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Paleobotany |
2Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 USA; 3Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Xiangshan, Beijing 100093, People's Republic of China
Received for publication September 2, 2003. Accepted for publication April 13, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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Key Words: China • Eocene • fossil • North Dakota • Nuphar • Nymphaeaceae • seed
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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). Assessments of phylogeny of extant angiosperm taxa based on sequence data from multiple genes indicate that the Nymphaeales reside in a group that diverged early from most other angiosperms (Qiu et al., 1999
, 2000
; Soltis et al., 1999). The fossil record of Nymphaeales has been traced at least back to the Late Cretaceous based on Paleovictoria flowers from the Turonian, ca. 90 million years ago (mya), of New Jersey (Gandofo et al., 2004
). There are suggestions from the paleobotanical record that the order may be traced to the Early Cretaceous. Although Friis et al. (2001)
attributed a flower from the Barremian or Aptian (125–115 mya) of western Portugal to Nymphaeales, Gandolfo et al. (2004)
challenged the assignment, noting that the characters of the flower are also consistent with Illiciales. Seeds with testa similar to extant Nymphaeales are also found in the same locality in western Portugal, but as noted by Friis et al. (1999)
seeds of Illiciales may also have similar testa, and the characteristic micropyle-hilum complex unique to seeds of Nymphaeales were found in only one specimen that was not illustrated. By the Tertiary, Nymphaeales were widely distributed in the Northern Hemisphere based upon fossil seeds (Dorofeev, 1973
, 1974
; Collinson, 1980
; Mai, 1988
; Cevallos-Ferriz and Stockey, 1989
) including both extinct and extant genera.
There remain many gaps in the fossil record of Nymphaeales, both geographically and stratigraphically. Whereas some of the modern genera, e.g., Brasenia, have been confirmed back to the Middle Eocene (Collinson, 1980
), other extant genera have been traced only to the Neogene as in the case of Euryale (Miki, 1960
). Extinct genera of nymphaealean affinity are known from the Eocene based on fossil seeds (Dorofeev, 1973
, 1974
; Cevallos-Ferriz and Stockey, 1989
). Here we provide evidence for recognition of the extant genus Nuphar in the Early Eocene of eastern China.
The newly recovered fossil seeds are from the Wutu Basin, about 170 km east of Jinan, the capital of Shandong Province, China. Although fossil plants have not previously been described from Wutu, mammalian remains have been known from the coal mines of this basin for four decades (Chow and Li, 1963
) and have been studied extensively. Based on the mammal fossils, the Wutu Formation is considered to be Early Eocene (Tong and Wang, 1998
). Although some authors suggest the age of the formation is Late Paleocene, most paleontologists accept the Early Eocene assignment (Bloch et al., 2001
).
In this article, we document anatomically preserved seeds of Nymphaeaceae from a coal mine of the Wutu Basin. These are the first permineralized seeds to be described from the Tertiary of China. We compare the fossil with other known fossil and living genera of Nymphaeaceae and demonstrate their affinities with the modern genus, Nuphar. This occurrence extends the record of this extant genus back to about 52 my. In addition, we report a similar specimen from the Paleocene of Almont, North Dakota, USA. Based on these records, and previously reported occurrences, we review the fossil record of the genus and implications for the phytogeographic history of the genus.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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Fossil seeds buried partially in the black shale or loosened from the shale were observed and described with the aid of a stereo microscope (Fig. 1A, B). Seeds showing different layers of surface cells were chosen for scanning electron microscopy (SEM). A thin transverse section of a seed with intact cuticle was made after SEM to reveal the anatomy of seed coat by transmitted light microscopy. Modern nymphaeaceous seeds were provided by the herbarium in Academia Sinica, Beijing (Nuphar japonica DC. and N. lutea (L.) Sm.), and by Dr. Donald Padgett (N. advena (Ait.) Ait.f. subsp. advena, N. advena (Ait.) Ait.f. subsp. orbiculata (Small) Padgett, N. microphylla (Pers.) Fern., N. pumila (Timm) DC. subsp. pumila, N. polysepala Engelm., N. variegate Durand). The modern Nuphar seeds were fractured to reveal internal anatomy by SEM.
Morphological and anatomical characters of nymphaealean seeds are useful in segregating each of the modern genera (Fig. 2) and thus have excellent application for the generic determination of fossil remains. We consulted prior surveys of nymphaealean seed morphology, e.g., Miki (1960)
, Dorofeev (1974)
, Collinson (1980)
, and Yamada et al. (2001)
. We use the same descriptive terminology as Collinson (1980)
.
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SYSTEMATICS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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Genus
Nuphar J. E. Smith, in Sibth & Smith
Section
Nupharella Dorofeev
Nuphar wutuensis sp. nov.
Holotype
PEPB54164.
Paratypes
PEPB54163, 54164, 54165, 54166, 54167, 54168, 54169-b, 54170; UF18953–38054, 38055, 38056.
Description
Seeds ellipsoidal to ovoid, 4–5 mm in length, 3–4 mm in width. Raphe ridge clearly visible externally. Smooth and globose, rounded at basal end, apex truncate with a circular cap 0.8–1 mm in diameter bearing a central micropylar protrusion. The raphe forms a prominent ridge on one side, the cap is in a plane oriented about 20°–45° from the long axis of the seed, dipping toward the raphe. The surface is covered by an outermost opaque layer without cellular detail, approximately 20–30 µm thick, underlain by a uniseriate layer of equiaxial pentagonal to hexagonal surface cells, and an inner layer 4–6 cells thick composed of thick-walled, periclinally elongate sclereids. The surface cells are pentagonal to polygonal and equiaxial without undulating or digitating. The lumens of the surface cells appear triangular when the seed is thin-cross-sectioned, approximately 20–30 µm high and 20–30 µm wide. The cell lumens of the inner sclereids are about the same height as those of the surface cells, and their width can be up to five times greater than their height (Fig. 3E).
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The thick black surface layer mentioned above appears to be coalified, and its original structure is not clear. We considered that it might represent a very thick cuticle; however, it is much thicker than the cuticle observed on modern nymphaeaceous seeds, and more generally, thicker than most plant cuticles known to be deposited in nature. Comparing these fossils with anatomically preserved seeds assigned to Nuphar section Nupharella by Dorofeev (1974)
, this thick layer corresponds in position to the highly thickened outer periclinal walls of the outer seed coat. Some of Dorofeev's specimens, which are compressed, but not coalified or permineralized, clearly show the structure of the cells comprising this layer (Dorofeev, 1974
: Plate 112, 5–11). In his specimens, each cell of the uniseriate sclerotesta has a cell wall that is of normal thickness—as thick as the wall of the cells of the inner testa—in the lower periclinal and anticlinal walls, but which becomes highly thickened apically such that the distal parts of the anticlinal walls, and the upper periclinal walls, are more than 10 times thicker than the proximal walls. Similar kinds of differentially thickened sclerotesta cells occur in Brasenia, Victoria, and some species of Nymphaea (Collinson, 1980
). Dorofeev also mentioned that in some of his specimens the outer periclinal walls of the sclerotesta are fused into a uniform mass without the visible boundaries of the cells, just like the condition of the Wutu seeds. Unable to confirm the composition of this thick black outermost layer of the Wutu seeds, we refer to this layer as the cuticle/outer periclinal wall. Presumably this outer portion of the surface layer was impermeable so that it was not permineralized, only coalified, when mineralizing fluids entered the micropylar opening.
The cap in this fossil is flat and with a circular outline, usually with a central protrusion where the micropyle is located. There is no depression surrounding the cap. The cuticle/ outer periclinal wall is thin on the edge of the cap. When cuticle is lost, the cap appears to be a disc-like structure 4–5 surface cells thick showing the impression of the surface cells. This is the infilling of the space that was under the cap, showing the arrangement of the cells that lined the testa. The surface cells of the testa in the cap region are hexagonal, tangentially elongate, and arranged uniformly (Fig. 1H).
The prominent raphe ridge runs longitudinally along one side of the seed and terminates at the margin of the cap (Fig. 1C). The canal of the raphe is clearly seen in the transverse section of the seed (Fig. 3A, B). Usually the surface of the seed from the central micropyle to the raphe is somewhat raised, and the cuticle/outer periclinal wall in this region is always retained (Fig. 1E, F, G, H). The hilum is inferred to have been located in this region because no other place shows any break on the smooth seed surface. However, detail of the hilum shape and size are not well preserved.
We found that there are important differences in the appearance of the "surface" of the seed, depending on which layers have been removed. The surface observed on modern seeds is generally the outer seed coat but in fossils the exposed surface is in some cases actually the internal cast of the seed coat, representing one of three or four different possible levels. Although our specimens show a pattern of isodiametric cells at the outer surface (Fig. 1J, L), the underlying layers are composed of elongate digitate cells (Fig. 1M, N). If the true outer layer were lost by abrasion or in the initial fracture in which a fossil seed is exposed, the exposed surface would not be homologous with the outer surface of a modern seed.
As we were finalizing our investigation of the Wutu fossil seeds, we discovered a remarkably similar specimen from the Paleocene of Almont, North Dakota (see Crane et al., 1990 for locality data). Although the cuticle/outer periclinal wall is not preserved well on this silicified specimen, the morphology and anatomy (Fig. 4) closely match those of Nuphar wutuensis, indicating that the genus, and perhaps the same species, extended back to the Tiffanian stage of the Paleocene.
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Seed morphology and anatomy of extant genera and several fossil taxa has been surveyed by light microscopy (Miki, 1960
; Dorofeev, 1973
, 1974
) and scanning electron microscopy (Collinson, 1980
; Yamada et al., 2001
). The most important characters for distinguishing genera are position of the hilum in relation to the cap and micropyle and shape of the surface cells of the seed coat. The differences of hilum position in mature seeds reflect differences in ovule development (Yamada et al., 2001
): ovules of Cabombaceae have a hood-shaped outer integument, whereas those of Nymphaeaceae typically have a cup-shaped outer integument.
Figure 2 shows selected morphological and anatomical characters of seeds of extant nymphaealean genera. The seeds from Wutu conform to the genus Nuphar in their size, position of the micropyle on the cap, and the surface of isodiametric cells. Seeds of Victoria, Nymphaea, Barclaya, and Odinea have testa cells that are elongate and have undulating margins such that adjacent cells interdigitate, whereas Euryale and Nuphar have testa cells that are isodiametric in surface view with smooth margins (Collinson, 1980
). The seeds from Wutu are very similar to extant Nuphar spp. in the anatomy of the testa. Seeds of different genera are also segregated by size. Whereas those of Nymphaea (up to 3 mm long) and Ondinea (up to 1.5 mm) are small, those of Euryale and Victoria are large (exceeding 6 mm). The Wutu seeds, being 4–5 mm long, conform to the size range of extant species of Nuphar.
In Nymphaeales, only Euryale and Nuphar have a clearly visible raphe ridge. In Euryale, the hilum is located outside of the cap, but in Nuphar the hilum is inside the cap (Miki, 1960
; Yamada et al., 2001
). These two genera are also distinguished anatomically, the inner layer in the testa could be more than 20 cells thick in Euryale, but in Nuphar it is only 3–5 cells thick. Miki (1960)
noted that Euryale and Nuphar both have a depression that encircles the cap, which is not present in Nymphaea. However, the presence and strength of the apical depression varies among and within Nuphar species, leading us to question the utility of this character for generic distinction. Although Nuphar microphylla has a pronounced depression, N. japonica almost has no depression and the depression in N. lutea is only slight. Hence, the lack of such a depression in the Wutu fossil does not exclude it from Nuphar.
Diagnostic characters of the Wutu fossil, including seed size, a prominent raphe ridge, hilum inside the cap, and 4–6 seriate sclerenchymatous layers in testa, support the identification of these fossils to the genus Nuphar. Nevertheless, Nuphar wutuensis is distinguished from the modern species we have examined in shape of the seed, shape of the cell lumen of the surface cells, and the extremely thick cuticle/outer periclinal wall of the surface cells. Modern Nuphar seeds are pear-shaped with the cap transverse to the long axis and on the top of the center; N. wutuensis is more elliptic, sometimes curved, with the cap slightly slanted toward the raphe. The shape of the lumen of the surface cells of the seven extant Nuphar species examined here is columnar to cuboid (Fig. 3G, H); that of Wutu seeds is droplet-shaped (Fig. 3D, E, F). The cuticle of modern Nuphar examined here is not thick, and the outer periclinal wall of the surface cells is typically not thicker or only slightly thicker than the inner periclinal wall and anticlinal walls.
Based exclusively on characters of seed morphology and anatomy, Dorofeev (1974)
separated Nuphar into two sections: sections Nupharella and Nuphar. Whereas sect. Nuphar includes both modern and fossil species, he recognized sect. Nupharella only from fossil representatives, principally from the early and middle Tertiary (Dorofeev, 1974
; Friis, 1985
). The main differences between the two sections are in the shape and position of the hilum and the morphology of cells making up the outer layer of the seed coat: in sect. Nuphar the hilum is circular and placed within the cap near the micropyle and the outer testa cells are cuboidal with outer tangential walls not especially thickened, whereas in sect. Nupharella, the hilum is elongate, placed partly on the cap and partly below; and the outer testa cells are columnar with thick cuticle/outer periclinal walls. The Wutu seeds have an elongate hilum placed inside a circular cap, and the cuticle/outer periclinal wall of the surface cells is thick (about equal in thickness to the width of the cell lumen), but the cells are cuboidal rather than columnar. The extant Nuphar seeds that we examined have a relatively thin cuticle/outer periclinal wall; if the outer wall is thickened it is never thicker than one-fourth of the width of the cell lumen. In addition, the shape of cell lumens of the surface cells in sect. Nupharella tends to be droplet-shaped and not cuboid or rectangular. If the lumen shape and thick outer periclinal wall of the surface cells is the delimitation for sect. Nupharella, seeds from Wutu clearly belong to sect. Nupharella.
Characters that distinguish sect. Nupharella from sect. Nuphar could alternatively be viewed as potentially distinguishing the taxon as a distinct genus from Nuphar because similar differences have been used to distinguish Paleoeuryale and Pseudoeuryale from the extant monotypic genus Euryale. Of the eight extant species of Nuphar currently recognized by Padgett (1999)
, seven have been studied as to seed morphology and anatomy. We have not examined all of the extant subspecies, but in all the modern Nuphar seeds examined, none has the features of sect. Nupharella. Promoting section Nupharella to the rank of genus seems reasonable because fossil seeds can be easily distinguished from modern ones. However, one should bear in mind that ranking for an extinct taxon based on characters of a single organ, not the characters of the whole plant, may not reflect the true phylogeny.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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described nine extinct species of Nuphar seeds, and Nuphar wutuensis meets the delimitation of his section Nupharella. Assigning them under the same generic name has the advantage of keeping track of related fossil records. Among the nine Nuphar species Dorofeev described, Nuphar wutuensis most closely resembles N. tomskiana, especially in possessing the thick black surface layer and triangular surface cell lumens (Dorofeev, 1974: p. 75–76; plate 111, 7–9).
A recent phylogenetic study in Nymphaeales strongly supports the division of Nymphaeales into two families: Cabombaceae, which includes Cabomba and Brasenia, and Nymphaeaceae, which includes the rest of the genera. Nuphar is the most basal group in Nymphaeaceae, with Victoria and Euryale forming a more derived monophyletic group (Les et al., 1999
). The floral and seed remains attributed to Nymphaeales from the early Cretaceous of West Portugal (Friis et al., 1999
, 2001
) would provides a minimum age of about 115 my for the evolution of the Nymphaeales. These records require confirmation, however, because they have not been clearly distinguished from Illiciales (Gandolfo et al., in press
). The oldest unequivocal record of the order is that of the nymphaeaceous flower Microvictoria from the Crossman Clay Pit locality of the Raritan Formation (Turonian, approximately 90 my, earliest Upper Cretaceous) in Sayreville, New Jersey, United States (Gandolfo et al., in press
). The placement of Microvictoria in Nyphaeaceae implies the two families Cabombaceae and Nymphaeaceae were resoved by that time; recognition of Nuphar seeds in the late Paleocene of North America and early Eocene of Asia, together with the prior recognition of Eocene Brasenia seeds (Dorofeev, 1973
, 1974
; Collinson, 1980
), provide even more substantial evidence that the two families were distinct by the early Tertiary.
Fossil seed investigations have played an important role in revealing the fossil history of the Nymphaeales, and it is clear that the order was more diverse during the Tertiary, at least in aspects of seed morphology, than it is today. Besides the eight extant genera, 14 extinct genera, from Paleocene to Pleistocene, have been assigned to Nymphaeales based on the morphology of fossil seeds: Allenbya, Barclayopsis, Braseniella, Dusembaya, Eoeuryale, Irtyshenia, Nikitinella, Palaeoeuryale, Palaeonymphaea, Protobarclaya, Pseudoeuryale, Sabrenia, Tavdenia, and Tomskiella. Dusembaya and Barseniella are similar to Brasenia and are placed in the Cabombaceae (Dorofeev, 1973
). Protobarclaya and Barclayopsis have been considered to be problematic (Mai, 1988
; Cevallos-Ferriz and Stockey, 1989
). All of these extinct genera have seeds either intermediate between those of the two extant genera or similar to one of the extant genera but different in some aspects.
Among the extinct genera, Irtyshenia is very similar to Nuphar. Polyhedral to hexagonal surface cells and hilum located on the edge of the cap are their shared characters. However, anatomy of the testa is different between the two genera. Interestingly enough, the two species assigned to Irtyshenia have slightly different testa anatomy too (Mai, 1988
). Tavdenia, Nikitinella, and Tomskiella have rectangular surface cells and a cap with separate micropyle and hilum; these are characters similar to Nuphar. However, their testa are more similar to Nymphaea or Victoria. Eoeuryale, Pseudoeuryale, and Palaeoeuryale also have polyhedral surface cells and a hilum near the edge of the cap, but their thick multicellular parenchyma layers make them look more like Euryale.
The taxonomy of extant Nuphar at the species level is troublesome partly due to the occurrence of hybridization between species (Padgett et al., 1999
). Depending on the authority, 15– 25 taxa are recognized at the rank of species. Recent phylogenetic analyses based on morphology, chloroplast DNA, and nuclear ribosomal DNA of 13 species (excluding two hybrids) support the recognition of two major lineages within Nuphar (Padgett et al., 1999
): One of the lineages is confined to the New World while the other (with the exception of a single species of boreal North America) is restricted to the Old World. Morphological characters supporting this distinction include fruits with much more elongated necks ("styles" of some authors) and correspondingly narrower stigmatic disks in the Old World group than in the New World group. Also, the Old World taxa have five sepals per flower and short anthers supported by relatively long filaments, whereas the New World representatives have more sepals per flower, more elongate anthers and shorter filaments. However, seed characters to support this distinction were not observed (Padgett et al., 1999
). Our preliminary observation on modern Nuphar seeds also shows that their characters of seed coat anatomy do not distinguish to the species level.
The Early Eocene occurrence of Nuphar wutuensis provides the oldest documentation of the genus for Asia. The oldest occurrence of the genus currently known is a specimen of N. cf. wutuensis from the Paleocene of North Dakota (Fig. 4). Elsewhere in the paleobotanical record, seeds of Nuphar have been recognized from the Oligocene of western Siberia (Dorofeev, 1963
, 1974
); the Plio-Pleistocene of Japan (Miki, 1960
); the Miocene of Poland (Szafer, 1947
) and Denmark (Friis, 1985
); the Pliocene of England (Reid and Reid, 1915
); the Middle Eocene of Republic, Washington (Wehr and Manchester, 1996
); and the early Oligocene of Oregon (Meyer and Manchester, 1997
). There are about 13 extinct species included in the genus Nuphar based on fossil seeds. Seven Eurasian species described by Dorofeev, a species from Denmark (Friis, 1985
), and Nuphar wutuensis belong to the sect. Nupharella. Members of sect. Nupharella ranged mainly from Paleocene to Miocene, although N. canaliculata Dorof. extended to the Pliocene. Sect. Nuphar has its earliest occurrence in the Pliocene (Dorofeev, 1974). The morphological difference in the sclerotesta—less thickened cuticle/outer periclinal wall in section Nuphar compared to section Nupharella—seems to indicate environmental adaptation.
Although nonseed characters remain unknown for N. wutuensis, there is some evidence of fruit morphology for other Paleogene fossils. In particular, the detached apical portion of the fruit, clearly showing the stigmatic disk, is preserved along with the seeds at the Middle Eocene Republic, Oregon (Wehr and Manchester, 1996
: Figs. 1, 2), and at the early Oligocene of Fossil, Washington (Meyer and Manchester, 1997
, plate 75, figs. 9, 10). Despite the occurrence of these fossils both in western North America, in both cases, the stylar necks are greatly elongate as in the extant lineage that is mainly in the Old World today.
Nuphar species occupy a diversity of freshwater habitats including ponds, lakes, and slow-moving streams. Today, the genus is distributed in temperate regions of North America from Alaska to Newfoundland south to northeastern Mexico and Cuba. In the Old World, Nuphar occurs in temperate Eurasia, east to the Kamchatka Peninsula in Russia, and Japan; throughout Europe and south to northern Africa (Padgett et al., 1999). The presence of Nuphar seeds in the Wutu basin indicates that the fossils were deposited in an environment of standing water, probably a lake or ponded area in which the lignite, now actively mined, was deposited.
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FOOTNOTES |
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4 E-mail: jchen{at}botany.ufl.edu
; phone: (352) 392-1721 ext. 250
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSSYSTEMATICSDISCUSSIONLITERATURE CITED |
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Cevallos-Ferriz S. R. S. R. Stockey 1989 Permineralized fruits and seeds from the Princeton Chert (Middle Eocene) of British Columbia: Nymphaeaceae. Botanical Gazette 150: 207-217[CrossRef]
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Crane P. R. S. R. Manchester D. L. Dilcher 1990 A preliminary survey of fossil leaves and well-preserved reproductive structures from the Sentinel Butte Formation (Paleocene) near Almont, North Dakota. Fieldiana Geology 1418: 1-63
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Qiu Y.-L. J. Lee F. Bernasconi-Quadroni D. E. Soltis P. S. Soltis M. Zanis E. A. Zimmer Z. Chen V. Savolainen M. W. Chase 1999 The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402: 404-407
Qiu Y.-L. J. Lee F. Bernasconi-Quadroni D. E. Soltis P. S. Soltis M. Zanis E. A. Zimmer Z. Chen V. Savolainen M. W. Chase 2000 Phylogeny of basal angiosperms: analyses of five genes from three genomes. International Journal of Plant Science 161: (Supplement 6) S3-S27[CrossRef][ISI]
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Yamada T. R. Imaichi M. Kato 2001 Developmental morphology of ovules and seeds of Nymphaeales. American Journal of Botany 88: 963-974
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