Welwitschiaceae from the Lower Cretaceous of northeastern Brazil

mary bernardes-de-oliveira

Pseudofrenelopsis and Brachyphyllum are two conifers that were part of the Lower Creta-ceous (Aptian) taphoflora of the Crato Formation, Araripe Basin, northeastern Brazil. The former genus includes, so far, P. capillata and indeterminate species, whilst the latter is mainly represented by B. obesum, the most common plant megafossil recovered from that stratigraphic unit. Here, the stem and leaf anatomy of Pseudofrenelopsis sp. and B. obesum specimens is revisited, including the first report of some epidermal and vascular traits for both taxa from the Crato Formation. Along with its paleoecological significance, the new data suggest the presence of more than one Pseudofrenelopsis species in the Aptian tapho-flora of the Araripe Basin and further support the taxonomic placement of B. obesum within Araucariaceae.

American Journal of Botany 92(8): 1294–1310. 2005. WELWITSCHIACEAE OF LOWER CRETACEOUS NORTHEASTERN BRAZIL1 FROM THE DAVID L. DILCHER,2,5 MARY E. BERNARDES-DE-OLIVEIRA,3 DENISE PONS,4 AND TERRY A. LOTT2 2 Paleobotany and Palynology Laboratory, Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611-7800 USA; 3Laboratório de Geociências of the Universidade Guarulhos and Instituto de Geociências of the Universidade de São Paulo, São Paulo, SP, Brazil; and 4Laboratoire de Paléobotanique et Paléoécologie, UMR 5143, Université Pierre et Marie Curie, Paris, France Welwitschiaceae, a family in the Gnetales, is known today from only one extant species, Welwitschia mirabilis. This species is distributed in the Namibian desert, along the western coast of southern Africa, about 10 km inland from the coast. Very little is known about the fossil record of this family. Lower Cretaceous megafossils of various organs, assigned to Welwitschiaceae, are presented here. These fossils include young stems with paired cotyledons attached (Welwitschiella austroamericana n. gen. et sp.), isolated leaves (Welwitschiophyllum brasiliense n. gen. et sp.), and axes bearing male cones (Welwitschiostrobus murili n. gen. et sp.). They were collected in the Crato Formation, which is dated by palynomorphs and ostracods as Late Aptian (114 to 112 million years ago). These sediments are exposed in the Araripe Basin of northeastern Brazil. This study brings together new information of the megafossil record of Welwitschia-like plants and also reports of pollen said to be similar to that of Welwitschia from Lower Cretaceous sediments. Key words: Aptian; Brazil; Crato Formation; Cretaceous; Gnetales; Welwitschia. The Gnetales is a group of seed plants that is poorly documented in the fossil record (Crane, 1988, 1996). Recent studies of the Lower Cretaceous sediments in Brazil provide important new data about the occurrence of the Gnetales (Osborn et al., 1993) and in particular the fossil record of Welwitschiaceae (Rydin et al., 2003). Welwitschiaceae is a family of Gnetales, represented today only by the unique species Welwitschia mirabilis (Hooker, 1863). This species lives scattered along a restricted strip of land 1200 km long and 140 km wide along the southwestern coast of Africa from the Nicolau River (north Mossamedes or Namibe, Angola) to the Kuiseb River (Swakopmund, Namibia). The western boundary occurs about 10 km inland from coastal South Africa, and its easternmost boundary may extend up to 150 km inland. This area corresponds to the northern and central part of the Namibian Desert, reaching eastward to the Mopane Savanna (Kers, 1967; von Willert, 1985; fig. 4 in Crane and Hult, 1988). Welwitschia mirabilis is a unique plant because of its restricted and isolated occurrence and its unusual growth habit. It is a desert plant well adapted to a harsh environment by the production of a short, broad, woody stem, a long tap root, and a crown of meristematic tissue deeply embedded in a circular groove forming a rim on the short, flat-topped to concave stem. Two opposite, broad, laminar leaves are produced from this stem. These leaves extend out over the surface of the desert, wearing away at their distal ends while they continue to be produced from an active basal meristem. The pollen and Manuscript received 24 June 2004; revision accepted 21 April 2005. The help of Dr. Joseph E. Armstrong for access to living seedlings of Welwitschia and Dr. Volker Wilde (Senckenberg Museum of Natural History) and the Paris Museum of Natural History (MNHN) for access to fossil material used in this study was essential and very much appreciated. The authors thank two anonymous reviewers, James Doyle and Alan Graham, for their comments. Support was provided in part by the University of Florida, Dilcher Research Funds, the Becker-Dilcher Paleobotany Research Fund, and the Fundacão de Amparo à Pesquisa do Estado de São Paulo, FAPESP 03/09407-4. This paper is the University of Florida Contribution to Paleobiology publication no. 534. 5 Author for correspondence (e-mail: dilcher@flmnh.ufl.edu) 1 seed cones are produced on dioecious plants on short upright axes that grow out from the leaf axes that are embedded in the meristematic circular groove. The megafossils presented in this paper including leaves, seedlings, and pollen cones provide evidence that the family Welwitschiaceae, currently endemic to southwestern Africa, was present in South America and probably was even much more widespread during the Lower Cretaceous. In addition to these megafossils, polyplicate pollen grains belonging to five genera with gnetalean affinities have been identified in the Lower Cretaceous sediments of the Crato Formation. They include Equisetosporites, Gnetaceaepollenites, Singhia, Steevesipollenites, and Regalipollenites distributed in 52 palynomorph species (Table 1). These species, and others related to gnetaleans, are widespread throughout Northern Gondwana in the Early Cretaceous (Tables 1, 2). Probably some of the artificial palynomorph species correspond to several unique botanical species. However, the extreme diversity of gnetalean palynomorphs in these Cretaceous sediments indicates that the Gnetales were diverse at this time (Osborn et al., 1993). It has been suggested that some of these pollen species are related to Welwitschiaceae (Lima, 1983; Osborn et al., 1993) because of their elliptical shapes, ribbed or striate surfaces, and the presence of a distinct sulcus, characters that are similar to extant Welwitschia pollen. Welwitschia is considered to be entomophilous because of the stickiness of the pollen that would hinder wind dispersal (Endress, 1996; Wetschnig and Depisch, 1999; J. Armstrong, Illinois State University, personal communication). Generally, entomophilous species have very limited pollen dispersal. Therefore, we might expect to find the megafossils of Welwitschiaceae in the same sediments that yield pollen types similar to extant Welwitschia. The first to recognize gnetalean megafossils in the Crato Formation, which tentatively were attributed to Ephedraceae and Welwitschiaceae, were Pons et al. (1992) and Bernardesde-Oliveira et al. (1999, 2000). A diverse assemblage of plants with gnetalean affinities was noted in Mohr and Friis (2000), 1294 August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM BRAZIL 1295 TABLE 1. Main Gnetalean Northern Gondwana microfossils (here essentially restricted to South America) with suggested affinities specifically to Welwitschia and Gnetales in general. Name Ephedripites 1968 Ephedripites group Ephedripites 1973 Ephedripites Location Referencea Age ambonoides Brenner, Peru Albian-Cenomanian 2 barghoornii-E. staplini NE Brazil; Colombia Albian-Cenomanian 8–13 brasiliensis Herngreen, NE Brazil Albian-Cenomanian 8, 9, 23 elsikii Herngreen, 1975 NE Brazil; Maranhão, Barreirinhas Basin Peru; NE Brazil Cenomanian Albian-Cenomanian NE Brazil Cenomanian Peru Peru NE Brazil; Suriname Albian Albian Aptian-Maastrichtian Aptian-Lower Albian Aptian-Albian Ephedripites pentacostatus Brenner, 1968 Ephedripites subtilis Regali, Uesugui & Santos, 1974 Ephedripites sulcatus Brenner, 1968 Ephedripites validus Brenner, 1968 Ephedripites sp. Equisetosporites albertensis Singh, 1964 Equisetosporites ambiguus Hedlund, 1966 in Lima 1980 (sic) Equisetosporites cancellatus Paden Phillips & Felix, 1971 Equisetosporites concinnus Singh, 1964 Equisetosporites costaliferous (Brenner, 1968) Lima 1980 Equisetosporites crenulatus Lima, 1981 Equisetosporites dudarensis (Deák, 1964) Lima in Pons, 1988 Equisetosporites elegans Lima, 1980 Equisetosporites elongatus (Horowitz, 1966) Lima, 1982 Equisetosporites evidens (Bolkhovitina, 1961) Lima, 1980 Equisetosporites fragilis Lima, 1980 Equisetosporites huguesi Pocock, 1964 Equisetosporites irregularis (Herngreen, 1973) Lima, 1980 Equisetosporites lanceolatus Lima, 1980 Equisetosporites laticostatus Lima, 1980 Equisetosporites leptomatus Lima, 1980 Equisetosporites luridus Lima, 1980 Equisetosporites maculosus Dino, 1994 Equisetosporites minuticostatus Lima, 1980 Equisetosporites mollis Srivastava, 1968 NE Brazil; Alagamar, Crato, Ipubi Fms. NE Brazil; Exu, Crato, Ipubi, Missão Velha, Rio Batateira Fms.; Colombia; Venezuela NE Brazil; Rio do Peixe NE Brazil; Alagamar, Codó, Crato, Ipubi, Missão Velha, Rio Batateira Fms. NE Brazil; Codó, Crato, Exu Fms.; Colombia; Peru NE Brazil; Crato, Exu Fms. NE Brazil; Alagamar, Crato, Ipubi, Missão Velha, Rio Batateira Fms.; Colombia; Peru; Venezuela NE Brazil; Crato Fm. NE Brazil; Codó, Crato Fms. NE Brazil; Crato Fm. NE Brazil; Codó, Crato, Exu Fms. NE Brazil; Crato, Exu Fms. NE Brazil; Barreirinhas, Crato, Exu Fms. NE Brazil; Crato, Exu Fms. NE Brazil; Alagamar, Crato, Exu Fms. NE Brazil; Alagamar, Crato, Exu, Jatoba, Missão Velha, Rio Batateira Fms.; Colombia NE Brazil; Alagamar, Crato, Missão Velha, Rio Batateira Fms. NE Brazil; Alagamar, Crato Fms. NE Brazil; Alagamar, Codó, Crato, Ipubi, Missão Velha, Rio Batateira Fms. Colombia 10–12, 23 2, 19, 36 23, 36 2, 3 2 1, 6, 9–11, 29 4, 6, 19, 21–23, 34 19–22, 27, 31–34, 38 Neocomian 26 Aptian-Albian 4, 5, 19, 21, 24, 27, 34 Aptian-Cenomanian 2, 19–24, 31, 32 Aptian-Albian 19–21, 23 Aptian-Cenomanian 2, 4, 5, 19, 21, 22, 27, 28, 32, 34 Late Aptian-Lower Albian Aptian-Albian 19, 21–23 Late Aptian-Lower Albian Aptian-Albian 19, 21, 22 Aptian-Albian 19–22 Aptian-Cenomanian Aptian-Albian 8–12, 14, 19–22, 37 19–23 Aptian-Albian 5, 19, 20, 22, 23 Aptian-Albian 5, 19–23, 25, 27, 31, 32, 34 Aptian-Albian 5, 19, 21, 22, 23, 27, 34 Aptian-Lower Albian Aptian-Albian Albian Notes Syn.; Ephedripites sp. B Sinanoglu in Pons, 1988 Syn.; Ephedripites costaliferous Brenner, 1968 Syn.; Ephedripites chaloneri (Brenner, 1968), Ephedripites strigatus Sinanoglu in Pons, 1988 4, 19, 21, 22, 24 19–24 Syn.; Ephedripites irregularis Herngreen, 1973 6, 34 5, 19–24, 27, 34 31, 32 Syn.; Equisetosporites translucidus Deák & Combaz in Pons, 1988 1296 TABLE 1. AMERICAN JOURNAL OF BOTANY [Vol. 92 Continued. Name Equisetosporites ovatus (Pierce, 1961) Singh, 1964 Equisetosporites procerus (Brenner, 1968) Lima, 1980 Equisetosporites reyrei Lima, 1981 Equisetosporites strigatus (Brenner, 1968) Lima 1980 Equisetosporites subcircularis Lima, 1980 Equisetosporites translucidus Deák & Combaz, 1967 Equisetosporites virginiaensis Brenner, 1968 Equisetosporites sp. Gnetaceaepollenites barghoornii (Pocock, 1964) Lima, 1980 Gnetaceaepollenites boltenhagenii Dejax, 1985 Gnetaceaepollenites chlatratus Stover, 1964 Gnetaceaepollenites diversus Stover, 1964 Gnetaceaepollenites fissuratus (Paden-Phillips & Felix, 1971) Lima, 1980 Gnetaceaepollenites jansonii (Pocock, 1964) Lima, 1980 Gnetaceaepollenites lajwantis Srivastava, 1968 Gnetaceaepollenites mollis (Srivastava, 1968) Lima, 1980 Gnetaceaepollenites oreadis Srivastava, 1968 Gnetaceaepollenites ornatus Lima, 1980 Gnetaceaepollenites perforatus Lima, 1980 Gnetaceaepollenites retangularis Lima, 1980 Gnetaceaepollenites santosii Lima, 1980 Gnetaceaepollenites uesuguii Lima, 1980 Gnetaceaepollenites undulatus (Regali, Uesugui & Santos, 1974) Lima, 1980 Gnetaceaepollenites sp. Regalipollenites Lima, 1980 Regalipollenites amphoriformis (Regali, Uesugui & Santos, 1974) Lima, 1980 Location NE Brazil; Alagamar, Crato, Exu, Ipubi, Missão Velha, Rio Batateira Fms.; Rio do Peixe NE Brazil; Crato Fm.; Peru NE Brazil; Crato, Exu Fms. NE Brazil; Codó, Crato Fms.; Colombia; Peru NE Brazil; Codó, Crato, Exu Fms.; Colombia Colombia; Venezuela Referencea Age Neocomian-Albian Aptian-Albian Notes 5, 19–22, 26, 27, 34 2, 3, 22 Syn.; Ephedripites procerus Brenner, 1968 Aptian-Albian 19–21, 23, 33 Aptian-Albian Syn;. Ephedripites strigatus Brenner, 1968 Aptian-Albian 2, 19, 20, 22, 24, 38 19–24, 32, 33 Aptian-Albian 32, 38 Syn.; Equisetosporites minuticostatus Lima; Ephedripites sp. C Sinanoglu, 1984 NE Brazil; Rio do Peixe Neocomian 26 NE Brazil; Crato Fm. NE Brazil; Alagamar, Crato, Exu, Ipubi, Missão Velha, Rio Batateira Fms. NE Brazil; Rio do Peixe; Barreirinhas Basin; Crato, Ipubi, Missão Velha, Rio Batateira Fms.; Colombia NE Brazil; Alagamar, Crato, Exu, Missão Velha Fms.; Rio do Peixe; Africa NE Brazil; Africa Aptian-Albian Aptian-Albian 19, 22, 30 5, 8, 10, 19, 20, 22, 27, 28, 33, 34 Neocomian-Cenomanian 8, 26, 27, 32–34 Neocomian-Cenomanian 5, 19–22, 26, 27, 34, 36, 40 Cenomanian 10–12, 14, 36, 40 NE Brazil; Crato, Exu Fms. Aptian-Albian 19–22 NE Brazil; Alagamar, Codó, Crato, Exu, Missão Velha, Rio Batateira Fms. Barreirinhas Basin NE Brazil; Rio do Peixe Upper Aptian-Cenomanian 5, 8, 12, 14, 19, 20, 22, 24, 26, 27, 28, 34 Neocomian 26 NE Brazil; Alagamar, Crato Fms. NE Brazil; Codó, Crato, Exu Fms. NE Brazil; Crato, Exu Fms. NE Brazil; Crato Fm.; Colombia NE Brazil; Codó, Crato Fms. NE Brazil; Alagamar, Crato Fms. NE Brazil; Crato, Exu Fms.; Rio do Peixe. NE Brazil; Crato, Exu, Missão Velha Fms. Aptian-Lower Albian Aptian-Albian 19, 20, 22, 24 Aptian-Albian 19, 20, 22–24 Aptian-Albian 19, 21–23, 31 NE Brazil; Crato Fm.; Suriname NE Brazil NE Brazil; Alagamar, Crato, Missão Velha Fms.; Barreirinhas Basin Syn.; Ephedripites sp. 9 in Herngreen, 1973 Syn.; Ephedripites jansonii (Pocock, 1964) Müller, 1968 5, 19, 21, 22 Aptian-Albian 4, 19, 21, 22, 24 Aptian-Lower Albian Neocomian-Albian 5, 19, 21–23 Aptian-Cenomanian Syn.; Ephedripites barghoornii Pocock, 1964 Syn.; Cornetipollis perforata in Dino, 1992 4, 5, 19–23, 26 5, 19–22, 27, 34, 36 Aptian-Turonian 1, 4, 19, 21, 22 Upper Aptian-Middle Albian (type species) Upper Aptian-Middle Albian 7, 19, 22, 17 5, 7, 19, 21, 22, 27, 34, 36 Syn.; Ephedripites undulatus Regali, Uesugui & Santos, 1974 Gnetalean Syn.; Steevesipollenites amphoriformis Regali, Uesugui & Santos, 1974 August 2005] TABLE 1. DILCHER ET AL.—WELWITSCHIACEAE FROM BRAZIL 1297 Continued. Name Location Singhia Srivastava, 1968 Africa Singhia acicularis Lima, 1980 Singhia crenulata Lima, 1980 NE Brazil; Crato Fm. NE Brazil; Alagamar, Crato Fms. NE Brazil; Alagamar, Crato Fms. NE Brazil; Codó, Crato Fms. Peru; NE Brazil; Codó, Crato, Exu Fms. NE Brazil; Alagamar, Crato Fms. NE Brazil; Exu, Crato Fms. NE Brazil; Crato Fm. NE Brazil; Crato Fm. Africa Singhia elongata (Horowitz, 1970) Lima, 1980 Singhia minima Lima, 1980 Singhia montanaensis (Brenner, 1968) Lima, 1980 Singhia multicostata (Brenner, 1968) Lima, 1980 Singhia minima Lima, 1980 Singhia punctata Lima, 1980 Singhia reyrei Lima, 1980 Steevesipollenites Stover, 1964 Steevesipollenites alatiformis Regali, Uesugui & Santos, 1974 Steevesipollenites binodosus Stover, 1964 Steevesipollenites cupuliformis Azéma & Boltenhagen, 1974 Steevesipollenites dayani Brenner, 1968 Steevesipollenites duplibaculum Regali, Uesugui & Santos, 1974 Steevesipollenites giganteus Regali, Uesugui & Santos, 1974 Steevesipollenites grambasti Azéma & Boltenhagen, 1974 Steevesipollenites multilineatus Stover, 1964 Steevesipollenites nativensis Regali, Uesugui & Santos, 1974 Steevesipollenites patapscoensis (Brenner, 1963) Lima, 1980 Steevesipollenites pygmeus Azéma & Boltenhagen, 1974 Steevesipollenites sp. Welwitschiapites Bolkhovitina 1953 ex Potonié 1958 Welwitschiapites NE Brazil Africa; NE Brazil; Crato, Exu Fms.; Sergipe & Barreirinhas Basins NE Brazil; Alagamar, Codó, Crato Fms. Peru; NE Brazil; Crato, Exu Fms. NE Brazil Referencea Age Cretaceous (type species) Aptian-Albian Aptian-Lower Albian Aptian-Lower Albian Aptian-Albian 16, 39 19, 21–23 5, 22 5, 22 2, 19–22, 24 Aptian-Lower Albian Aptian-Albian 5, 19, 21, 22 Syn.; Ephedripites montanaensis Brenner, 1968 Syn.; Ephedripites multicostatus Brenner, 1968 19–23 Upper Aptian Upper Aptian Cenomanian-Turonian (type species) Albian 19, 21–23 4, 22 17, 40 Aptian-Cenomanian 8–11, 19–22, 36, 40 Gnetalean 23, 36 Aptian-Albian 5, 19, 21, 22, 24 Albian-Cenomanian 2, 3, 19, 20 Albian-Cenomanian 23, 36 NE Brazil Cenomanian 23, 36 NE Brazil; Codó, Crato, Exu Fms. Africa; NE Brazil Aptian-Albian 19–22, 24 NE Brazil Cenomanian 36 NE Brazil; Crato, Exu Fms. NE Brazil; Crato, Exu Fms. NE Brazil; Crato Fm. USSR Aptian-Albian 19–22 Aptian-Albian 19–22 Aptian-Albian Cretaceous (type species) 19, 21, 22, 28 15, 16, 18, 35 Albian 29 NE Brazil Syn.; Ephedripites elongatus Horowitz, 1970 19, 21–24 Aptian-Cenomanian Albian-Cenomanian Notes Gnetalean 8, 11, 12, 14, 40 Aff. near Welwitschia, then assigned to Schizaea, then Ephedripites, and now not Welwitschia; 5 Corniculatisporites Kuvaeva 1972 a (1) Belsky et al., 1975; (2, 3) Brenner, 1968, 1976; (4) Crane and Maisey, 1991; (5, 6) Dino, 1992, 1994; (7) Dino et al., 1999; (8–11) Herngreen, 1973, 1974, 1975, 1981; (12) Herngreen and Chlonova, 1981; (13) Herngreen and Dueñas Jimenez, 1990; (14) Herngreen et al., 1996; (15–17) Jansonius and Hills, 1961, 1976, 1979; (18) Krutzsch, 1961; (19–25) Lima, 1978a, b, 1979, 1980, 1981, 1982, 1984; (26) Lima and Coelho, 1987; (27) Lima and Perinotto, 1984; (28) Mabesoone and Tinoco, 1973; (29) Müller, 1966; (30) Osborn et al., 1993; (31, 32) Pons, 1983, 1988; (33, 34) Pons et al., 1990, 1996; (35) Potonié, 1958; (36) Regali et al., 1974; (37) Regali and Viana, 1989; (38) Sinanoglu, 1984; (39) Srivastava, 1968; (40) Stover, 1964. while Rydin et al. (2003) proposed Cratonia cotyledon, for a seedling they relate to Welwitschia. In this paper we present both vegetative and reproductive fossils of Welwitschiaceae from the Crato Formation. The abundant and diverse plant macrofossils from the Crato Formation are frequently well preserved because of their calcification. The first published research on the fossil plants of the Santana Group was by Duarte (1985). She identified Brachyphyllum from the Crato and Romualdo Formations and Podozamites, Nymphaeites, and Choffatia from the Crato For- mation. Since then, there has been a growing body of literature of the megafossil plants from the Crato and/or Santana Formations (Crane and Maisey, 1991; Pons et al., 1992; Martill et al., 1993; Barreto et al., 2000; Mohr and Friis, 2000; Mohr and Rydin, 2002; Mohr and Eklund, 2003; Rydin et al., 2003; Mohr and Bernardes-de-Oliveira, 2004). An overview of the Crato Formation flora presented by Martill et al. (1993, plates 10–13) demonstrated the presence of gymnosperms, angiosperms, and possible gnetaleans. Bernardes-de-Oliveira et al. (1993, 1999, 2000) recorded the presence of Araucariaceae 1298 AMERICAN JOURNAL and Welwitschiaceae. A winged fruit, which was caliciform, syncarpic, and tetralocular, was described by Barreto et al. (2000). A synthesis of fossil plants from the scientific collections of the University of São Paulo, the Federal University of Pernambuco, the Departamento Nacional Produção Mineral Museum (in Crato, state of Ceará [CE]), and the Paleontological Museum of Rural Cariri University (URCA, in Santana do Cariri, CE) was presented by Dilcher et al. (2000a, b). The collections include leaves attached to stems articulated like Schizoneura, bulblike structures of Isoetites with preserved sporophylls, fern fronds, conifer bracts, a bifoliate seedling and young isolated leaves of Welwitschiaceae, Ephedra-type stems with leaves and attached strobili, angiosperm leaves, folicules, winged fruits, and petals. Mohr and Eklund (2003) noted, based upon a collection of Crato Formation plants purchased by the Museum der Naturekunde in Berlin, that the flora represents elements from terrestrial environments and also a few reputed aquatic taxa. Of the 80 species they recognize from this collection, 20 taxa are assigned to angiosperms, predominately dicotyledons, and one putative monocotyledon. Locality and stratigraphy—The Araripe Basin is situated in the interior of northeastern Brazil and extends into the states of Piauı́, Pernambuco, and Ceará occupying an area of 8000 km2. It is located between meridians 388309 and 40509 W longitude and 7859 and 78509 S latitude. It consists of Paleozoic and Mesozoic sediments, forming one of the inland Mesozoic basins originating at the time of the breakup of Gondwana and the initial opening of the South Atlantic Sea (Berthou, 1990; Brito-Neves, 1990; Martill et al., 1993; Ponte and Ponte Filho, 1996) (Fig. 1). The lithostratigraphy and age of sediments in this basin have had a long history of controversy (table I in Martill et al., 1993). A new lithostratigraphic column for the Aptian to Albian sequence in this basin was formally proposed by Neumann (1999) and Neumann and Cabrera (1999) and is followed here (Fig. 3). In this proposal, the Santana Group includes all sedimentary post-rift sequences of the Araripe Basin consisting of the Rio Batateira, Crato, Ipubi, Romualdo, and Arajara Formations. The Santana Group corresponds to the most fossiliferous unit of the basin. In this Group, the Crato Formation is the second unit and consists of horizontal strata of thin laminated plate-like limestone with several shales, siltstones, marls, and lime–sandstone intercalations. This limestone was deposited under conditions of lacustrine flooding, terrigenous to carbonate sedimentation, in a continental lacustrine system with several shallow and wide lakes (Neumann and Cabrera, 1999; Neumann et al., 2002) (Fig. 2). The environment suggested by Bechly (1998) and Mohr and Rydin (2002) was marine or lagoonal. However, Maisey (1991) makes a strong case for the basin to represent low-energy inland freshwater lakes. The sediments indicate that there were some episodic higher energy events in the lake system, and the few echinoids near the top of the sediments suggest a late marine incursion into this freshwater lake system. The underlying Rio da Batateira Formation may be gradational or interdigitate with the Crato Formation and sometimes the Crato Formation lies disconformably on the Abaiara Formation (Neocomian) or on the Cristalin Basement rocks. Its maximum thickness is about 30 m (Martill et al., 1993). The upper contact with the Ipubi Formation is normal to grada- OF BOTANY [Vol. 92 tional. In the sediments of the Crato Formation there are excellently preserved ostracods, insects, arachnids, bivalves, gastropods, fishes, amphibians, crocodiles, pterosaurs, lizards, birds, coprolites, algae, pteridophytes, gymnosperms, angiosperms, and their palynomorphs (Maisey, 1991). The Crato Formation limestones are exploited for the cement industry and ornamental rocks, and during this mining abundant fossil remains are exposed. Based on palynomorphs and ostracods, Hashimoto et al. (1987), Arai et al. (1989, 1999, 2001), and Coimbra et al. (2002) considered that the Rio da Batateira and Crato Formations belong to the lower Alagoas stage. This included the Sergipea variverrucata palynozone that corresponds to the Upper Aptian (Fig. 3). The presence of pollen grains in these sediments, including Classopollis, monosulcate cycadophytes, and polyplicates related to Gnetales (including probable representatives of Ephedra and Welwitschia), has been used to suggest a dry regional climate, with high diurnal temperatures in the area where the Crato sediments were deposited (Lima, 1983). A similar environment also has been postulated for other parts of Northern Gondwana (Vakhrameev, 1970; Brenner, 1976; Doyle, 1977; Herngreen and Chlonova, 1981; Herngreen et al., 1996), although Doyle et al. (1982) suggested that some regional climates were warm, but not arid. MATERIALS AND METHODS Most of the plant fossils described in this study belong to the ‘‘Murilo Rodolfo de Lima’’ Collection of the Departamento de Geologia Sedimentar e Ambiental, Instituto de Geociências, Universidade de São Paulo. They are catalogued under GP/3E numbers. Other specimens catalogued as SMB were made available by Dr. Volker Wilde from the collections of the Senckenberg Museum of Natural History, Frankfurt am Main, Germany. The plant fossils were collected from several outcrops of the Crato Formation, all situated in the northern flank of the ‘‘Chapada do Araripe.’’ Collections were made by amateur collectors or purchased from collectors and donated to the Universidade de São Paulo. Collectors include Mrs. Urania Gusmão Corradini, Mrs. Maria Aparecida Vulcano, and Prof. Dr. Murilo Rodolfo de Lima. One specimen from the ‘‘Murilo Rodolfo de Lima’’ Collection was given to the Paris Museum of Natural History (MNHN) and was loaned for this investigation. The material from the Senckenberg Museum of Natural History was purchased from a collector who purchased and exported them from the same region and formation in Brazil. Modern material were examined from the Paleobotany Division, Florida Museum of Natural History, University of Florida, and supplied by Dr. Joseph E. Armstrong, Illinois State University. Some plant megafossils from the Crato Formation are preserved as impressions in thin laminated limestone, but the majority contains delicately preserved morphological details. According to X-ray analysis done at the Instituto de Geociências of the Universidade de São Paulo, permineralization occurred through partial replacement of plant tissues by iron minerals (goethite) and calcite. The plant fossils in this report were studied under a stereomicroscope with a camera lucida and with a Zeiss Axiophot optical binocular microscope with epifluorescence illumination (Zeiss, Thornwood, New York, USA). SYSTEMATICS Division—Trachaeophyta. Class—Gnetatae/Gnetopsida. Order—Gnetales. Family—Welwitschiaceae Markgraf (1926). August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM BRAZIL 1299 Figs. 1–2. Locality map of the Araripe Basin in northeastern Brazil. 1. Map of the Araripe Basin formations. 2. Map of South America and various basins in the northeast. Modified after Pons et al. (1996) and Viana et al. (1999). Genus—Welwitschiella Dilcher, Bernardes-de-Oliveira, Pons et Lott, gen. nov. Type species—Welwitschiella austroamericana Dilcher, Bernardes-de-Oliveira, Pons et Lott sp. nov. Generic diagnosis—An ovoid-shaped principal axis bearing two small opposite lanceolate cotyledons diverging from the apical area. Cotyledons with first-order venation parallel and equidistant throughout, each vein originating successively from a marginal vein. Parallel second-order veins interspersed between first-order veins. Etymology—Genus ‘‘Welwitschia’’ plus ‘‘ella’’ (Lat.) diminutive suffix for ‘‘little’’ in order to say ‘‘small Welwitschia.’’ Species—Welwitschiella austroamericana Dilcher, Bernardes-de-Oliveira, Pons et Lott sp. nov. (Figs. 4, 7–10). 1300 AMERICAN JOURNAL OF BOTANY [Vol. 92 Fig. 3. Araripe lithostratigraphical and chronostratigraphical column. Fossils collected in the Post-Rift Stage, Crato Formation. Modified after Ponte and Ponte-Filho (1996). Specific diagnosis—Principal axis oval to round, 9–10 mm long and 7–9 mm wide, with broad end-bearing cotyledons. Two opposite cotyledons arise from the axis at a 908 angle, often arching out to an angle of 45–608. The cotyledons are oblong-lanceolate, 5.8–6.3 cm long and 0.7–1 cm wide. The cotyledons have a dichotomous pair of first-order veins just above attachment to the axis. One vein appears unbranched and traverses half the cotyledon distance. The second vein produces parallel veins, each vein originating successively upward, 0.6–1 mm from each other, at an angle of divergence of 20–308. Eight to 10 parallel first-order veins observed. Parallel second-order veins interspersed between first-order veins with possibly a few thin oblique lateral second-order veins present that arise from first-order veins at a 10–208 angle, joining opposite second-order veins forming apically oriented, poorly developed chevrons. Etymology—Species ‘‘austroamericana,’’ from South America. Holotype—GP/3E-7529, ‘‘Murilo Rodolfo de Lima’’ Collection, Departamento de Geologia Sedimentar e Ambiental, Instituto de Geociências, Universidade de São Paulo, Brazil. August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM BRAZIL 1301 Figs. 4–10. Young plants in cotyledonary stage of Welwitschiella austroamericana sp. nov, Crato Formation, Araripe Basin, Brazil. 4, 8, GP/3E-7529. 4, 9, 10. Whole plant. 4. Cotyledons with prominent subparallel venation. 5. Seedling of Welwitschia mirabilis, a: hypocotyl axis; b: first growth of paired leaves; c: cotyledons still attached. 6. Enlargement of Fig. 5 showing a split in the epicotyl axis between the clasping leaf bases of the cotyledons. 7. Epicotyl axis showing the two clasping cotyledon leaf bases. GP/3E-7530b. 8. Enlargement of right cotyledon shown in Fig. 4 showing venation and rare ghost chevrons (arrows). 9. Cotyledons spreading out from an axis. The cotyledons narrow and their bases clasp the axis. SMB 16437. 10. Counterpart shown in Fig. 7, cotyledons narrow at base and spread out from the axis. GP/3E-7530a. Scale bar for Figs. 4, 5, 7, 9, 10 5 5 mm; Fig. 6 5 2.5 mm; Fig. 8 5 3 mm. 1302 AMERICAN JOURNAL Additional specimens—GP/3E-7530a, b. Number of specimens examined—Three. Locality—Chapada do Araripe, northeastern Brazil. Age and stratigraphy—Late Aptian, Crato Formation. Description—Welwitschiella austroamericana consists of an axis bearing two lateral cotyledons. The main axis is round, to ovoid, to broadly triangular in shape and laterally compressed. It probably was cylindrical in form during life. The base appears rounded or it may taper, both ending in a narrow hypocotyl (broken off in Figs. 4, 7, and 10 [about 1 mm in diameter] or the hypocotyl may be absent in Fig. 9). The axis apex appears to be flat, and the cotyledons appears to arise from either side of the axis and extend upward and arch outward from this disc (Figs. 4, 7, 9, 10). The surface of some axes may be rugose while others are smooth. The cotyledons are oblong-lanceolate in shape, often with a missing apex, and the ends are often frayed. The basal portion of the cotyledons taper to their point of attachment with the axis and may appear slightly twisted. The cotyledon bases expand down below the point of attachment and appear to clasp or arise from the sides of the young woody axis, resulting in swollen areas on either side of the axis (Figs. 4, 7, 9). These bases seem to remain intact, even when the axis begins to disintegrate. Near the cotyledon attachment is a pair of first-order veins that appear to dicotomize. Because of the twisted nature of most of the cotyledons, it is difficult to trace the complete venation of a cotyledon. But as shown in Fig. 8, the venation of half of a cotyledon is seen. One vein branches five times as it continues along the cotyledon margin. This results in several parallel veins that extend to the tip of the cotyledon where some appear to fuse. A total of 8–10 parallel, first-order veins are present. Several parallel second-order veins are interspersed between the first-order veins. Toward the apex, most of the lateral veins end at the lateral margin. In only a few areas of one specimen is it possible to observe weakly developed oblique lateral second-order opposing veins joining to form poorly defined apically oriented chevrons (Fig. 8). Discussion—The morphology of these cotyledons exclude a close relationship to monocotyledons by the organization of the venation, such as an absence of a midvein, and longitudinal veins that end blindly at the lateral margins. Also, monocotyledons have an alternate, rather than an opposite phyllotaxy. A close relationship to palm seedlings is further excluded by the absence of plications (Uhl and Dransfield, 1987). The morphology of these cotyledons are similar to those of Welwitschia mirabilis seedlings, in characters such as their opposite and divergent orientation, the tapering at their attachment to the young axis, their expanded and clasping base that is broadly attached to the axis (Figs. 4, 7, 9), and their parallel firstorder venation with weakly developed chevrons (Rodin, 1953; Sykes, 1910, 1911; Figs. 5, 6). We were able to observe 18mo-old greenhouse seedlings (J. Armstrong, Illinois State University, photographed, measured, and sent material) that show persistent cotyledons as the young leaves begin to grow (Figs. 5, 6). The size ranges of extant cotyledons are 2.8–3.5 cm long and 3–5 mm wide, each with 6–8 veins (Sykes, 1910; Rodin, 1953; J. Armstrong, Illinois State University, personal communication). The fossil cotyledons presented here are 6 OF BOTANY [Vol. 92 cm long and 7–10 mm wide, each with 8–10 veins. The sizes of the fossil cotyledons are slightly larger than any recorded cotyledons from greenhouse-grown plants. The classic chevrons or inverted Ys seen in the venation of the cotyledons consists of hypodermal fibers (Rodin, 1953), which do not seem to be well-preserved in the fossils, but can be observed with careful observation (Fig. 8). Genus—Welwitschiophyllum Dilcher, Bernardes-de-Oliveira, Pons et Lott gen. nov. Type species—Welwitschiophyllum brasiliense Dilcher, Bernardes-de-Oliveira, Pons et Lott sp. nov. Generic diagnosis—Isolated leaves of indefinite length, short or elongated, triangular to linear, entire margin, isobilateral symmetry, coriaceous, with numerous subparallel vascular bundles, usually with high venation density. Base of maximum width and is curved/enrolled. Etymology—Genus ‘‘Welwitschia’’ plus ‘‘phyllum’’ (Gr.), leaf. Species—Welwitschiophyllum brasiliense Dilcher, Bernardes-de-Oliveira, Pons et Lott sp. nov. (Figs. 11, 12, 16). Specific diagnosis—Leaves are triangular to linear, 8.9–70 cm long and 2.8–5 cm wide, with a longitudinal crease extending half the leaf length. Lamina is thick textured, the apex is acute, and the base curved to semicircular. Primary venation is subparallel, convergent near the apex, with some disappearing into the margin. Venation is equidistant, with a density of 9–15 bundles/cm of leaf width. Etymology—Species ‘‘brasiliense’’ (Lat.), from Brazil. Holotype—GP/3E-6035, ‘‘Murilo Rodolfo de Lima’’ Collection, Departamento de Geologia Sedimentar e Ambiental, Instituto de Geociências, USP. Paratypes—GP/3E-6033, -6034a and -6034b, SMB 16480. Number of specimens examined—Seven. Locality—Chapada do Araripe, northeastern Brazil. Age and stratigraphy—Late Aptian, Crato Formation. Description—The leaves (Figs. 11, 12, 16) are elongated to triangular shaped, ranging from 8.9 to 70 cm long and 2.8–5 cm wide with a basal width of 3.5–5.4 cm. The leaf symmetry is isobilateral with an entire margin, and the leaf lamina is thick and coriaceous in texture. The leaves are often creased longitudinally from the base to just less than half the leaf length. The apex is acute (Fig. 12) or may be frayed and worn, breaking the leaf into longitudinal segments (Fig. 16). The maximum width is at the base that may be semicircular or curved with tissue extending downward to form the curve (Fig. 16). Other leaf bases show a slight curvature and/or may appear to be thickened or rolled (Figs. 11, 12). These leaf base shapes suggest a direct attachment to the stem along the entire leaf base width. The venation is formed by subparallel vascular bundles, somewhat convergent near the apex with some August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM BRAZIL 1303 Figs. 11–18. Leaves and cones of Welwitschiaceae, Crato Formation, Araripe Basin, Brazil. 11, 12, 16. Isolated leaves of Welwitschiophyllum brasiliense sp. nov. 11. Elongated leaf. GP/3E-6033. 12. Triangular leaf. GP/3E-6035. 13, 14, 17, 18. Cones of Welwitschiostrobus murili sp. nov. 13, 14. Cones. 40033. 15. Male cones of Welwitschia mirabilis. Isolated leaf of Welwitschiophyllum brasiliense sp. nov. 16. Leaf with frayed apex. SMB 16480. 17. Cone. GP/3E5802. 18. Cone. GP/3E-7531. Scale bar of Figs. 11, 16 5 5 cm; Fig. 12 5 10 mm; Figs. 13–15 5 5 mm; Figs. 17, 18 5 1 cm. 1304 TABLE 2. AMERICAN JOURNAL OF BOTANY [Vol. 92 Gnetalean megafossils with suggested affinities to Welwitschia. Name Location Referencea Age Notes Masculostrobus clathratus Ash Arizona Upper Triassic 1, 4, 5, 8, 14, 18 Decheyllia gormanii Ash Arizona Upper Triassic 1, 3, 4, 5 Piroconites kuespertii Gothan Germany Early Jurassic 4, 7, 8, 14 Heerala antiqua (Heer) Krassilov Angarolepis odorata Krassilov & Bugdaeva Eragrosites changii Duan Siberia Siberia Middle Jurassic Middle Jurassic China 6, 16 Axis, repro. Infructescence aff. Ephedra/Welwitschia Chaoyangia liangii Duan China 6, 16 Leaf, axis, repro. Fruit aff. Welwitschia Gurvanella dictyoptera Krassilov Cyperacites sp. Mongolia Mongolia 3, 9, 10, 12, 16 3, 5, 9, 10, 12 Eoantha zherikhinii Krassilov Lake Baikal, Central Asia Eastern North America Upper JurassicLower Cretaceous Upper JurassicLower Cretaceous Neocomian Valanginian-Barremian Barremian-Aptian Aptian 3–5 Fruits, aff. Welwitschia Infructescense. Similar to Drewria Ovulate reproductive organ. Ass. with Ephedripites Leaf, axis, repro. Leaf aff. Welwitschia. Pollen aff. Welwitschia-like Seedling, aff. Welwitschia Axis, repro., similar to Drewria Leaf, similar to Drewria Drewria potomacensis Crane & Upchurch Cratonia cotyledon Rydin, Mohr, Friis Cyperacites potomacensis Berry Conospermites hakeaefolius Ett. Brazil Eastern North America Czech Republic Aptian-Albian Albian Cenomanian 13 13 3–5, 11, 14 15 2–5 3–5, 17 Pollen organs. Pollen, Gnetaceaepollenites chinleanus, previous aff. uncertain but recent aff. is Ephedra/Welwitschia Shoots, leaves. Ass. with Masculostrobus clathratus, aff. Gnetalean Microsporophyll. Pollen, Ephedripites, aff. Ephedra/ Welwitschia Seeds, aff. Welwitschia Bracts, aff. Welwitschia a (1) Ash, 1972; (2) Berry, 1911; (3, 4) Crane, 1988, 1996; (5) Crane and Upchurch, 1987; (6) Duan, 1988; (7) Gothan, 1914; (8) van Konijnenburg-van Cittert, 1992; (9–12) Krassilov, 1982, 1984, 1986, 1997; (13) Krassilov and Bugdaeva, 1988; (14) Osborn et al., 1993; (15) Rydin et al., 2003; (16) Sun et al., 1998; (17) Velenovský and Viniklář, 1926; (18) Zavada, 1990. disappearing into the margin (Figs. 11, 12). The preservation of typical leaves allows for only an approximate vein count, with a high vein density of about 9–15 bundles/cm, with 40– 50 veins from margin to margin. The preservation of one specimen (Fig. 11) allows for an exact count of 65 veins near the base and 44 veins in the middle region. Basal veins may be 0.8–1.0 mm thick, while the veins in the mid-section of the leaf are equidistant and 0.4–0.5 mm thick. Only seven specimens were available for study, and more variation in size and form probably exists, which should be seen as more material becomes available. Discussion—Characters relating these leaves to Welwitshiella austroamericana and thus to the co-occurring fossils are parallel first-order veins that are equidistant, convergent near the apex, with some veins disappearing into the margin. Although a number of synapomorphies of Gnetales (Crane, 1996) were not observed, the following characters are similar to Welwitschia: the isobilateral form of the leaves, possible thickening of the epidermis, triangular elongated leaf shape with a wide base, longitudinal splitting from a frayed leaf apex, a somewhat thickened or creased mid-leaf area (Figs. 11, 12), and numerous parallel veins. The frayed leaves are not particularly long and may have been broken in deposition rather than as in wind-blown frayed ends of the long and large leaves of living W. mirabilis. Some of the leaf blade bases suggest an attachment around a stem, long tapering leaf length, and the rolled base, suggesting the leaf may have been enrolled into or ensheathed in deep grooves (Kubitzki, 1990). These isolated leaves somewhat resemble the long, linear, parallelveined Desmiophyllum leaves that are associated with microsporophylls of Piroconites from the Early Liassic of Franken, Germany (van Konijnenburg-van Cittert, 1992; Crane, 1996) (Table 2). The Desmiophyllum/Piroconites complex may be related to Gnetales (van Konijnenburg-van Cittert, 1992), with Desmiophyllum leaves similar to Welwitschia but without the cross veins (Doyle, 1996). Desmiophyllum-like leaves have been noted in the Crato Formation (Crane, 1996), with four illustrated specimens described as ‘‘large parallel-veined reedlike leaves of uncertain affinity’’ (Maisey, 1991, p. 429). Genus—Welwitschiostrobus Dilcher, Bernardes-de-Oliveira, Pons et Lott gen. nov. Type species—Welwitschiostrobus murili Dilcher, Bernardes-de-Oliveira, Pons et Lott sp. nov. Generic diagnosis—Cones are terminal or axillary on slender striated axes. Cones with a decussate pattern of striated scales. Each scale is folded along its median longitudinal line, giving the cone a square cross section. Scale apex acute. Etymology—Genus ‘‘Welwitschia’’ and ‘‘strobus’’ (Lat.), cone. August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM Species—Welwitschiostrobus murili Dilcher, Bernardes-deOliveira, Pons et Lott sp. nov. (Figs. 13, 14, 17, 18). Specific diagnosis—Striated axes 30–210 mm long by 2.5– 3.4 mm wide. Reproductive cones narrowly elliptic to elliptic. Cone axis diameters are 0.5–1.1 mm. Etymology—Species ‘‘murili’’ (Lat.), in honor of Prof. Murilo Rodolfo de Lima, the palynologist who assembled much of the collection of fossils used in this paper. Holotype—MNHN 40033, Muséum National d’Histoire Naturelle (MNHN), Paris. Additional specimens—GP/3E-5802, -7531. BRAZIL 1305 scribed by Pearson (1929) and ones we examined from our collection in the Florida Museum of Natural History (Fig. 15) in size, form, decussate arrangement of scales, and position on long slender axes. Attempts to prepare pollen from these fossil cones and to observe pollen in or attached to them by epifluorescence microscopy was not successful. The scales of W. murili (Figs. 13, 14) are similar to the basal scales with acute apices of Welwitschia male cones. It is difficult to observe the subtending bracts typical of Welwitschia (Pearson, 1929) in the cones of Welwitschiostrobus murili. The reproductive cones illustrated in Figs. 17 and 18 are somewhat similar to the cones in Martill et al. (1993: Plate 12, Fig. 2). For this study, only one species of fossil cone is proposed. When more material is available, the cones illustrated in Figs. 17 and 18 may yield sufficient characters to keep or remove them from W. murili. Number of specimens examined—Three. Locality—Chapada do Araripe, northeastern Brazil. Age and stratigraphy—Late Aptian, Crato Formation. Description—The reproductive cones are terminal or axillary, with a decussate pattern of paired scales. All the scales have an acute apex. The specimen MNHN 40033 (Figs. 13, 14) has an axis 33 mm long and 3 mm wide, terminating in a central cone and two opposite branches. Each branch is 30– 35 mm long and 2.5 mm wide, with the apices bearing cones organized in a dichasium. Cone scales are striated, with the apices forming the corners of a square, and curved toward the apex. The apex of the left branch bears one well-preserved cone and two fragmented and poorly preserved cones (Fig. 14). The well-preserved cone is 20 mm long and 6.5 mm wide. The central cone is partially preserved and is 17 mm long and 4 mm wide, showing a central axis approximately 0.5 mm in diameter with axillary bracts. The right lateral cone is too poorly preserved to be measured. The right axis bears cones that appear smaller and perhaps less developed than those just described. The cones at the base of this dichasium are 10 mm long and 6 mm wide. The central cone is incomplete, with scales preserved at the base and distally axillary bracts. The reproductive cones of GP/3E-5802 (Fig. 17) and GP/3E-7531 (Fig. 18) are axillary and terminal, on striated monopodial articulated axis, measuring 55–210 mm long and 3–4 mm wide. These axes bear opposite, lateral axes that emerge at nodes. Both the main axes and lateral axes are striated, and the lateral axes appear to ensheathe the axis from which they arise. It is difficult to determine whether the lateral axes represent leaves, bracts, axes, or remnants of old cone axes. The cones measure 40 mm long and 10 mm wide, with an axis 1.1 mm in diameter (Fig. 18). Discussion—The dichasial organization, in which reproductive spikes are borne both terminally and laterally at the apex of stems found in Welwitschiostrobus murili, resemble Drewria potomacensis Crane and Upchurch (1987). However, the pollen cones described here are compact cones (Figs. 13, 14, 17, 18) and are quite similar to recent Welwitschia pollen cones (Fig. 15). They are unlike the loose reproductive structures (spikes) of D. potomacensis. The specimens illustrated in Figs. 17 and 18 have opened their cone scales after pollen dispersal. Welwitschiostrobus murili represents pollen cones that are quite similar to recent Welwitschia pollen cones de- DISCUSSION The flora of the Crato Formation is considered allochthonous (Martill et al., 1993) that is reflected in the state of the preservation in our specimens. The broken or frayed tips of some leaves (Fig. 16) and a few cotyledons (Figs. 4, 9) suggest that some transport of the fossils reported here took place when much of the Crato Formation plant material was deposited. The basal portions of seedling specimens are abraded and broken at the hypocotyl with no roots preserved (Figs. 4, 7, 9, 10), suggesting that the young seedlings were broken from their growth position and transported to a site of deposition. The overall placement and character of the seedlings are reminiscent of the dispersal pattern of Welwitschia mirabilis seedlings in dry riverbeds of Southwest Africa (Pearson, 1906). It appears that these Welwitschiella seedlings represent very young plants that were ripped up and deposited when still in a cotyledon stage before bearing their first pair of foliar leaves. We suggest here that Welwitschiella specimens are probably young seedling plants in the cotyledon stage because the fossils demonstrate numerous characters of Welwitschia seedlings in the cotyledon stage detailed next. Data on extant Welwitschia is based on literature (Sykes, 1911; Rodin, 1953) and photographs, specimens, and personal communications (supplied by J. Armstrong, Illinois State University). The seeds germinate readily and remain in a cotyledon stage for several months. After approximately 6–8 mo, paired leaves are produced at the apex of the epicotyl, or short broad axis, from which the cotyledons remain attached (Fig. 5). These paired leaves are held together and grow straight up between the cotyledons. Just such a 2-yr-old seedling is illustrated by Sykes (1911). Eventually the cotyledons drop away, and the two paired leaves will fold down pointing in opposite directions, the typical form of Welwitschia familiar to most. As the axis enlarges, the width of the leaf base also increases. So the leaves shown in Figs. 11, 12, and 16 probably came from young plants with larger axes than those illustrated here in the cotyledon stage (Figs. 4, 7, 9, 10). Plants of reproductive age were present as evidenced by the pollen cones also preserved in the Crato Formation, Welwitschiostrobus murili. While these cones do not have pollen preserved, there are numerous types of Welwitschia-like pollen grains described from the Crato Formation (Table 1). Another fossil, Cratonia cotyledon, recently described from the Crato Formation, is considered to represent the cotyledon stage of a closely related genus to Welwitschia (Rydin et al., 1306 AMERICAN JOURNAL 2003). Cratonia cotyledon appears to be represented by a single specimen and has distinct chevron or ‘‘Y’’ venation that allies it to Welwitschia. The specimen consists of two broad leaves that overlap one another, a feeder and a root, but the hypocytol is reported as missing. The leaves are 40 mm long and 18 mm wide at the base and have approximately 20 main veins. In C. cotyledon, the proposed cotyledons are entirely different from cotyledons of Welwitschia (Figs. 5, 6) and Welwitschiella austroamericana described here (Figs. 4, 7–10). The leaves of C. cotyledon differ from extant cotyledons and our specimens by their broad base, more or less uniform width, numerous veins, lack of a tapering base, leaves not clasping the epicotyl axis, and the pronounced display of the ‘‘Y’’ venation pattern. The cotyledons of extant Welwitschia often appear to spread out, are narrow (maximum of 5 mm width), have few main veins (6–10), taper near their base, clasp the young axis or epicotyl partially enclosing it, and the ‘‘Y’’ pattern of venation is less well formed than in the mature leaves. Also, the axis splits and increases in diameter as the leaves are produced (Fig. 6: extant; Fig. 7: fossil, before leaves are initiated). Cratonia cotyledon is similar to what we have seen for the first postcotyledonary leaves in seedlings of Welwitschia (Figs. 5, 6) where the leaves have a broad base, from which they continue to grow, and are oriented in an overlapping fashion. Because C. cotyledon does not exhibit these characters, we suggest that it may be a seedling in an early leaf stage from which the cotyledons and portions of the axis are missing. Conversely, it may be a seedling stage of a plant with cotyledons similar to but differing in the above characters from what is known for Welwitschia today, perhaps in an extinct line of plants. Welwitschiella austroamericana, while very similar to Welwitschia seedlings in the cotyledon stage, does have some differences. The cotyledons of W. austroamericana are longer (fossil: 5–6 cm; extant: 3–4 cm) and wider (fossil: 5–6 mm; extant: 3–6 mm) compared to extant cotyledons. Also, the number of veins given in the literature (Sykes, 1911; Rodin, 1953) of approximately 6–8 in Welwitschia cotyledons is less than the 10–12 estimated in W. austroamericana. We observe only a few, poorly preserved chevrons or ‘‘Y’’ type patterns in the venation of the fossils. This may be because the chevrons or ‘‘Y’’ vein pattern in the cotyledons are the result of the presence of only a few hypodermal fibers (Rodin, 1953), in contrast to a well-formed pattern in the vascular bundles of the mature leaves of Welwitschia (Rodin, 1953). The hypodermal fibers of the cotyledons would not preserve as well as those of the mature leaf vascular bundles. Some of these differences between the extant and fossil material may be the result of where the seeds were grown. The fossils must have grown outside in an open environment, while seedlings reported in the literature were grown in greenhouses. Also, the Brazilian, Cretaceous-age plants may be a distinct population, with distinct characters, separate in time and space from the extant African populations. The similarities and differences that are found in the various fossils described here, to extant Welwitschia mirabilis, raise questions of their relationships that are reflected by our choice of taxonomic assignment. This question is compounded by the nature of our paleobotanical data. That is, we are working with isolated organs such as seedlings at the cotyledon stage, leaves, and pollen cones. We may think that they grew together as one plant, but we cannot demonstrate this because they are not in organic connection. Because of this, it is necessary to OF BOTANY [Vol. 92 assign to them an individual generic name for each isolated, unconnected organ. Also, in spite of many similarities, it is better not to assign these organs, at this time, to the modern W. mirabilis but only to the extant family. The fossils presented in this paper, the fossil reported by Rydin et al. (2003), and earlier pollen records of Lima (1978a, b, c, 1979, 1980, 1981, 1982) firmly establish the presence of Welwitschia-related plants in the Crato Formation of Brazil. Overall cotyledon form, size, basal insertion, and venation of Welwitschiella austroamericana are similar to cotyledons of Welwitschia mirabilis (Sykes, 1910, 1911). Similar leaf characters in Welwitschiophyllum brasiliense are found in Welwitschia (Kubitzki, 1990). Cone characters such as dichasial organization, size, form, position on slender axes, and decussate arrangement of scales of Welwitschiostrobus murili are similar to the pollen cone characters of Welwitschia mirabilis (Pearson, 1929; Leuenberger, 2001). Cones similar to W. murili were noted by Martill et al. (1993) from the Crato Formation. Because of all the characters of the fossils presented here, they are placed in the family Welwitschiaceae. The similarities and differences of the specific characters detailed in this report illustrate the extent to which these characters were already found in the ancestral stock of living Welwitschia. The presence of Welwitschiaceae in the Lower Cretaceous of Brazil and in the modern flora of Africa provides support for floral exchange between Africa and South America during the Mesozoic (Raven and Axelrod, 1974; Coetzee, 1993). Other fossil data suggest it continued even through the Paleogene (Dilcher, 2000; Jaramillo and Dilcher, 2001). The presence of the fossils presented here in the Lower Cretaceous of Brazil is important in the evolution and dispersal of plants in the Mesozoic. This demonstrates clearly an exchange of biota during the Mesozoic between Africa and South America. A similar link has been established with the presence of dinosaurs that also link South America, Africa, and Asia during the Lower Cretaceous (Sereno et al., 2004). This early exchange of gymnosperms must also have been taking place in a variety of angiosperms. It has been suggested that a Cretaceous biotic exchange may have been important in the dispersal of common tropical angiosperm elements between southeastern Asia, Africa, South America, and southeastern North America (Dilcher, 2000). Other megafossils with Welwitschia-like characters are recorded in both Mesozoic-age land masses of Gondwana and Laurasia (Fig. 19). They include a Cenomanian leaf from the Czech Republic, Conospermites hakeaefolius (Velenovský and Viniklář, 1926; Crane, 1988), and Decheyllia gormani from the Upper Triassic of Arizona (Ash, 1972; Crane, 1988). Although pollen associated with D. gormani and Masculostrobus clathratus resembles pollen of both Ephedra and Welwitschia, an affinity with Gnetales is uncertain due to characters of the pollen, winged seeds, and ‘‘cones’’ of leaflike microsporophylls (Crane, 1988; Zavada, 1990; van Konijnenburg-van Cittert, 1992; Osborn et al., 1993). Duan (1998) described Chaoyangia as an angiosperm fruiting axis from northeastern China, while Sun et al. (1998) suggested that these ‘‘fruits’’ are the same as those that Krassilov (1986) recognized as Gurvanella and considered them a protoangiosperm from Russia. Sun et al. (1998) pointed out that Gurvanella, with its winged seeds, is similar to those of Welwitschia and suggested that Welwitschia-like plants appear to have extended to China and Russia during the Mesozoic. Some have suggested that the presence of winged seeds indicates a closer link between Ephedra and August 2005] DILCHER ET AL.—WELWITSCHIACEAE FROM Fig. 19. Aptian palaeogeographic map showing Gnetalean microfossil (circles) and megafossil (squares) localities (see Tables 1 and 2). 1. Masculostrobus, Decheyllia, Arizona, USA, Upper Triassic. 2. Piroconites, Germany, Early Jurassic. 3. Heerala, Angarolepis, Siberia, Middle Jurassic. 4. Eragrosites, Chaoyangia, China, Upper Jurassic/Lower Cretaceous. 5. Gurvanella, Monogolia, Neocomian. 6. Cyperacites, Mongolia, Valanginian-Barremian. 7. Eoantha, Central Asia, Barremian-Aptian. 8. Drewria, Eastern North America, Aptian. 9. Equisetosporites, Aptian-Albian, Venezuela. 10. Cratonia, present study, Ephedripites, Equisetosporites, Gnetaceaepollenites, Regalipollenites, Singhia, Steevesipollenites, Brazil, Aptian-Cenomanian. 11. Gnetaceaepollenites, Steevesipollenites, Senegal, Aptian-Cenomanian. 12. Singhia, Steevesipollenites, Peru, Aptian-Cenomanian. 13. Equisetosporites, Gnetaceaepollenites, Colombia, Aptian-Cenomanian. 14. Cyperacites, Eastern North America, Albian. 15. Conospermites, Czech Republic, Cenomanian. Modified from Smith et al. (2004). Welwitschia (Zhou et al., 2003), while phylogenetic analyses based on morphology and molecular data suggest a closer link between Gnetum and Welwitschia (Crane, 1985; Doyle and Donoghue, 1986; Doyle, 1996; Bowe et al., 2000; Chaw et al., 2000; Gugerli et al., 2001; Rydin et al., 2002). Table 2 lists the various reports of possible Welwitschia-like megafossils from the Mesozoic. However, the affinities of the Triassic fossils are in dispute. The microfossil history of Welwitschiaceae is complex because of numerous name changes. The previous pollen records that have been reported as having Welwitschia affinities now have been revised to include Welwitschia, Ephedra, and even ferns (Lima and Oliveira-Babinski, 1991; Table 1). Certainly, the widespread record of pollen ascribed to Welwitschia during the Mesozoic in both land-masses of Gondwana and Laurasia should make it clear that the Mesozoic distribution of Welwitschia-like plants must have been widespread. Welwitschialike pollen was found with Drewria potomacensis (Crane and Upchurch, 1987). Welwitschia-like pollen, Welwitschiapites has been reported from the Lower Cretaceous of the Caucasus, Crimea, Austria, Hungary, Canada, and Brazil (Müller, 1966; Herngreen and Chlonova, 1981), including the Crato Formation of Brazil (Lima, 1978c; Osborn et al., 1993). The affinity of the type species of fossil pollen (Welwitschiapites magniolobatus Bolkh. ex Potonié) to Welwitschia remains uncertain (Bolchovitina, 1953; Kremp et al., 1959; Krutzsch, 1961; Jansonius and Hills, 1976). Ephedripites, Equisetosporites, and Gnetaceaepollenites, which are closely related to Ephedra and Welwitschia (Lima, 1978a; Trevisan, 1980; Crane and Ligdard, 1990; Osborn et al., 1993), have been reported from the Lower Cretaceous Crato (Santana) Formation (Table 1). Based upon such widespread reports of the pollen, we suggest this is further evidence that Welwitschia and Welwitschia-like plants were much more widespread throughout the world than previously thought. The presence of Welwitschiaceae in the Lower Cretaceous BRAZIL 1307 of Brazil may also provide insights into climatic requirements for modern Welwitschia (arid to semiarid) based upon the modern distribution of the genus, the nature of the associated fossils and the sediments, and Welwitschia-like fossils (suggested arid to semiarid to mesic). Welwitschia is capable of growing in more mesic climates and does so readily in greenhouse settings (von Willert et al., 1992; Jacobson and Lester, 2003). This suggests, along with possible aquatic plants in the Crato Formation (Duarte, 1985; Mohr and Friis, 2000), that regional climates were warm, but not arid (Doyle et al., 1982). Welwitschia-like plants eventually reached the savanna-woodland habitat of Africa (Axelrod and Raven, 1978) due to a widespread connection in the Cretaceous of South America and Africa (Raven and Axelrod, 1974; Sereno et al., 2004; Smith et al., 2004). Desertification and isolation during the Tertiary and Quaternary limited the distribution of other less drought-adapted plants (Axelrod and Raven, 1978), resulting in the isolation and endemic distribution of extant Welwitschia in southwestern Africa today (Jacobson and Lester, 2003). LITERATURE CITED ARAI, M., J. C. COIMBRA, AND A. C. SILVA-TELLES JR. 1999. Biostratigraphical synthesis of the Araripe Basin, northeastern Brazil. Anais da Academia Brasileira de Ciências 71: 816 (Abstract). ARAI, M., J. C. COIMBRA, AND A. C. SILVA-TELLES JR. 2001. 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Welwitschiaceae from the Lower Cretaceous of northeastern Brazil

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