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Paleobotany |
Department of Ecology and Evolutionary Biology and Biodiversity Research Center, University of Kansas, 1200 Sunnyside Avenue, Lawrence, Kansas 66045-7534 USA
Received for publication October 27, 2006. Accepted for publication March 2, 2007.
ABSTRACT
Secondary phloem anatomy of several species of Cycadeoidea is described from trunks in the Wieland Collection, Peabody Museum of Natural History. The trunks were collected from the Lakota Formation, Lower Cretaceous, Black Hills of South Dakota. Secondary phloem is extensively developed and consists of alternating, tangential bands of fibers and sieve elements, with rare phloem parenchyma. Uniseriate rays, 2–22 cells high, occur between every one to three files of the axial system. Fibers are long, more than 1200 µm, approximately 26.6–34.2 µm in diameter, and have slit-like apertures on the lateral walls. Sieve elements range from 16–25 µm in diameter and are up to 500 µm long. Elliptical sieve areas appear on both end and radial walls and measure 10 µm across; minute spots, which may represent sieve pores, are present within the sieve areas. Secondary phloem of North American Cycadeoidea is similar in organization (alternating tangential bands) and cell types (sieve cells, fibers, axial parenchyma) to that known in other extant and fossil cycadophytes and some seed ferns. The unusual pattern of cell types and thickness of secondary phloem is discussed in the context of plant habit, phloem efficiency, and potential phylogenetic importance.
Key Words: Bennettitales • Cycadeoidea • cycadophytes • Lower Cretaceous • secondary phloem anatomy • South Dakota
The Bennettitales are a group of fossil seed plants known from the Triassic to the Cretaceous, with a worldwide distribution. Bennettitalean foliage is similar to that of true cycads in that both groups produce generally coriaceous pinnate fronds; it is often difficult to distinguish the two in fossils. Two families historically have been recognized in the Bennettitales, based on overall habit of the plant and differences in reproductive structures. Members of the Williamsoniaceae are generally reconstructed as having slender branching stems lacking persistent leaf bases, with pedunculate, monosporangiate cones borne at the tips of lateral branches, although some are known with apparently bisporangiate cones (Watson and Sincock, 1991
). The Cycadeoidaceae have short, truncated, rarely branched stems characterized by an armor of persistent, helically arranged leaf bases; bisporangiate cones are borne in the axils of the leaf bases. Cycadeoid (= Cycadeoidaceae) reproductive organs consist of tightly aggregated microsporophylls surrounding a central receptacle that bears numerous sessile, orthotropous ovules separated by interseminal scales (e.g., Crepet, 1974
; Rothwell and Stockey, 2002
).
Buckland (1828)
, Carruthers (1868)
, McBride (1893)
, and Ward (1898)
provided some of the earliest reports on Bennettitales and suggested affinities with the Cycadales. Sporadic reports of the organs of these plants continued until the early 1900s. The first comprehensive study of North American fossil cycadeoids was Wieland's monograph (1906
, 1916
), which focused on silicified trunks collected from the Black Hills of South Dakota, USA. Wieland suggested that the cycadeoids had their closest affinities with the flowering plants, based on the structure and morphology of what he interpreted to be mature cones ("flowers" of Wieland, 1906
). Wieland's (1906) reconstruction of Cycadeoidea Buckland, with the reproductive units as open flower-like structures, has been widely reproduced. Although this reconstruction is now known to be erroneous, the Bennettitales have continued to be important in hypotheses of seed plant phylogeny (e.g., Crane, 1985
; Nixon et al., 1994
; Doyle, 2006
; Hilton and Bateman, 2006
) and have been included in the anthophyte clade (e.g., Doyle and Donoghue, 1987
). Using some of the same specimens studied by Wieland, in addition to new reproductive material, Delevoryas (1963)
detailed the basic structure of Cycadeoidea cones and included specimens at different stages of development. He reinterpreted the cones as remaining closed at maturity (Delevoryas, 1963
, 1965
, 1968
). The next focus on the Cycadeoidaceae involved the reproductive biology of the plants, including the development of ovules and megasporogenesis (Crepet and Delevoryas, 1972
; Crepet, 1974
). This research contributed to the hypothesis that Bennettitales were self-pollinated, and Crepet (1974)
hypothesized that strong inbreeding depression may have contributed to their extinction. Occasional cross pollination may have occurred as a result of herbivory, based on the presence of galleries in the cones (Crepet, 1974
).
Despite extensive studies on the reproductive organs of Cycadeoidea, there has been relatively little work done on the vegetative anatomy in this taxon, with the exception of following the course of vascular tissue into the leaves and reproductive organs (Wieland, 1906
; Andrews, 1943
; Delevoryas, 1960
). While these studies consider the conducting elements in a general context, there has been no detailed work on the cell types and tissue systems in the stem. Although a few authors have noted the presence of preserved secondary phloem in cycadeoids (e.g., Wieland, 1906
; Sharma and Bohra, 1977
), these have been restricted to one or two specimens. Phloem anatomy, especially secondary phloem, has been described from a number of other fossil gymnosperms, especially among the Paleozoic seed ferns (e.g., Williamson, 1887
; Scott, 1899
; Hall, 1952
; Rothwell and Taylor, 1972
; Rothwell, 1975
; Russin, 1981
; Smoot, 1984a
, b). Our knowledge of phloem structure in the Mesozoic cycadophytes, however, remains limited. It is the intent of this study to detail the secondary phloem anatomy of Cycadeoidea from the Lower Cretaceous of the Black Hills and to evaluate cycadeoid phloem structure within the larger context of seed plant evolution.
MATERIALS AND METHODS
The present study is based on transverse and longitudinal sections of four species of Cycadeoidea: C. wielandiiWard (1899)
, C. payneiWard (1898)
, C. nanaWard (1898)
, and C. dartoniWieland (1916)
. Due to the rarity of specimens, especially those with adequate preservation of phloem tissue, transverse, tangential, and radial sections of each species are not available, so the description of the secondary phloem represents a composite analysis based on all four species. All specimens are petrified in silica and were prepared using standard petrographic thin section techniques (Hass and Rowe, 1999
) and photographed with a digital camera. Slides include material from Wieland's collection at Yale University, with additional thin sections prepared of selected specimens. All specimens are from the Lower Cretaceous Lakota Formation in southwestern South Dakota (Dahlstrom and Fox, 1995
); specimens and slides are deposited in the Peabody Museum of Natural History, Yale University, under acquisition numbers YPM 151551, 53463, 53464, 5255, 5175, 5215, 5181, 53465, 53466, 53467; Trunk nos. 00, 59, 77, and 210.
RESULTS
Cycadeoidea stems have been reported as up to nearly a meter in diameter (Crepet, 1974
). Parenchymatous pith and cortex containing secretory cells make up the major portion of the stem with a relatively narrow band of vascular tissue, most of which represents secondary growth. According to Wieland (1906)
, up to 70% of the stem is parenchymatous tissue in C. wielandii. The primary vascular system consists of an endarch eustele. Wieland (1906)
and Crepet (1974)
mentioned that the width of the secondary xylem is equal to the width of the secondary phloem. In the present material, secondary xylem measured up to 11 mm wide and secondary phloem up to 6 mm (Figs. 1, 2). Vascular rays are all uniseriate. Because rays occur between every 1–3 files of tracheids, the wood is considered manoxylic (Fig. 3).
|
). Individual tracheids are typically rectangular, 39–72 µm in radial diameter and up to 2.3 mm long. Across the xylem, there is a decrease in radial tracheid diameter (Fig. 5); the oldest tracheids near the pith range from 36–60 µm in diameter, while those nearer the cambium are 24–36 µm in diameter. Separating the secondary xylem and phloem is a 221.7-µm-wide zone of translucent material that topographically represents the position of the vascular cambium (Figs. 6, 7); however, no cellular detail is preserved.
|
9.5–28.5 µm) than those nearer the cortical region, where they range from 28.5–47.5 µm. In some cases, fiber walls appear as a series of helical bands in longitudinal section (Figs. 9, 11). We interpret these to represent cells in which the cell walls have begun to degrade, thus revealing the underlying microfibrillar structure.
|
). Both axial and ray parenchyma is present in Cycadeoidea phloem. Axial parenchyma is rare, but when present the cells are rectangular, thin walled, and measure 33 µm in diameter and 99 µm in length (Fig. 9). Axial parenchyma is seen only near the cambium, perhaps suggesting that most cells were crushed in the outer phloem. The majority of the parenchyma in the secondary phloem occurs in the form of abundant, uniseriate rays that range from 2–22 cells high (Fig. 14). Ray cells in the region of the cambium are approximately 60 µm in tangential diameter, increasing in size toward the outer edge of the phloem, where they are up to 96 µm. Rays occur between every two to three cells of the axial system.
DISCUSSION
An examination of the stems of fossil and extant Cycadales and fossil Bennettitales shows several common characteristics. These include a large parenchymatous pith, which in cycads sometimes comprises up to one half of the diameter of the stem, and secretory canals, which occur in the pith and cortex (Greguss, 1968
; Artabe et al., 2005
). Several distinct anatomical characteristics, however, separate the cycads from the Bennettitales. Most notable is the presence of girdling leaf traces in cycads, whereas the Bennettitales produce direct leaf traces (Taylor and Taylor, 1993
). Another distinctive feature is the presence of medullary vascular bundles in some cycads, which appear to be absent in Bennettitales (Wieland, 1906
).
Although numerous studies have been completed on bennettitaleans from around the globe, there is a scarcity of information on secondary phloem anatomy in these plants. Wieland (1906)
did not provide details of Cycadeoidea phloem anatomy, but merely mentioned its presence when describing the xylem. Sharma and Bohra (1977)
described the phloem in two bennettitaleans, Ptilophyllum sahnii and Bucklandia dichotoma, from the Cretaceous of India. In P. sahnii, sieve cells, parenchyma, and fibers are present, but no detail is provided regarding either the number of cells or their distribution. Sieve cells are reported to be elongate (1.4 mm long) and tapered, with closely spaced sieve areas on their lateral walls. The sieve cells in B. dichotoma have blunt end walls with circular sieve areas. In both genera, parenchyma and sieve cells are more abundant than fibers. One apparent difference in the sieve elements of Cycadeoidea when compared with those of these other fossil bennettitaleans, is the greater width (16–25 µm vs. 8–18 µm) and shorter length (500 µm vs. 1400 µm) of Cycadeoidea sieve elements (Sharma and Bohra, 1977
). Arborescent types may have longer and narrower sieve cells to compensate for transport disruption due to cell destruction, which may not have been as much of a problem in the thicker, predominantly parenchymatous Cycadeoidea (Larcher, 2003
). These differences may simply represent constraints imposed by the relatively short stature of the Cycadeoidea trunks rather than being of any systematic or phylogenetic significance.
Fibers occur in the secondary phloem of fossil cycads, extant cycads, and Bennettitales. In some extant cycads there are tangential bands of fibers, but these alternate with bands of phloem parenchyma instead of sieve cells, with rare sieve cells appearing near phloem parenchyma; in other cycads, fibers and parenchyma are in no specific arrangement (Esau, 1969
). Cycad and bennettitalean sieve cells possess elliptical sieve areas on both radial and oblique end walls. Centricycas, from the Late Cretaceous of Antarctica, appears to have some secondary phloem as evidenced by rows of thick-walled cells outside the secondary xylem (Cantrill, 2000
, fig. 3-C), however no description is provided for a more detailed comparison. Antarcticycas schopfii, a well-preserved cycad stem from the Middle Triassic of Antarctica, has a ring of vascular bundles, each up to 7 mm wide (Smoot et al., 1985
). Sieve cells in the secondary phloem alternate with a region of crushed cells that represent either axial parenchyma or phloem fibers. Sieve areas are elliptical and present on end and lateral walls. The preservation of the secondary phloem in Antarcticycas and Centricycas is not sufficient to make a detailed comparison with that of Cycadeoidea, but the three taxa are similar in the presence of alternating, tangential bands of cells, and the abundance of sieve cells in Antarcticycas and Cycadeoidea.
Several anatomically preserved cycad stems from South America have been described with preserved secondary xylem and phloem, including Menucoa (Petriella, 1969
) from the Upper Cretaceous and lower Paleogene of Argentina (Artabe and Stevenson, 1999
), Vladiloxylon from the Upper Triassic of Chile (Lutz et al., 2003
), and Worsdellia from the Upper Cretaceous of Argentina (Artabe et al., 2004
). The girdling leaf traces identify these taxa as members of the Cycadales. Menucoa cazaui is short and squat, measuring 75 cm tall and 60 cm in diameter (Petriella, 1969
), while Worsdellia has been reconstructed as arborescent. The secondary phloem of Menucoa, Worsdellia, and Vladiloxylon contains abundant fibers like those in Cycadeoidea, although they are larger in both Worsdellia (34–54 µm) and Vladiloxylon (60 µm) (Lutz et al., 2003
; Artabe et al., 2004
). In many specimens, only the fibers are preserved, and other anatomical details of the phloem, such as cell organization, are lacking, so a comparison of the proportion of fibers to either sieve cells or phloem parenchyma cannot be made.
Some fossil cycads have been described with preserved thin-walled elements in the secondary phloem, including Michelilloa waltonii (Archangelsky and Brett, 1963
) from the Triassic of Argentina, Lyssoxylon grigsbyi from the Triassic of Arizona (Gould, 1971
), Charmorgia dijolii from the Upper Triassic of Arizona (Ash, 1985
), Sanchucycas gigantea from the Cretaceous of Japan (Nishida et al., 1991
), and Brunoa santarrosensis from the Upper Cretaceous of Argentina (Artabe et al., 2004
). Of these genera, Brunoa is the least comparable to Cycadeoidea, consisting mainly of fibers with only a few sieve cells and no axial parenchyma described. Michelilloa includes fibers, sieve cells, and axial parenchyma in the secondary phloem, but the arrangement of the cells is not described. Charmorgia, Lyssoxylon, and Sanchucycas resemble Cycadeoidea in the organization of the secondary phloem. All three have fibers organized into tangential bands with rows of thin-walled cells between the bands. These thin-walled cells cannot be distinguished as either axial parenchyma or sieve elements, and sieve areas have not been identified in Charmorgia and Lyssoxylon. Cycadeoidea and Lyssoxylon have slit-like apertures on the fibers in the secondary phloem, while no apertures were described in Charmorgia or Sanchucycas.
A common feature in both Cycadeoidea and extant cycads is the large amount of secondary phloem in relation to secondary xylem (Figs. 1, 2); secondary phloem is nearly equal in width to secondary xylem in some cycads (Worsdell, 1896
), as it is in Cycadeoidea. Anatomical studies of the secondary phloem in extant cycads detail sieve cells, axial parenchyma, and fibers (Worsdell, 1896
; Chamberlain, 1911
; Miller, 1919
). The radial files formed by secondary xylem and secondary phloem, seen in Cycadeoidea (Fig. 7), are also seen in cycads (Chamberlain, 1911
). Esau (1969)
mentions tangential bands of fibers in extant cycads and notes that their abundance varies among genera. Sieve cells in Cycadeoidea and extant cycads have oblique end walls and sieve areas on both end and radial walls (Esau, 1969
). In contrast to the large amount of phloem fibers in Cycadeoidea, Wieland (1906)
describes extant cycad phloem as mostly thin-walled cells except at the base of the stem where sclerenchymatous elements are abundant. In Macrozamia the secondary phloem appears as bands of thick- and thin-walled cells (Worsdell, 1896
), similar in appearance to Cycadeoidea secondary phloem.
Some studies suggest that growth habit may be a factor in the abundance of fibers in the secondary phloem. In Cycas media, an arborescent form, there are a large number of fibers in the secondary phloem compared to sieve cells, and the fibers are organized into tangential bands (Miller, 1919
). In the secondary phloem of Lepidozamia hopei, which may reach 20 m in height, fibers are abundant, while in some subterranean species such as Stangeria paradoxa, secondary phloem fibers occur only sporadically, and in some of these, the cell wall is relatively thin (Greguss, 1968
). In extant taxa whose habit resembles that of Cycadeoidea, such as Cycas siamensis and Macrozamia communis, there are few fibers in the secondary phloem (Greguss, 1968
). Secondary phloem anatomy in Cycadeoidea more closely resembles that in the erect cycads, even though it was of short stature, perhaps revealing an intermediate stage of development between the globose and erect habits.
Secondary phloem anatomy has been described from a number of Paleozoic and Mesozoic seed plants and reveals similarities and differences with that in Cycadeoidea. Among the Paleozoic pteridosperms, secondary phloem structure is known in Callistophyton boyssetii (Russin, 1981
; Smoot, 1984b
), Heterangium americanum (Hall, 1952
), and Medullosa noei (Smoot, 1984a
). Callistophyton and Heterangium both have alternating tangential bands of cells, but unlike Cycadeoidea, the bands consist of alternating sieve cells and axial parenchyma; phloem fibers do not occur in these taxa. Medullosa noei secondary phloem has all three cell types found in Cycadeoidea (Smoot, 1984a
). In Medullosa there are regular, repeating tangential bands of fibers, sieve cells, and parenchyma. Sieve cells possess elliptical sieve areas nearly as wide as the cell on both the lateral and end walls (Smoot, 1984a
). One of the distinguishing features of the sieve cells in Medullosa is their extended length (up to 4.2 mm) compared to only 500 µm in Cycadeoidea. This difference may reflect pronounced differences in growth habit between these two plants, because Medullosa is a medium-sized tree that has been reconstructed either as upright (Stewart and Delevoryas, 1956
) or as a "leaner" (Hamer and Rothwell, 1988
). The fusiform initials in some Carboniferous pteridosperms, however, are known to be some of the longest ever recorded. Hall (1952)
reported tracheids in H. americanum longer than 9 mm. On the other hand, due to the limitations of available thin sections, sieve cells in Cycadeoidea may be somewhat longer than the ones we could measure in a single section.
Mesozoic seed plants with preserved secondary phloem include Pentoxylon sahnii from the Cretaceous of the Rajmahal Hills, India (Sharma and Bohra, 1977
) and the corystosperm, Cuneumxylon spallettii from the upper Middle Triassic of the Paramillo Formation in Argentina (Artabe and Brea, 2003
). In Pentoxylon, only sieve elements and phloem parenchyma make up the tangential bands of the secondary phloem; no fibers are present. Cuneumxylon has abundant axial parenchyma and numerous fibers scattered throughout the phloem; sieve cells, however, were not observed due to poor preservation. Of all the Paleozoic and Mesozoic seed plants, Cycadeoidea phloem most closely resembles that of Medullosa.
In comparison with extant conifers, Cycadeoidea phloem has similar cell organization to that seen in the Taxodiaceae and Cupressaceae. The secondary phloem in both groups is stratified in tangential bands and fibers are abundant (Abbe and Crafts, 1939
). While Cycadeoidea phloem has alternating bands of fibers and sieve cells, secondary phloem cells in members of the Taxodiaceae and Cupressaceae are commonly arranged in bands of fibers, sieve cells, phloem parenchyma, sieve cells, fibers, etc. (Esau, 1969
).
For extant cycads, Chamberlain (1911)
mentions the close resemblance between the xylem and phloem suggesting a reason that phloem may have been overlooked in previous analyses. In some Cycadeoidea specimens the xylem is preserved as a dark tissue, while the phloem appears more translucent (Wieland, 1906
). In other species the reverse is true (Figs. 1, 2, 6). This differential preservation may account for the lack of detailed information about secondary phloem, because species with translucent phloem may have been interpreted as being poorly preserved, or when opaque, confused with xylem elements. Chamberlain (1919)
also mentions that the cycad stem stores a large amount of water. Because water was available throughout the stem, perhaps the nearly one to one ratio of secondary xylem to secondary phloem can be related to the short transport distance in Cycadeoidea.
Phloem fibers are a dominant feature in the secondary phloem of Cycadeoidea. Worsdell (1896)
suggested that the presence of abundant fibers was necessary in a principally parenchymatous stem. In such a tissue system, he suggested that numerous fibers in secondary phloem provided additional support in the stem. With such a large proportion of cross-sectional diameter consisting of parenchymatous pith and cortex, xylem tracheids and phloem fibers might have functioned in stem support. In extant cycads, however, the abundance of secondary phloem fibers varies among genera (Greguss, 1968
), in contrast to Worsdell's conclusion. A slightly modified interpretation of Worsdell's hypothesis concerning the large number of fibers in Cycadeoidea phloem may be related to sieve cell efficiency. The large number of sieve cells may indicate that individual cells were relatively inefficient at transport. If the few axial parenchyma cells are indicative of their scarcity and not their lack of preservation, then the small amount of axial parenchyma involved in loading the sieve cells for transportation would require a large number of sieve cells to effectively move photosynthates. In this scenario, numerous fibers would contribute to providing support for the sieve cells. The long fibers could also contribute support to the axis because there is a small amount of wood produced relative to the size of the axis. Niklas (1997)
, however, has suggested that the majority of the stem support in cycads is provided by the persistent leaf bases, perhaps contradicting the hypothesis that phloem fibers helped in this role in Cycadeoidea. Without a modern analog or biomechanical model, however, no definitive conclusion can be made.
The small number of axial parenchyma cells presents a physiological enigma in Cycadeoidea. The absence of parenchyma cells could reduce the rate of photosynthate loading into the sieve cells for transport. Conversely, axial parenchyma may have been abundant in Cycadeoidea, but was not preserved or was crushed during fossilization. The presence of a few axial parenchyma cells near the cambial zone suggests that they may have been crushed or otherwise altered in the older phloem or cannot be distinguished from sieve cells.
The boundary between presumably functional and nonfunctional phloem is not readily apparent in Cycadeoidea. Sieve cells close to the cambial zone appear to be plugged with callose. Callose that completely covers the sieve areas is assumed to represent definitive callose in nonfunctional sieve cells (Esau, 1939
). In radial section, it can be seen that no sieve cells were preserved next to the vascular cambium, so actual functioning phloem may not have been preserved. The sieve cells nearest the cambial zone all appear to have definitive callose suggesting that the functioning phloem may have been only a few cells wide when the plant was alive.
The extensive production of secondary phloem in relation to secondary xylem appears to be a feature that is unique to the cycadophytes (= Cycadales and Bennettitales). In many extant seed plants, phellogen eventually differentiates within the secondary phloem, destroying the older phloem to the outside. Because no cork cambium is present in Cycadeoidea, the secondary phloem remains more intact in older stems. A possible plesiomorphic character in the secondary phloem of seed plants is the presence of tangential bands of cells. Cell organization may be of potential use in lower level systematic studies because the tangential bands contain different cell types and are often arranged in specific series in particular taxa as presented in this study. Secondary phloem anatomy in Cycadeoidea, with alternating fibers and sieve cells, is unique; no other genera have such an abundance of these two cells. The present study on Cycadeoidea and future studies on the anatomy of other extinct seed plants may present the opportunity to relate climate, plant habit, and anatomy within some of these fossil groups.
FOOTNOTES
1 The authors thank the Yale Peabody Museum of Natural History for the loan of specimens and slides used in this study. The project was partially supported by the National Science Foundation, grant no. OPP-0229877. 
2 Author for correspondence (rybergp{at}ku.edu
)
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