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Paleobotany |
2Laboratoire de Paléontologie, Université Montpellier II, place Bataillon, 34095 Montpellier, France; 3Institute of Geology, Academy of Geological Sciences, 26 Baiwanzhuang Road, 100037 Beijing, China; 4European Synchrotron Radiation Facility, BP 220, 38043 Grenoble, France
Received for publication October 20, 2004. Accepted for publication April 15, 2005.
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ABSTRACT |
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Key Words: Charophyta • evolution • morphology • paleoecology • Paleozoic • umbellids • x-ray synchrotron microtomography
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Doubtful remains of Sycidiales of the Lower–Upper Silurian transition have been reported from Canada (Mamet et al., 1992
). Although restricted to Europe (Ishchenko and Saidakovsky, 1975
; Ishchenko and Ishchenko, 1982
; Conkin and Conkin, 1992
) and eventually North America (Mamet et al., 1992
) during the Silurian, they became highly diversified and widely distributed thereafter as a consequence of major cladogenesis during the Devonian and Lower Mississipian (Grambast, 1974
).
Despite rich documentation, a certain number of uncertainties remain. Though all three orders and eight of the 12 families in the classification adopted for the forthcoming treatise (Feist et al., 2005
) were already present in the Devonian, Paleozoic charophyte floras have characteristic features. The direction of spiralling of cells in the Trochiliscaceae and Moellerinaceae differs from that of modern forms; similarly, the large size and thick wall of some Sycidiaceae as well as the calcified coronular cells in Karpinskya (Trochiliscaceae) and in the Chovanellaceae have not been reported from post-Paleozoic charophyte floras. Some Devonian forms moreover have not been unanimously considered to be charophytes; this is exemplified by the various attributions of Sycidium (Peck 1934a
) as a lycopod "seed," a polyp, a phyllopod egg, and a foraminifer. More recently, Langer (1976)
included Sycidium with some uncertainty in Charophyta and Lu et al. (1996)
considered the Pinnoputamenaceae as a group whose nature remains unclear. Maslov (1961)
suggested that Sycidium and Chovanella were not true gyrogonites, but were utricles, supplementary envelopes made by thalleous elements. Though utricles are mostly found in the Clavatoraceae of Late Jurassic and Cretaceous age, these have also been recognized in Pinnoputamenaceae from the Lower Devonian of Europe (Feist and Feist, 1997
). This paper demonstrates that the fructification of most Paleozoic taxa consists of a gyrogonite surrounded by a supplementary cover, the utricle, made of generally calcified cells of vegetative origin; these results are exemplified by new material from China and material in existing charophyte collections. The new data were obtained using microscopy and high-resolution x-ray synchrotron microtomography applied to charophytes for the first time.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) in which a solution of 80% acetic acid (250 mL) and white copper sulphate (100 g) are mixed in a glass jar under a fume-hood 2 h before use. Completely dry rock, cut into pieces approximately 1 cm across, is placed in the solution and left bubbling 12–48 h until most of limestone has been dissolved. The solution is then neutralized with ammonium hydroxide, washed, and sieved under water. This treatment was used for the hardened marls from China.
Method of preparation for thin sections of individual charophyte specimens
Axial sections are the most often used. They provide unequalled information on the calcified wall and on the basal plate; more rarely, when elucidating the apical structure, the sections allow taxonomic attribution, generally at the family level. This preparation also allows examination of the oospore wall if it has been preserved. The procedure consists of embedding a specimen in resin, then thinning both faces by polishing in the desired orientation (Feist et al., 2005
).
High resolution x-ray synchrotron microtomography
To obtain data on three-dimensional (3D) structures, we used high-resolution phase contrast x-ray synchrotron microtomography (µCT) performed at the European Synchrotron Radiation Facility (ESRF, Grenoble, France) on the ID19 beamline. Three-dimensional reconstruction of virtual slices is obtained from a set of numerical radiographs taken during complete or half rotation of the specimen under study. Microtomography is a recent development of medical computerized tomography that provides nondestructive high-resolution 3D information. Using a third-generation synchrotron such as the ESRF to perform µCT presents numerous advantages compared with industrial microtomographs (Salvo et al., 2003
). First, as the beam is extremely bright, it is possible to use monochromatic x-rays instead of a white beam. It avoids the beam-hardening effect commonly observed with industrial microtomographs. This strong brightness also provides very high resolution down to the submicrometric scale. Because the beam is nearly parallel, there is no magnification of pictures on the detector. It avoids geometric artefacts due to the cone beam. Because the beam is partially coherent, it is possible to perform µCT in phase-contrast mode by increasing the distance between the sample and the detector. Interferences highlight the visibility of the edges and of internal interfaces of the sample (Buffière et al., 1999
; Baruchel et al., 2001
; Stevenson et al., 2003
; Weiss et al., 2003
).
We used an optical system linked to a 2048-pixel fast read-out, low noise (FReLoN) charge coupled device (CCD) camera in order to obtain pixel sizes of 0.7 or 1.4 µm, with a field of view of 1.4 mm. For the largest specimens of Sycidium xizangense f. turbineum, we used a pixel size of 2.8 µm with a field of view of 2.8 mm. We used a beam in the 2/3, 1/3 mode with an energy of 25 keV. To work in phase contrast, the camera was moved back by 15 mm and 50 mm for the largest samples.
Samples were placed in a plastic cone glued onto a nail. This simple setting permits the number of contact points between the sample and the support to be limited. It further facilitates the virtual separation of the sample from surrounding noise.
Data were originally recorded on 32 bits. In order to reduce the data size, we recoded the reconstructed slices on eight bits. Strong ring artefacts were present. They were removed by using a script specially developed on Adobe Photoshop version 5.5 software (Adobe Systems, Inc., San Jose, California, USA). Samples were then virtually separated from the surrounding background and from the plastic cone by 3D segmentation with VGStudio Max version 1.1 (Volume Graphics, Heidelberg, Germany) software. This software was also used to create all the 3D pictures from the microtomographic data and to reconstitute the internal structures in three dimensions.
Microscopy
Confocal microscopy
With a confocal microscope, three-dimensional images of a sample are obtained by scanning many thin optical sections through a cut and polished specimen. We used a Biorad 1024 CLSM system (Zeiss Advanced Imaging Microscopy [A. I. M.], Jena, Germany). This beam scanning system uses a Nikon (Tokyo, Japan) Optiphot II upright microscope and an Argon-Krypton ion laser (Nikon) (15 mW) with two emission lines: at 488 nm and 568nm. A series of optical sections were collected and projected onto a single image plane using LASER SHARP 1024 software and processing system (Zeiss A. I. M.). Images were scanned at 1024 x 1024 pixel resolution with a 20x and 60x Nikon planapochromatic objective lenses. Observations were performed at the Centre Régional d'Imagerie Cellulaire (Lapeyronie Hospital, Montpellier, France).
Light microscopy
Polished and thin sections of isolated specimens were observed in transmitted or in reflected light using an Olympus (Tokyo, Japan) BX51 microscope connected to an Olympus DP12 digital camera). We used three UMPlan F1 objectives: 5x, 10x, and 20x.
Scanning electronic microscopy
For scanning electron microscopy (SEM), specimens were glued onto a stub and coated with platinum; the coating was thick enough (15–20 nm) to avoid electronic charge generated by the spherical shape of the charophyte fructifications.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The symmetry of the fructification, well marked by numerous basal cells, differs from a gyrogonite where the pentagonal basal pore is surrounded only by smooth spiral cells without supplementary short cells.
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The multilayered wall is also visible in thin sections of S. xizangense f. turbineum (Figs. 6, 9, and 10) as well as in Trochiliscus podolicus (Fig. 17), Pinnoputamen occitanicum (Fig. 21), and Karpinskya laticostata (Fig. 19).
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), the vesicle appears as two long bands adjoining the inner side of the thick wall.
The precise morphology and position of the vesicles have been obtained by observations from high-resolution x-ray synchrotron microtomography (µCT). The 3D view of Sycidium foveatum (Fig. 7) shows, on the external surface, the long vertical primary calcified branches, subdivided into polygonal pits characterizing the genus; on the right side of this image, where the underlying external structure has been removed (in a virtual sense), appears a double-walled vesicle, fastened to the two poles of the fructification. A similar structure is visible in Trochiliscus podolicus (Fig. 18), although the external cells (not figured) are spiraled and devoid of polygons; the isolated vesicle is bottle-shaped with an enlarged base. In both species the vesicles are covered with spherical corpuscles that, according to T. N. Taylor (University of Kansas, personal communication), recall the spores of a parasitic chytrid colonizing thalli of Palaeonitella from the Devonian Rhynie Chert (Taylor et al., 1992
).
A polished section of Sycidium reticulatum (Fig. 16) shows gyrogonite cells visible by transparency below and inside the thin wall of the vesicle. Thus the latter does not represent the oospore membrane, as thought previously (Peck, 1934a
). Besides Paleozoic forms, a vesicle also occurs in the Clavatoraceae Atopochara ulanensis Kyansep-Romashkina (pl. 1, fig. 3a, 3b in Wang and Lu, 1982
); in that case, the wall of the vesicle is a thin calcareous layer located, as in Sycidium, below the external wall of the fructification.
Gyrogonite remains
In species possessing utricles, gyrogonite cells are rarely seen from the exterior. As regards the Paleozoic, the only example is Ampullichara talimuica f. crassa Yang and Zhou (Figs. 24, 25), which has an open apical pore and 12 dextrally spiraled cells surrounded by three large cells that do not reach the apex. This is a rudimentary utricle with the calcified external branches not coalescent. The gyrogonite, half-included in the utricle, presents all the characters of the Moellerinaceae.
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, Catillochara moreyi). The high number of cells visible in sections of Paleozoic forms suggests that they are spiraled and that their number is higher than five. If the gyrogonite cells were vertical, only two units would be apparent in a longitudinal section. The orientation of spiraling cannot, however, be determined from thin sections or polished surfaces.
Calcified branches, pores, and canals
In S. xinjianzense f. turbineum the internal part of the fructification (Fig. 5) has long, vertical, clear, calcified units (primary branches) separated by thin dark lines representing the primary canals. An internal basal view (Fig. 4), once the external layers have been removed, shows four branches that can be interpreted as corresponding to the G–J cells of Fig. 2. Cross sections of the same species (Figs. 9, 10) exhibit the crystallized central area, a dark gray layer (possibly representing the gyrogonite), and small black triangular structures corresponding to sections of primary canals from which originate dark lines that correspond to secondary canals.
In reflected light, a specimen of S. reticulatum shows numerous canals radiating from a central area that might represent the vesicle (Fig. 11), ending at the surface of the fructification (Figs. 12, 26). Langer, who first studied this material, demonstrated that the pores are located in the angles of the polygons (Langer,
1976, pl. 25, figs. 2, 3: Langer, 1991,
fig. 2.1, 2.2). A µCT view of S. xinjianzense f. turbineum (Fig. 8) also displays polygonal pits with pore canals in their angles, well below the surface. This disposition (Fig. 26) recalls the thallus structure of charophytes, made of nodes and internodes. The internal and external polygons would represent two successive nodes, separated by secondary branches of radiating canals figuring the internodes.
In summary, the fructification includes a total of 18 primary branches and 18 primary canals, both subdivided into 10–15 successive verticils of secondary branches and secondary canals (Fig. 27). When primary branches and canals are not subdivided into verticils, no polygons are formed at the surface of the utricle. This explains why some Trochiliscus species, such as T. lipuensis Z. Wang et al. (1980)
, show well-marked subdivisions whereas in others, such as T. podolicus Croft (1952)
, the external cells appear to be completely smooth. Our model also explains the variable morphologies found in Sycidium utricles. The most complex is obviously S. xinjiangense f. turbineum, showing successive layers of polygons (Figs. 8– 10) in addition to verticiliated canals and calcified branches (Fig. 27). In some species, S. reticulatum (Fig. 26), S. foveatum (Fig. 7), and S. volborthi eifelicum forma a (Fig. 14), the external surface corresponds to the view of the internal layer of polygons in S. xijiangense f. turbineum (Fig. 8). In S. volborthi eifelicum forma b (Fig. 15), the tips protruding from the polygons represent the ends of the secondary calcified branches. Fructifications of this type have been grouped by Langer (1991)
in the subgenus Centroporus.
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DISCUSSION |
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The only charophyte group that shares this feature is the Mesozoic family Clavatoraceae. Among them the Clavatoroideae also have a complex utricle wall, and the Atopocharoideae a vesicle. In addition, the same trend towards disappearance of the antheridia at the surface of the utricle can be observed both in the Cretaceous Perimneste-Atopochara lineage and in the lineage from Pinnoputamen occitanicum to its Chinese descendant P. yunnanensis during the Devonian (Feist et al., in press
). Despite these resemblances, Paleozoic and Mesozoic groups are far from being identical; the disposition and the high number of calcified branches and canals (nearly 300 in Sycidium) are unknown in the Clavatoraceae, although these differences could be interpreted as variations of a general bauplan. The main character that differentiates both groups concerns the gyrogonite, which underwent evolution (Grambast 1974
). In the Clavatoraceae, included in the Charales Charinae, the gyrogonite has undoubtedly five sinistrally spiraled cells (Feist and Grambast-Fessard, 1991
), whereas gyrogonite remains found in Paleozoic forms with a utricle show that the cell number of the gyrogonite is higher than five and more likely 12 as in Ampullichara talimuica f. crassa. In fact, five-celled gyrogonites did not exist during Devonian times, appearing no earlier than the Pennsylvanian (Peck, 1934b
). The only Early Paleozoic species without a utricle was Moellerina laufeldi Conkin, from the Upper Silurian (Ludlow) of Gotland (Sweden; Conkin and Conkin, 1992
), the oldest undoubted charophyte species, whose small-sized gyrogonites present 8–12 spiraled cells; it could possibly have occupied the space inside the utricles of Sycidium, Trochiliscus, Karpinskya, Pinnoputamen, and Xinziangochara.
The potential disposition to develop a utricle, demonstrated experimentally in extant species (Ducreux, 1975
; Feist et al., 2005
), might be a phenomenon inherent in Charophyta that could have developed at any time, and could presumably also develop in the future.
The discovery of a utricle in most Paleozoic taxa implies new phylogenetic relationships among Paleozoic families (Fig. 28). We regard the Moellerinaceae as occupying a central position in the phylogeny of the group. On the left side of the diagram, one group of their descendants constitute the gyrogonites inside the utricles in the four families, Sycidiaceae, Trochiliscaceae, Chovanellaceae and Pinnoputamenaceae, composing the Sycidiales. On the right side, a second descendant group of the Moellerinaceae is thought to represent the utricle-free ancestors of the Charales by inversion of spiralization and reduction of cell number in an evolutionary lineage from the Eocharaceae to the Characeae, which includes all extant species.
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), occurring in habitats of abnormal salinity (hyper- or low salinity) from the Givetian to the Mississipian (Mamet, 1970
; Peck, 1974
) worldwide. They have been regarded as foraminifers (Loeblich and Tappan, 1964
) as well as utricles of charophytes (Poyarkov, 1966
; Edgell, 2003). Our data support the charophyte hypothesis, at least for some umbellids such as the specimens figured by Mamet (1970
, figs. 1, 2): Quasiumbella sp. seems to represent a form of Chovanellaceae and Biumbella braznikhovae Mamet (1970
, figs. 8, 9) resembles a tangential section of Trochiliscus podolicus Croft (Trochiliscaceae). The lid that covers the umbellid apex may correspond to coalescent apical cells found in the Chovanellaceae and in Karpinskya (Croft) Grambast (Trochiliscaceae). The three Quasiumbella species illustrated by Sedgell (2003
, pl. 3) may represent calcified vesicles of Sycidiales.
As we have argued that the morphological similarities between Sycidiales and Clavatoraceae are homoplasous rather than expressing true phylogenetic relationships, the development of a supplementary calcified envelope in two different periods may have resulted from similar external constraints. Indeed, both the Silurian–Devonian and Jurassic–Cretaceous transitions were characterized by increased terrestrialization. Charophytes, which are pioneer plants (Corillion, 1975
; Feist et al., 2005
), could rapidly colonize new ecological niches (brackish coastal lagoons and freshwater lakes) on emerging land areas after the collision of the continental blocks at the end of the Silurian and after the regression of the sea in several areas during the Upper Jurassic and Lower Cretaceous. The Silurian charophyte localities of the problematic Sycidiales in Canada (Mamet et al., 1992
) and Ukraine (Ishchenko and Ishchenko, 1982
) are both situated in the south tropical arid zone (Scotese, 2001
); during the Upper Jurassic, the Clavatoraceae occurred under analogous climatic conditions in North Africa and Hampshire (Feist et al., 1995
). The solidly packed structure of the utricle can be viewed as an organ of protection of the zygote against dessication. In this regard, Graham and Gray (2001
, p. 150) already suggested that Early Paleozoic charophyceans may have occupied ephemeral aquatic environments. In Silurian species, utricles may have built up progressively, in parallel with what occurred with the Clavatoraceae. During the Oxfordian, the porocharacean gyrogonite of Nodosoclavator was surrounded by a sole whorl of branchlets (Mojon, 1989
); 20 million years were necessary to attain the state of condensed utricles in Clypeator and Globator during the Tithonian (Feist et al., 1995
). If we suppose a similar interval of time for development of utricles in Paleozoic forms, the initial state of primitive utricles may have originated in the Upper Ordovician. Gyrogonites of Moellerinaceae that occur inside Paleozoic utricles are necessarily older than the oldest Sycidiales, i.e., the Ludlovian Praesycidium siluricum T. A. and A. A. Ishchenko and the doubtful Wenlockian Sycidiale from Canada (Mamet et al., 1992
). The utricle-free state is probably the primary state in charophyte evolution. According to molecular data, the charophyte clade may extend as far back as the Precambrian-Cambrian boundary (Chapman and Buchheim, 1991
; Graham and Gray, 2000).
In conclusion, in challenging the generally accepted view, we have demonstrated that the majority of Paleozoic taxa are provided with utricles. High-resolution x-ray synchrotron microtomography has allowed a three-dimensional approach of the charophyte fructifications to be developed; it has permitted internal structures characteristic of utricles to be visualized, that could not have been discerned by other means. Hence, the presence of gyrogonites covered with utricles extends further back in the fossil record than was previously known. This evidence implies a new phylogenetic scheme for Charophyta, where the 11 families composing the group are all related, directly or indirectly, to the Moellerinaceae; the presence of utricles in the Mesozoic Clavatoraceae is a homoplasy. Further research may point in three directions: (1) Investigations are needed to reveal the structure of the gyrogonites inside the utricles, in particular with regard to the direction of spiralling and the number of cells, essential for determining phylogenetic relationships between families. (2) High-resolution x-ray synchrotron microtomography has to be applied to other families and to the Clavatoraceae in particular, in order to reveal the complex structures of the utricles in three dimensions, and generally in all cases where information on internal structures must be obtained without destruction of the fossil. (3) A search for Early Paleozoic ancestors of the group may give insights into the origins and development of the charophyte gametangium (female reproductive organ surrounded by a multicellular wall) during early stages of charophyte evolution. This might help us to determine whether they present a pattern of algal type or of land plants.
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FOOTNOTES |
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5 Author for correspondence (e-mail: mofeist{at}isem.univ-montp2.fr
)
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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= 488 + 568 nm). 23. Scanning electron micrograph, lateral view. Vertical cells and nodal basal cell of the utricle. Scale bar = 150 µm
