Bennettitales of the English Wealden. Palaeontographical Society, London, UK.
Zimmerman, W. 1933. Paläobotanische und phylogenetische Beiträge, I–V. Palaeobiologica, Wien 5: 321–348.
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