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Pa l a e o b o ta n y
Jaguariba wiersemana gen. nov. et sp. nov., an Early Cretaceous member of crown group Nymphaeales (Nymphaeaceae) from northern Gondwana Clément Coiffard,1 Barbara A.R. Mohr1 & Mary E.C. Bernardes-de-Oliveira2 1 Museum of Natural History, Leibniz Institute for Research on Evolution and Biodiversity, Department of Collections, Invalidenstr. 43, 10115 Berlin, Germany 2 CEPPE-Post-Graduation, Research and Specialization Centre of the University of Guarulhos, Praça Theresa Cristina 1, 07023-070, Guarulhos (SP) Brazil; and Institute of Geosciences, University of São Paulo, Rua do Lago 562, Cidade Universitaria, 05508-080, São Paulo, Brazil Author for correspondence: Clément Coiffard,
[email protected] Abstract Morphology and anatomy of a fossil nymphaealean plant, Jaguariba wiersemana gen. nov. et sp. nov. from the late Early Cretaceous of northeastern Brazil, and extant aquatic flowering plants are comparatively studied. Characteristic features indicate that Jaguariba gen. nov. is a member of Nymphaeaceae, and may belong to Nymphaeoideae. The occurrence of both Nymphaeaceae and Cabombaceae (e.g., Pluricarpellatia peltata) in the Lower Cretaceous contradicts recent molecular dating implying a Late Cretaceous–Early Tertiary divergence for those families. Furthermore, the morphology of the fossil and sedimentologic and taphonomic data indicate that Jaguariba gen. nov. had an aquatic ecology similar to living Nymphaeaceae. Thus the taxon was part of the aquatic vegetation of the Crato lake in association with Pluricarpellatia peltata, an earlier described cabombaceaen aquatic angiosperm. Keywords Cabombaceae; Early Cretaceous; morphology; Nymphaeaceae; South America
Received: 20 June 2012; revision received: 2 Oct. 2012; accepted: 28 Oct. 2012.
Introduction Aquatic angiosperms are well-represented in the Lower Cretaceous (145–100 Ma); they are certainly present since the Barremian (130–125 Ma). One of these ancient taxa, Archaefructus Ge Sun & al. (Sun & al., 1998; Friis & al., 2003; Endress & Doyle, 2009) from China, had possible affinities to early Nymphaeales. Another aquatic angiosperm, Montsechia vidalii (Zeiller) C. Teixeira found in Spain (Gomez & al., 2006), is of unknown affinities. By the Aptian-Albian, water plants became more common and comprised taxa of uncertain affinities such as Klitzschophyllites Lejal-Nicol, from the late Aptian–late Albian of the northern Gondwana region (Mohr & Rydin, 2002, Mohr & al., 2006; Gomez & al., 2009), as well as various nymphaealean taxa. Ploufolia cerciforme Sender & al. (late Albian, Sender & al., 2010) is considered to represent a nymphaealean taxon. Nelumbites E.W. Berry, from the late Albian of North America (Upchurch & al., 1994) seems to represent the oldest aquatic Nelumbonaceae (Proteales). The early appearance of Nymphaeales is not surprising, because Nymphaeales are the second branching clade among the extant basal angiosperms. Nymphaeales are not only present among fossils in the Early Cretaceous because of their old age, but also because of their aquatic habitat, which makes this clade prone to fossilization. Among Nymphaeales, Cabomb aceous affinities have been suggested for three taxa during the Early Cretaceous. They include Pluricarpellatia peltata
B.A.R. Mohr & al. from the late Aptian (Mohr & al., 2008), Scutifolium jordanicum David W. Taylor & al. from the Albian (Taylor & al., 2008), and Brasenites kansense Hongshan Wang & Dilcher from the late Albian (Wang & Dilcher, 2006). Despite the relatively common occurrence of aquatic angiosperms in the Lower Cretaceous, finds of Nymphaeaceae are scarce. Fossils of this family are recorded since the early Albian with the mesofossil Monetianthus mirus E.M. Friis & al. (Friis & al., 2009) and from Turonian strata with Microvictoria svitkoana Nixon & al. (Gandolfo & al., 2004, but see Endress, 2008). Nymphaealean seeds from the early Santonian of Japan have been found to show features of Cabombaceae/Nymphae aceae, but cannot be attributed to any living taxon with certainty (Takahashi & al., 2007). Exotestal and operculate seeds similar to those of Nymphaeales are also known from the early Albian of Portugal (Friis & al., 2010). So far the oldest unequivocal megafossil of Nymphaeaceae is “Nymphaea ” mesozoica Dobruskina from the Turonian (ca. 90 Ma) of Israel (Dobruskina, 1997). Aquatifolia fluitans Hongshan Wang & Dilcher (Wang & Dilcher, 2006) from the late Albian is most likely an early divergent member of Nymphaeaceae, though it displays several features such as petiolar floats that are unknown in living Nymphaeaceae (Wang & Dilcher, 2006). In contrast to this Cretaceous record, recent molecular dating infers a young age for the divergence of Cabombaceae and Nymphaeaceae. Yoo & al. (2005) estimated that Cabomb aceae and Nymphaeaceae diverged during the Paleogene.
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The Crato flora is one of the few Lower Cretaceous equatorial floras. Compared to mid-latitude palaeofloras of similar age (e.g., the Lower Zone I flora of the Potomac group, Doyle & Hickey, 1976; Hickey & Doyle, 1977; Hochuli & al., 2006), the Crato flora is diverse and contains many angiosperms, especially representatives of rather derived clades such as magnoliids, monocots and eudicots. Therefore the finds of crowngroup nymphaealean taxa are not completely surprising.
Materials and methods The Crato flora. — The studied plant fossils come from open air pits in the area of Santana do Cariri (northeastern Brazil) where the Early Cretaceous Crato plattenkalk limestone is mined for construction purposes. The outcrops yield a broad range of fossils, including plant remains. The Crato palaeoflora is highly diverse, comprising about 80 taxa. Palynological studies by Lima (1989), Batten (2007) and Heimhofer & Hochuli (2010), plus studies of the macroflora (Mohr & al., 2007) reveal a wide array of spore-bearing and seed plants. The gymnosperm component consists of conifers, cycads and gnetophytes and includes members of Araucariaceae (Kunzmann & al., 2004) and Cheirolepidiaceae (Pseudofrenelopsis Nath. and Tomaxellia S. Archang.) (Kunzmann & al., 2006). The gnetophytes are remarkably diverse with representatives of Ephedraceae (Osborn & al., 1993; Mohr & al., 2007), Welwitschiaceae (Rydin & al., 2003) and members not yet described families such as Nova olindia L. Kunzmann & al., Cearania L. Kunzmann & al. and Cariria L. Kunzmann & al. (Kunzmann & al., 2007, 2009, 2011) and several additional taxa (Löwe & al., in press; Mohr & al., 2012). The angiosperm component of the Crato flora is unique, in that flowering structures connected to vegetative parts are preserved. Almost all of these plant fossils belong to dicotyledonous angiosperms. Water plants, some closely related to the Nymphaeales (Pluricarpellatia and the nymphaealean taxon described here), are relatively common (Mohr & Friis 2000; Mohr & al., 2007). A putative basal lauralean taxon, Araripia florifera B.A.R. Mohr & H. Eklund, shares several features with Calycanthaceae (Mohr & Eklund, 2003). Several stalks with free carpels attached to a receptacle may be of magnolialean origin (Mohr & Friis 2000). Endressinia B.A.R. Mohr & Bernardes-de-Oliveira and Schenkeriphyllum B.A.R. Mohr & al. seem to be closely related, share many characters with Magnoliaceae and belong most likely to this family (Mohr & al., 2013, but see Doyle & Endress, 2010). Eudicots were present as well, most likely belonging to ranunculids and to basal Proteales (Mohr & al., 2007). Treatment of the material. — The specimens reported in this study were collected in the Northeast of Brazil from open cast pits close to the town of Nova Olinda, between Nova Olinda and Santana do Cariri (State of Ceará). The fossils are preserved as reddish brown iron oxide permineralizations or light brown impressions on light yellow-brown limestone slabs. The iron oxide of the compression material can be very brittle and crumbly. Epidermal cell structures and vascular tissues are rarely preserved. 142
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The fossils were studied under a Leica Wild M8 Light Microscope (LM) and a digital camera DFC 420. Cellular details of the epidermis of the leaves, such as anatomy and arrangement of stomata, or arrangement of non-modified epidermal cells, were partly visible under the light microscope. Characteristics of the anatomy (stomata, non-modified epidermal cells, etc.) were observed with the scanning electron microscope (SEM). For SEM studies, differently sized pieces of the leaves were removed from the specimens, directly mounted on stubs and sputtered for 4 minutes with Au/Pd on a Polaron SC7640 sputter coater. The SEM-photographs were taken on a Zeiss EVO 50 SEM. Images were processed with GIMP v.2.6.6 (http://www.gimp.org). The leaf architecture was described according to the Manual of Leaf Architecture (Ellis & al., 2009). The phylogenetic analysis was performed by adding the fossil states to an existing phylogenetic dataset created for Nymphaeales based on vegetative characters (Taylor, 2008). It included all 33 taxa of the original analysis with the addition of Jaguariba. The fossil was coded 11?01002111122221111011 30202130001?20? (for character description, see Appendix 1). Maximum parsimony analyses were conducted using PAUP* v.4.0b10 (Swofford, 1999). All characters were unordered and heuristic searches were made using 1000 random-addition replicates with tree-bisection-reconnection (TBR) branch swapping with MULTREES on. The material used for this paper is housed in the palaeobotanical collections of the Museum of Natural History, Berlin (MB. Pb.). Overall, five specimens were available for the description of Jaguariba. These are the type specimen (MB. Pb. MB. Pb. 1997/1291), the paratype (MB. Pb. 1999/615), another more or less complete plant (MB. Pb. 1999/614), an additional leaf (MB. Pb. 1999/612), plus a specimen in a private collection. Following UN recommendations, the paratype (MB. Pb. 1999/615) will be deposited in the country of origin (Brazil) at the Institute of Geosciences of the University of São Paulo.
Systematic Description Order Nymphaeales Dumort. Family Nymphaeaceae Salisb. Jaguariba Coiffard, B.A.R. Mohr & Bernardes-de-Oliveira, gen. nov. – Type: Jaguariba wiersemana Generic diagnosis. – Herbaceous plant with leaves arising directly from a rhizome. Leaves alternate, simple, petiolate, peltate (attachment of lamina very eccentric). Base wide obtuse, lobate. Apex obtuse, rounded. Primary venation actinodromous, 9 primary veins radiating from the base. Secondary venation festooned brochidodromous with excostal venation in the outer 1/4 of the lamina. Agrophic veins compound. Spacing of secondary veins increasing toward the base. Angle of secondary veins: one pair of acute basal secondaries. Course of secondary veins mostly zig-zag, due to deflection at origin of tertiaries, curved upward. Intersecondaries weak. Tertiary veins mixed opposite/alternate near mid-vein and random reticulate near margin. Tertiary veins convex and sinuous. Angle
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of tertiary veins to primary veins obtuse. Angle variability of tertiary veins inconsistent. Quaternary veins regular polygonal reticulate. Derivatio nominis. – Jaguariba is derived from the Rio Jaguaribe, the main river of the Ceará state. It means the “jaguar’s river” in the Tupi-Guarani language. Jaguariba wiersemana Coiffard, B.A.R. Mohr & Bernardesde-Oliveira, sp. nov. Holotype: MB. Pb. 1997/1291 (Repository: Museum für Naturkunde, Berlin) Paratype: MB. Pb. 1999/615 (Repository: Institute of Geosciences, University of São Paulo). Type locality: Brasil, Nova Olinda, Region Araripe, open carst pit. Type stratum: Crato Formation, Nova Olinda member Species diagnosis. – Lamina nano- to notophyll, elliptic to slightly ovate. Basal extension length / lamina length ratio
