Megaspore and microspore massulae of Paleoazolla patagonica gen. et sp. nov. are described from the Upper Cretaceous of La Colonia Formation, Chubut ...
American Journal of Botany 86(8): 1200–1206. 1999.
PALEOAZOLLA, A NEW HETEROSPOROUS FERN FROM THE UPPER CRETACEOUS OF ARGENTINA1 ANA ARCHANGELSKY,2,3 CARLIE J. PHIPPS,3 THOMAS N. TAYLOR,3 AND EDITH L. TAYLOR3 2
Museo Paleontolo´gico E. Feruglio, 9 de Julio 655, 9100 Trelew (Chubut), Argentina; 3Department of Ecology and Evolutionary Biology and the Natural History Museum and Biodiversity Research Center, University of Kansas, Lawrence, Kansas 66045
Megaspore and microspore massulae of Paleoazolla patagonica gen. et sp. nov. are described from the Upper Cretaceous of La Colonia Formation, Chubut Province, Argentina. The new fern possesses megaspore complexes with three to four glochidiate floats attached directly to the megaspore; a columella-like structure appears to be absent. The megaspore wall consists of a two-layered exine that is smooth to irregularly perforate, a two-layered perine with a spongy, densely packed endoperine, and a loosely organized exoperine. Infrafilosum hairs cover the exoperine. Microspore massulae are irregular in size and shape and bear multibarbed glochidia that generally have anchor-shaped tips. A comparison with other azollaceous and salviniaceous genera, particularly Azolla, is provided, together with a discussion of some evolutionary trends within the family. Key words:
Argentina; Azollaceae; heterosporous ferns; Paleoazolla patagonica; Upper Cretaceous.
The Azollaceae is a family of heterosporous ferns that is well represented in the fossil record (Late Cretaceous– Recent). Several genera are only known from fossils, with Azolla Lamarck known from both fossil and extant specimens. Vegetative remains of these heterosporous ferns are rarely preserved in the fossil record (Saunders and Fowler, 1993; Hoffman and Stockey, 1994). However, because megaspore complexes and massulae are impregnated with sporopollenin (Lucas and Duckett, 1980; van Bergen, Collinson, and de Leeuw, 1993) these structures are commonly found in fossil deposits. The taxon described here is based solely on reproductive structures. In the southern hemisphere, extant and Quaternary species of Azolla have been described, with fewer reports from the Cretaceous and Tertiary of Argentina. Fossil massulae of the Azollaceae, including Azolla, Parazolla, and Azollopsis, have been reported from the Upper Cretaceous of Chubut, Mendoza, and Rı´o Negro Provinces (Papu´, 1988a, b) and the Mata Amarilla Formation, Santa Cruz Province (Stough, 1868). However, the megaspore record is restricted to Azolla from the Upper Miocene of Parana´ Basin (Gamerro, 1981). MATERIALS AND METHODS Stratigraphy—The Colonia Formation is located between the Telsen and Sierra Rosada (Puesto Pintihueque) regions along the plateau border, in Chubut province, Argentina. Argillaceous portions of the lower and middle levels of the formation are continental, probably lacustrine deposits, reflecting periodic wet and dry intervals (Ardolino, and Franchi, 1996). Fossil plants and the remains of the dinosaur Carnotaurus sastrei were found in the wet units. The upper part of the sequence changes gradually to a marginal and shallow marine environment with an important assemblage of micro- and megafauna. Foraminifera found 1 Manuscript received 12 February 1998; revision accepted 21 January 1999. The authors thank Luı´s Lezama for his work on material preparation. This research was funded in part by NSF grant number OPP-9596197 to ELT and TNT.
at different localities of La Colonia Formation indicate a Maastrichtian age, but Ardolino and Franchi (1996) extend the age of these localities to the Campanian. Therefore, they assign the levels below the foraminifera to the pre-Campanian. A palynological study of La Colonia Formation is currently underway to more accurately determine the precise age of the lower and middle units. Palynology—The samples were mechanically disaggregated and treated for 7 d with hydrofluoric acid (70%) to remove silicates and washed twice at 608C with hydrochloric acid (50%) to remove carbonates. The specimens were decanted and washed several times without centrifugation because of their fragile nature. This was especially important as extensive agitation could disassociate the component structures of the massulae and megaspores and alter their original size. As a result of these techniques several hundred specimens were recovered. Specimens were mounted either in glycerine jelly for light microscopy or directly on stubs for scanning electron microscopy (SEM). Light microscopy observations were made with a Zeiss Universal compound microscope. SEM observations were made at 5 kV with an Hitachi S570 microscope. Microspore massulae were cleared with concentrated Schultze’s reagent for 30 min. Specimens for transmission electron microscopy were dehydrated in a graded ethanol series and embedded in LR White low viscosity resin. Ultrathin sections were mounted on Formvar-coated slot grids (Rowley and Moran, 1975), triple stained with potassium permanganate (1%, 1.5 min), uranyl acetate (1%, 12 min) and Reynolds’ lead citrate (9 min) and viewed at 80 kV on a JEOL JEM-1200 EX II microscope. Specimens are housed in the Museo Paleontolo´gico Egidio Feruglio (MPEF), Trelew, Argentina. Terminology—As the vegetative portions of Paleoazolla have not been discovered, the only terminology used is that of the reproductive parts. The megaspore complex or apparatus consists of the megaspore body (5infraspore of Sweet and Hills, 1976) and the floating or ‘‘swimming’’ apparatus (5supraspore of Sweet and Hills, 1976). The latter consists of pseudocellular structures, or floats, that are attached to the megaspore either directly or by a columella (a filamentous structure located above the trilete suture; Hoffman and Stockey, 1994) and collar (a structure that delimits the periphery of the proximal surface of the megaspore; Fowler and Stennett-Willson, 1978). Wall stratification in hydropteridinean megaspores is generally complex, and different terminologies have been applied. In this paper we
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follow Kempf’s (1969) terminology in which the sporoderm is separated into three principal layers: intine (thin inner layer usually not preserved in fossils), exine (megaspore wall proper), and perine (additional external layer, perispore of many authors). The perine is generally two layered with an inner endoperine and outer exoperine from which abundant hairs arise to form the filosum. Hairs that originate below the collar region (over the megaspore itself) are termed infrafilosum. If they originate from the collar region and columella, they represent the suprafilosum (Fowler and Stennett-Wilson, 1978). The microspores of this family (except Ariadnaesporites) are variable in number and embedded in a pseudocellular matrix termed the massula (Fowler, 1975; Lucas and Duckett, 1980; Saunders and Fowler, 1992). Generally, massulae have external projections termed glochidia, which serve to attach them to megaspores by entanglement with the filosum (Hoffman and Stockey, 1994).
DESCRIPTION Division—PTERIDOPHYTA Order—HYDROPTERIDALES Willdenow Suborder—HYDROPTERIDINEAE Rothwell and Stockey Family—AZOLLACEAE Christensen Genus—PALEOAZOLLA GEN. NOV. (Archangelsky, Phipps, Taylor et Taylor) Generic diagnosis —The same as for Paleoazolla patagonica sp. nov. Specific diagnosis —Paleoazolla patagonica Archangelsky et al. sp. nov. Megaspore apparatus up to 950 mm long, 700 mm wide, composed of an ellipsoidal, commonly flattened megaspore and a complex of three or four floats; megaspore up to 650 mm long, 350 mm wide, and 115 mm thick; floats nearly spherical, 200–350 mm in diameter and attached directly to one end of the megaspore; float divided into a smooth inner zone up to 6 mm thick and an irregularly alveolate outer zone up to 25 mm thick covered by multibarbed hairs (glochidia); megaspore wall up to 52 mm thick, divided into a 7–10 mm thick exine and a 28–42 mm thick perine; perine organized into a dense spongy endoperine 4–10 mm thick and a loosely organized, irregularly packed 18–20 mm thick exoperine covered by a 6–12 mm thick infrafilosum. Massulae irregular, 350–490 mm diameter, with a pseudocellular alveolar structure from which the glochidia arise as external projections; glochidia multibarbed, up to 60 mm long, and 5 mm wide, nonseptate, commonly with irregularly distributed anchor-shaped tips adpressed to the massula surface; numerous rounded, inaperturate microspores per massula, microspores 42–63 mm in diameter. Holotype—MPEF PALIN 1 (Fig. 2). Paratypes —MPEF PALIN 2–5 (Figs. 1, 3–5), MPEF PALIN 171F (109.8/5.3 Zeiss Universal Compound light microscope, Fig. 6), MPEF PALIN 1712 (109.8/3.6 Zeiss Universal Compound light microscope, Fig. 7), MPEF PALIN 6–16 (Figs. 8–18).
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Type locality —Cerro Buitre, NE Chubut Province. Stratigraphic horizon —La Colonia Formation, Upper Cretaceous. Etymology —The generic name Paleoazolla is derived from the genus Azolla; the prefix alludes to its fossil condition. The specific epithet patagonica refers to the southern region of Argentina, Patagonia, where the specimens were collected. The megaspore complex consists of an ellipsoidal, often flattened megaspore attached to a ‘‘swimming apparatus’’ of three or four floats (Figs. 1–3). The entire complex is 580–(800)–950 mm long and 450–(560)–700 mm wide; the megaspore is 470–(570)–650 mm long, 240– (290)–350 mm wide, and 100–(115)–150 mm thick. Floats are spherical to ovate, attached directly to the megaspore at one end, and range from 200 to 350 mm in diameter. There is no apparent differentation into a columella and collar, and a suprafilosum is absent (Figs. 1, 2, 4). Occasionally two megaspores are found attached to each other in the region of the swimming apparatus, possibly because of float entanglement. The megaspore sporoderm is up to 52 mm thick and is divided into an exine and a perine. The exine is 4–10 mm thick and is subdivided into two zones. The inner zone is composed of two stratified layers of perforations irregular in shape and size, while the outer zone contains few large perforations that are mainly distributed in the upper portion of the layer close to the perine (Figs. 13, 14). The perine is also subdivided into two zones. The endoperine is 4–10 mm thick and appears dense, with numerous small (,1 mm diameter), irregular alveoli (Figs. 12, 13). The exoperine is in close contact with the endoperine, 13–20 mm thick, has a loose organization with large, irregular luminae (up to 20 mm in diameter), and contains fibrils or threads that are oriented roughly parallel to the exine surface (Figs. 13, 15). The fibrils are up to 4 mm long, anastomose frequently, and are irregularly distributed. The exoperine of the megaspore is covered by a 6–15 mm infrafilosum layer, which is formed by numerous ‘‘hairs’’ that are oriented parallel to the exine surface and derived from the exoperine (Figs. 8, 9, 12). The floats are divided longitudinally into a smooth inner zone (Figs. 5, 11) and an irregularly alveolate outer zone (Fig. 11), which is covered by multibarbed, irregularly distributed glochidia that are up to 30 mm long and attached to the float surface (Fig. 10). The microspore massulae of Paleoazolla are commonly found both isolated and attached to the megaspore floating apparatus, but are rarely found attached to the megaspore body. Massulae are 350–490 mm in diameter, and irregular in shape with a pseudocellular alveolate organization (Fig. 7); alveoli are highly variable in size and up to 20 mm in diameter. The glochidia are nonseptate, range from 20 to 60 mm long and from 1 to 5 mm wide, and are multibarbed with anchor-shaped tips (Figs. 16, 17), which are occasionally flattened (Fig. 18). Barbs are alternate or opposite and 3–6 mm long, while anchorshaped tips are from 4 to 5 mm wide, with the two points of the anchor recurved (Figs. 16, 17). In some areas of the massulae, the glochidia form dense mats, while in other regions they are absent. Numerous rounded micro-
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Figs. 1–8.—Paleoazolla patagonica (SEM). 1. Megaspore complex with three floats. MPEF PALIN 2. 3120. 2. Megaspore complex with four floats. MPEF PALIN 1. 380. 3. Megaspore complex with irregularly shaped massulae attached to floats. MPEF PALIN 3. 380. 4. Specimen with reduced megaspore and three floats. MPEF PALIN 4 3100. 5. Section showing organization of float and smooth inner surface of the float. See Fig. 11 for detail of insert. MPEF PALIN 5. 3250. 6. Part of a massula showing numerous inaperturate microspores. MPEF PALIN 171F. 3160.
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spores can be found inside the pseudocellular matrix (Fig. 6). These microspores are 42–63 mm in diameter and have a micropitted surface; however, no apertures were observed even after clearing with concentrated Schultze’s reagent (Fig. 6). Microspores always occur within the pseudocellular matrix of the massula and could not be separated for SEM observation of the surface structure. The presence of microspore massulae attached to the megaspore complex, along with the size and dispersed nature of the megaspores, suggests that the megaspores are developmentally mature. Comparisons with other taxa—More than 50 fossil and extant species of Azolla are currently recognized (Batten and Kovach, 1990), and the genus is widespread throughout the world. Azolla is divided into six sections on the basis of several vegetative and reproductive characters (Saunders and Fowler, 1993): Rhizosperma, Azolla, Simplicispora, Kremastospora, Filifera, and Antiqua. The first two are known from both fossil and extant records, whereas the last four are known exclusively from fossil material. Section Azolla is most similar to Paleoazolla based on the number of floats. It is represented by the five extant species A. filiculoides Lam., A. rubra R.Br., A. caroliniana auct. non Willd, A. microphylla auct. non Kaulf. and A. mexicana Presl, and the two fossil species A. indica Trivedi and Verma and A. intertrappea Sahni and Rao. Paleoazolla patagonica and extant species of Azolla both have three floats per megaspore; however, other characters of the modern species clearly differentiate them from Paleoazolla. These include the presence of single-barbed glochidia on the massulae, a large megaspore collar, and three-zoned floats in the modern species (Saunders and Fowler, 1993) as compared to mutibarbed glochidia, no collar, and two-zoned floats in Paleoazolla. The megaspore wall structure is also significantly different. Azolla has a broadly columnar, commonly baculate or tuberculate exoperine (Collinson, 1992), whereas Paleoazolla has a loosely packed and spongy structure with fibrils oriented roughly parallel to the exine surface. Several characters differentiate Paleoazolla patagonica from the fossil Azolla species as well. Fossil Azolla species with three floats have been described from the Upper Cretaceous to the Lower Paleocene by several authors. However, most of these reports have not been verified as the materials are poorly preserved (Collinson, 1980, 1991, 1992; Saunders and Fowler, 1993). The earliest well-known species with three floats are A. indica (Trivedi and Verma, 1971) and A. intertrappea (Sahni, 1941; Sahni and Rao, 1943) from the Cretaceous/Tertiary boundary of India (Courtillot et al., 1988; Duncan and Pyle, 1988). Azolla indica, from the Deccan Intertrappean beds of Mohgaon Kalan, India, has a spherical, columellate megaspore with a size range that is one-half to twothirds of that of P. patagonica and possesses one to three floats that are not always clearly differentiated. The megaspore wall is similar to P. patagonica, with two
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principal layers (exine and perine) and the megaspore thickness is similar, but A. indica has no infrafilosum. Massulae and microspore sizes are much smaller in A. indica (80–90 and 22–29 mm, respectively), and although glochidia possess anchor-shaped tips, they are septate and not multibarbed as in P. patagonica. Azolla intertrappea, from the Deccan Intertrappean cherts of Sausar, Central Provinces, India, has a spherical but smaller megaspore body (;215 mm in diameter) and three spongy floats that form a pyramidal projection of the megaspore wall (Sahni and Rao, 1943) that covers nearly half the megaspore. Glochidia are anchor shaped but not multibarbed and about half as long as those in P. patagonica. In Argentina there is no record of Upper Cretaceous Azolla megaspores, but Papu´ (1988a, b) described Azolla massulae from the Paso del Sapo Formation, Chubut Province. These unnamed species have glochidia that are anchor shaped, but not multibarbed, and in general are smaller than those of Paleoazolla patagonica. Papu´ (1988b) also described Azolla massulae from the Angostura Colorada Formation, Rı´o Negro province, which lack glochidia and possess trilete microspores smaller than those of P. patagonica. Grapnelispora, a genus described by Stover and Patridge (1984) from the Upper Cretaceous of New Zealand and Australia, was reported from several localities in Antarctica and Argentina (Palamarczuk and Gamerro, 1988; Askin, 1990; Papu´, 1990, 1993, 1997). One of the two species described, G. loncochensis, although morphologically different from the megaspore of P. patagonica, has glochidia on the megaspore that are almost identical to the glochidia on the massulae of P. patagonica. The morphological differences between Grapnelispora and Paleoazolla megaspores (and other genera of the Hydropteridineae) are so numerous that we suspect that the similarities of the anchoring systems are due to parallel evolution, rather than homology. There are several other heterosporous fern megaspore genera from the Late Cretaceous and Early Paleocene that are believed to be related to the Azollaceae. Glomerisporites Potonie´ is known from a single assemblage from the Upper Cretaceous of the Netherlands (Hall, 1974). It differs from Paleoazolla patagonica in having a megaspore that is multifloated with a general distribution of small floats, a megaspore exoperine that is tectate-columellate with external circinate hairs, and a single microspore per massula with circinate glochidia. Another Late Cretaceous genus is Parazolla Hall from North America (Hall, 1969), which was recently included as part of the description of Hydropteris (Rothwell and Stockey, 1994). Its exine is at least twice as thick as that of P. patagonica, and there are a larger number of plate-like extensions that are not true floats attached to the proximal megaspore surface. The perine is complex with circinate glochidia that extend out from the surface. Microspore massulae are ‘‘banana-shaped’’ with simple, unbarbed glochidia on the surface. Azollopsis Hall (Sweet and Hills, 1974) also occurs in
← 7. Several microspores covered by pseudocellular structure and with multibarbed, anchor-shaped glochidia (arrows). MPEF PALIN 1712. 3500. 8. Smooth-walled hairs that make up the infrafilosum layer on the surface of the megaspore. MPEF PALIN 6. 31490.
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Figs. 9–18.—Paleoazolla patagonica (Figs. 9–12, 16–18 SEM; Figs. 13–15 TEM). 9. Detail of megaspore showing the alveolar surface of the exoperine (arrow) and infrafilosum layer. MPEF PALIN 7. 32000. 10. Detail of alveolate float structure (arrow) with multibarbed, anchor-shaped glochidia on the surface. MPEF PALIN 8 31500. 11. Detail of float structure showing alveolate organization. MPEF PALIN 9. 31200. 12. Section
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the Late Cretaceous and Early Paleocene of North America. The megaspore has more than 32 evenly distributed floats, which are smaller than those of Paleoazolla patagonica, and are entangled in a mesh of long ‘‘hairs.’’ The megaspore wall structure is very distinctive, with a narrow and uniform granular endoperine and a fibrous thicker exoperine that is ornamented with hair-like appendages (Collinson, 1991, 1992). Papu´ (1988b) reported Parazolla and Azollopsis massulae from the Late Cretaceous Angostura Colorada Formation of Argentina. However, in this case, the poor preservation and scarcity of the material together with the morphological variability of massulae between genera do not allow the specimens to be unequivocally assigned to those genera. Salvinia Adanson extends from the Cretaceous/Tertiary boundary to the present and has been reported from various geographic regions. The specimens lack floats, are eglochidiate, and have massulae that have not been found attached to the megaspore. The structure of the megaspore wall is also different, specifically the exoperine, which possesses abundant, round to ellipsoidal cavities that vary in size among the different species. A much more geographically restricted genus is Azinia Balvjeva, a multifloated and eglochidiate taxon known from a single Upper Cretaceous assemblage in the former Soviet Union (Andrews and Boureau, 1970). This genus is morphologically very similar to Azolla (Collinson, 1992). Ariadnaesporites was described from several regions of the world (Hall, 1974), including Europe, South America, India, North America, and Africa and currently includes 24 species (Kovach and Batten, 1989). The similarities in both morphological characters and size between megaspores and microspores of Ariadnaesporites are the principal features that distinguish this genus from Paleoazolla patagonica. In addition, the ultrastructure of the two genera is distinct. The exine and perine in Ariadnaesporites are approximately the same thickness and the perine consists of an exoperine of closely packed fibrils that become less dense in the endoperine (Collinson, 1991; Batten, Collinson, and Knobloch, 1994), the opposite of what is found in P. patagonica. DISCUSSION By the Late Cretaceous and early Tertiary there was considerable diversity within the Azollaceae, but relatively few of the characters exhibited by extinct taxa are found in modern representatives of the family (Collinson, 1992). As a result, a number of evolutionary trends have been hypothesized for the reproductive morphology of the family, and especially for Azolla (e.g., Fowler, 1975; Martin, 1976; Collinson, 1980; Saunders and Fowler, 1993). It has generally been accepted, and recently restated, that one of the trends in hydropteridinean mega-
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spores has been the reduction in float number (e.g., Jain and Hall, 1969; Hall and Bergad, 1971; Jain, 1971; Hall, 1974; Saunders and Fowler, 1993). This idea is based on the fact that modern representatives of Azolla have few floats, while many fossil genera such as Glomerisporites, Azollopsis, and several extinct sections of Azolla have numerous floats. However, other genera that are contemporaneous with these megaspores have three or fewer floats (e.g., Azolla indica, A. intertrappea). As a result of this disparity, Collinson (1980) suggested that there was a rapid diversification of taxa in the Late Cretaceous resulting in a variety of float numbers and arrangements, and therefore float number does not follow a clear-cut evolutionary trend. Paleoazolla supports this concept, since it represents another early megaspore with a small number of floats. Other hypothesized evolutionary trends have been based on the increasing complexity of float attachment and arrangement. For example, Fowler (1975) suggested that the dome-shaped columella lacking floats is the basic component of the swimming complex in the Late Cretaceous, and it is from this organization that the columella became progressively differentiated into separate areas that constitute the multifloat-like structures. However, the lack of a columella in Paleoazolla patagonica suggests that both morphologies may be early types. Within the Azollaceae there appears to be a basic structural organization of the megaspore wall. The wall consists of two principal layers, an exine and a perine. Among all hydropteridinean genera it is the perine that shows the greatest variability at the ultrastructural level (Collinson, 1992; this paper). However, the perine has not yet been used for the diagnosis of various genera, and little has been written on evolutionary trends in megaspore wall ultrastructure (Hoffman and Stockey, 1994). We believe that the structure of the megaspore wall may have some taxonomic significance if there is uniformity in preparation techniques, and therefore we have included characters of the megaspore wall in the diagnosis of Paleoazolla. Paleoazolla patagonica represents another contradiction to the theory that float number in heterosporous fern megaspores has decreased through time and that possession of many floats is the ancestral state (Saunders and Fowler, 1993). Based on this evidence, a more plausible evolutionary scenario might be that there is no direct change from one float type to another within heterosporous ferns overall. Both few and multifloated megaspores existed in the Late Cretaceous as separate lineages, and only the few-floated megaspore lineages survived to the present, as Collinson (1980) has suggested. A cladistic analysis of the group could help to resolve this question; however, at present only megaspore characters are known from many of the fossil genera, and a phylogeny based
← of a megaspore showing exine (E), endoperine (D), exoperine (x), and infrafilosum (I). MPEF PALIN 10. 31700. 13. Ultrathin section of a megaspore showing exine (E), endoperine (D). To the outside of the endoperine is the exoperine (x). MPEF PALIN 11. 32500. 14. Detail of exine (E) showing several layers. MPEF PALIN 12. 36000. 15. Ultrathin section of exine, perine and infrafilosum (arrow). MPEF PALIN 13. 32000. Compare Figs. 13–15 with Fig. 12. 16. Multibarbed glochidia adpressed to the massula surface. MPEF PALIN 14. 34000. 17. Multibarbed glochidium extending from massula surface, showing recurved barbs. MPEF PALIN 15. 35000. 18. Multibarbed glochidium showing slightly different tip morphology. MPEF PALIN 16. 35000.
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on such few characters would not be robustly supported even if a signal could be produced. In addition, P. patagonica is one of only a few megaspores known whose description includes fine structural features. Paleoazolla patagonica does prove that the heterosporous ferns were highly diverse in reproductive morphology early in their evolutionary history and that theories of megaspore evolution need to be reevaluated. LITERATURE CITED ANDREWS, H. N., AND E. BOUREAU. 1970. VI-Classe des Leptosporangiopsida. In E. Boureau [ed.], Traite´ de Pale´obotanique, vol. IV, Fasc. 1, Filicophyta, 17-406, Masson et Cie, Paris. ASKIN, R. A. 1990. Cryptogam spores from the upper Campanian and Maastrichtian of Seymour Island, Antarctica. Micropaleontology 36: 141–156. ARDOLINO, A., AND M. FRANCHI. 1996. Hoja Geolo´gica 4366-I Telsen, provincia del Chubut. Subsecretarı´a de Minerı´a de La Nacion, Direccio´n General del Servicio Geolo´gico, Boletı´n numero 215, Buenos Aires. BATTEN, D. J., M. E. COLLINSON, AND E. KNOBLOCH. 1994. Ariadnaesporites and Capulisporites: ‘‘water fern’’ megaspores from the Upper Cretaceous of Central Europe. Review of Palaeobotany and Palynology 83: 159–174. BATTEN, D. J., AND W. L. KOVACH. 1990. Catalog of Mesozoic and Tertiary megaspores. American Association of Stratigraphic Palynologists Contribution Series 24. COLLINSON, M. E. 1980. A new multiple-floated Azolla from the Eocene of Britain with a brief review of the genus. Paleontology 23: 213–229. ———. 1991. Diversification of modern heterosporous pteridophytes. In S. Blackmore and S. H. Barnes [eds.], Pollen and spores: patterns of diversification, Systematics Association, special vol. no. 44, 119–150. Clarendon Press, Oxford. ———. 1992. The Late Cretaceous and Paleocene history of salvinialean water ferns. In J. Kovak-Eder [ed.], Palaeovegetational development in Europe and regions relevant to its palaeofloristic evolution, 121–127. Natural History Museum, Vienna. COURTILLOT, V., G. FE´RAUD, H. MALUSKI, D. VANDAMME, M. G. MOREAU, AND J. BESSE. 1988. Deccan flood basalts and the Cretaceous/Tertiary boundary. Nature 333: 843–846. DUNCAN, R. A., AND D. G. PYLE. 1988. Rapid eruption of the Deccan flood basalts at the Cretaceous/Tertiary boundary. Nature 333: 841– 843. FOWLER, K. 1975. Megaspores and massulae of Azolla prisca from the Oligocene of the Isle of Wight. Palaeontology 18: 483–507. ———, AND J. STENNETT-WILLSON. 1978. Sporoderm architecture in modern Azolla. Fern Gazette 11: 405–412. GAMERRO, J. C. 1981. Azolla and Salvinia (Pteridophyta, Salviniales) en la Formacio´n Parana´ (Mioceno Superior), Santa Fe, Repu´blica Argentina. Paleobotanica Latinoamericana, Circular informativa da Associac¸ao Latinoamericana de Paleobotanica e Palinologia: 12– 13 (Abstract). HALL, J. W. 1969. Studies of fossil Azolla: primitive types of megaspores and massulae from the Cretaceous. American Journal of Botany 56: 1173–1180. ———. 1974. Cretaceous Salviniaceae. Annals of the Missouri Botanical Garden 61: 354–367. ———, AND R. D. BERGAD. 1971. A critical study of three Cretaceous salviniaceous megaspores. Micropaleontology 17: 345–356. HOFFMAN, G. L., AND R. A. STOCKEY. 1994. Sporophytes, megaspores, and massules of Azolla stanleyi from the Paleocene Joffre Bridge locality, Alberta. Canadian Journal of Botany 72: 301–308. JAIN, R. K. 1971. Pre-Tertiary records of Salviniaceae. American Journal of Botany 58: 487–496. ———, AND J. W. HALL. 1969. A contribution to the early Tertiary fossil record of the Salviniaceae. American Journal of Botany 56: 527–539. KEMPF, E. K. 1969. Elektronenmikroskopie der megasporen von Azolla
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