The Early Cretaceous Aroid, Spixiarum kipea gen. et ...

Coiffard & al. • Early Cretaceous Araceae

TAXON — 13 Sep 2013: 12 pp.

PA L A E O B O TA N Y

The Early Cretaceous Aroid, Spixiarum kipea gen. et sp. nov., and implications on early dispersal and ecology of basal monocots Clément Coiffard,1 Barbara A.R. Mohr1 & Mary E.C. Bernardes-de-Oliveira2 1 Museum of Natural History, Department of Collections, Berlin, Invalidenstr. 43, 10115 Berlin, Germany 2 CEPPE-Post-Graduation and Research 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 monocotyledon from the late Early Cretaceous and extant monocots are compared. Anatomy was examined based on publications, while leaf morphology, especially the venation, required new observations on fresh and herbarium material. Spixiarum kipea gen. et sp. nov. belongs most likely to Araceae, and may be sister to Orontioideae or is even part of this tribe. Consequently, proto-Araceae were most likely present during the Early Cretaceous in South America. The occurrence of Spixiarum in South America indicates a north Gondwana origin for Orontioideae and and thus may indicate a Gondwanan origin for proto-Araceae. Sedimentological and taphonomic context indicate that Spixiarum had probably a helophytic ecology similar to living Orontioideae and formed possibly the aquatic vegetation of the Crato Lake in association with the Nymphaeales Pluricarpellatia peltata and Jaguariba wiersemana. Early Cretaceous monocotyledon remains have been rarely recorded. It is debatable if their scarceness is a sign of low diversity or may be due to taphonomic/ecologic reasons. Key words Araceae; Early Cretaceous; leaf venation; monocots; Orontioideae

Received: 12 Dec. 2012; revision received: 28 Mar. 2013; accepted 29 Aug. 2013. DOI: http://dx.doi.org/10.12705/625.21

INTRODUCTION Early monocot fossil record. — Except for a few fragmentary remains of putative Alismatales (“Pennipollis” flower, but see Doyle & al., 2008) and Araceae (Friis & al., 2010, 2011), our knowledge of early monocot evolution is poor (Herrera & al., 2008). However, reconstruction of the phylogeny of monocots in general, and Araceae more specifically, remains of great interest, even though the basic patterns have been recognized using molecular methods (Chase 2004; Cusimano & al., 2011). Araceae is today one of the most diverse monocotyledonous families. It is globally widespread growing from the wet tropics to the mid and high latitudes as far north as Alaska (Nauheimer & al., 2012). The fossil record of monocot leaves during the Early Cretaceous is restricted to one taxon, Acaciaephyllum Fontaine, from the eastern North American Potomac Group, however, its monocot nature is not generally accepted (Gandolfo & al., 2000). Reproductive structures are represented by several charcoalified flowers and inflorescences of monocots with araceous affinities from Portugal (e.g., “Araceae fossil sp. A” and “Araceae fossil sp. B”, Friis & al., 2010) as well as other putative Alismatales (Pennistemon portugallicus E.M. Friis & al.; Friis & al., 2010, but see Doyle & al., 2008). Several of the Liliacidites Robert A. Couper pollen taxa fit modern monocotyledon pollen (Doyle & al., 2008), and Mayoa portugallica E.M. Friis & al. (Late Barremian-Aptian) may also represent Araceae (Friis & al., 2004).

Early Cretaceous fossils described so far in the literature come from North America and southwestern Europe (Portugal), but no remains of monocots from South America have been reported previously. Klitzschophyllites Lejal-Nicol (Mohr & Rydin, 2002; Mohr & al., 2007) from the Early Cretaceous Crato Formation of Brazil and from northern African and southern European localities may belong to the monocots, but its affinity is not fully understood. Gomez & al. (2009) considered Klitzschophyllites Lejal-Nicol to represent a basal dicotyledon, closely related to Ranunculales, while Friis & al. (2011) considered it a spore-bearing plant, even though sporangia/spores have never been observed in connection with this plant. Thus, its relationship is still unclear. The Crato site and flora. — The plant fossils of the Crato site 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, of which plant remains are a minor part. The Crato palaeoflora is diverse, comprising about 80 taxa. Palynological studies by Lima (1989), Batten (2007) and Heimhofer (Heimhofer & Hochuli 2010) and studies of the macroflora (Mohr & al., 2007) reveal a wide array of pteridophytes and seed plants. The gymnosperm component consists of conifers (including members of Araucariaceae (Kunzmann & al., 2004), and Cheirolepidiaceae (Pseudofrenelopsis Nath., Tomaxellia S. Archang.) (Kunzmann & al., 2006), cycads, and gnetophytes. The gnetophytes are remarkably diverse with representatives of Ephedraceae (Pons & al., 1992; Osborn

Draft version for proof purposes only.

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& al., 1993; Mohr & al., 2007), Welwitschiaceae (Rydin & al., 2003), and genera not yet assigned to a family, e.g., Novaolindia L. Kunzmann & al., Cearania L. Kunzmann & al., and Cariria L. Kunzmann & al. (Kunzmann & al., 2007, 2009, 2011), and several additional taxa (Löwe & al., 2013). 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 dicot-like angiosperms. Aquatic plants possibly related to the Nymphaeales (Pluricarpellatia B.A.R. Mohr & al. and an additonal new taxon, Jaguariba wiersemana Coiffard & al. (Coiffard & al., 2013) are relatively common (Mohr & Friis, 2000; Mohr & al., 2007). A putative basal lauralean taxon, Araripia florifera B.A.R. Mohr & H. Eklund (Mohr & Eklund, 2003), shares several features with Calycanthaceae. Several stalks with free carpels attached to a receptacle might 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 therefore most likely belong to this family (Mohr & Bernardes-de-Oliveira, 2004; Mohr & al., 2013). Eudicots likely belonging to the ranunculids and basal Proteales (Mohr & al., 2007; Mohr & al., in prep.) are also present.

at the Herbarium Berolinense” (Röpert, 2000), and the published literature (Tomlinson, 1969; Hickey & Peterson, 1978; Kubitzki, 1998a, b; Keating, 2003; Riley & Stockey, 2004, Herrera & al., 2008). The morphology and anatomy of the fossil leaves were compared to those of Araceae, Taccaceae, Stemonaceae, Tecophileaceae, Asparagaceae s.l., and Zingiberales as these families showed the closest similarities. Fresh and herbarium specimens were provided by the Munich Botanical Garden and Herbarium Berolinense. Photographs of extant taxa venation were processed with GIMP. To enhance the venation, images were treated with a Gaussian border-detect algorithm and described using the terminology of Hickey & Peterson (1978). In this terminology, the vein orders are coded as A = thickest, B = thinner, C = still thinner and D = thinnest. Most of the fossil material used for this paper is maintained in the palaeobotanical collections of the Museum of Natural History, Berlin (MB. Pb.). Overall, six specimens were available for the description of Spixiarum. These are MB. Pb. X1 (the holotype), MB. Pb. 1996/1374 (the paratype), MB. Pb. 2002/1054 MB. Pb. 2002/1347, and MB. Pb. 1999/563 (an additional leaf), plus a specimen in a private collection. Following U.N. recommendations, the paratype (MB. Pb. 1996/1374) will be deposited in the country of origin (Brazil) at the Institute of Geosciences of the University of São Paulo.

MATERIALS AND METHODS RESULTS The specimens reported in this study were collected in northeastern 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 compressions 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. Coalified compressions come from the basal part of the Nova Olinda Member. The fossils were studied using a Leica Wild M8 light microscope equipped with a DFC420 digital camera. 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. Details of the epidermis (e.g., stomata, non-modified epidermal cells) were observed with a scanning electron microscope (SEM). For SEM studies, pieces of leaves were removed from the specimens, directly mounted on stubs and twice coated with Au/Pd for four minutes with a Polaron SC7640 sputter coater. SEM images were taken on a Zeiss EVO 50 SEM and processed with GIMP (v.2.6.6, GNU Image Manipulation Programme, free software, http://www.gimp.org). Leaf architecture is described based on the Manual of Leaf Architecture (Ellis & al., 2009). Leaves of extant monocots from a large number of families, focusing mainly on the clades designated as net-veined by Givnish & al. (2005), were examined in the Herbarium Berolinense, as well as on the website “Digital specimen images 2

Systematic palaeobotany

Spixiarum Coiffard, B.A.R. Mohr & Bernardes-de-Oliveira, gen. nov. – Type: Spixiarum kipea Generic diagnosis. – Plant herbaceous, rhizomatous. Roots much branched, lateral roots thin; young leaves somewhat smaller, short petiolate, older leaves with petioles three to four times longer than those of the younger leaves, emerging from the rhizome. Leaves simple with entire margin; venation parallel-pinnate, costa limited to lower half of leaves; parallel primaries recurved exmedially, higher-order parallel veins branching from the proximal side of lower-order parallel veins; highest-order parallel veins recurved exmedially, compared to lower-order parallel veins; primary transverse veins conspicuous, crossing higher-order parallel veins with an irregular course; higher-order transverse veins irregular. Derivatio nominis. – Named after the early naturalist Johann Baptist von Spix from Munich (Germany), who collected scientific material during his expedition to Brazil (1817–1820) and for the first time mentioned well-preserved fossil fishes from Early Cretaceous strata of the Araripe Basin (Santana Formation) in his report in 1828, and Arum, referring to the araceous affinities of the fossil. Spixiarum kipea Coiffard, B.A.R. Mohr & Bernardes-deOliveira, sp. nov. – Holotype: Brazil, Nova Olinda, Crato Formation (Museum für Naturkunde, Berlin, MB. Pb. X1). — Figure 1.



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Species diagnosis. – Leaf microphyllous, blade lanceolate; base acute, cuneate; apex acute, rounded; 10–20 parallel primary veins; four subsets of parallel veins arranged according to the formula AdddCdddBdddCdddA. Species description. – Spixiarum is a herbaceous plant with leaves arising directly from a rhizome (Fig. 1). The rhizome was

probably horizontal in life, and is about 5 mm in diameter. It is preserved on a length of 5 cm. Adventitious roots are up to 1.5 mm in diameter. Leaves are spirally arranged in a rosette. They are within the microphyll size class, and have entire margins. Blades are ovate, 20–40 mm wide by 50–100 mm long, with petioles that are more than 50 mm long (Fig. 2A, D) and Fig. . Spixiarum kipea gen. et sp. nov., general habit of plant (holotype, MB. Pb. X1). — Scale bar = 3 cm.


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2–4 mm wide. Base is acute, cuneate. Apices are acute and rounded (Fig. 2A, B, D). Leaf venation (Fig. 2B, C, E, F) is parallel-pinnate, only in the basal half marked by denser primaries forming a costa. Elsewhere without a visible costa (Fig. 2C). About 10–20 parallel primary veins arise near the leaf base. They are subparallel, bent outward, terminating at an angle of 20°–70° at the margin, 1.1–2.3 mm apart. Parallel secondaries branch from the proximal side of parallel primaries close to the costa and are subparallel to primaries. Parallel tertiaries (Fig. 3B) branch from the proximal side of parallel primaries and secondaries in the medial quarter of the blade. The parallel running quaternaries (Fig. 3B) are very dense, 0.2–0.5 mm apart. They are subparallel to secondaries in the medial part of the leaf and nearly perpendicular towards the leaf axis along the margin. The four subsets of veins tend to be arranged according to the formula AdddCdddBdddCdddA. The primary transverse veins (Fig. 3B) are widely spaced, oblique, nearly parallel to the leaf with irregular course. The higher-order transverse (Fig. 3B) veins are irregularly oriented. In the paratype specimen (Fig. 2A), the leaves are anatomically preserved by iron oxide. The leaves are dorsiventral, 350–400 μm thick, with epidermal cells that are polygonal (tetragonal to hexagonal) and mostly isohedral (l/w: 2.40 ± 0.38) (Fig. 4A). These cells are 82–295 μm long, 19–22 μm high and 40–117 μm wide. The anticlinal walls are straight to curved. Papillae occur on the outer surface of the cuticle (Fig. 4B). They display a primary wall that is 4.2–6.6 μm thick. The cuticle is 4.6–6.8 μm thick. The stomatal distribution is amphistomatic with scattered stomata with a density of 15–20 per mm². Their organization is anomocytic (Fig. 4C) and the apertures are longitudinally oriented (Fig. 4D). The guard cells are kidney shaped (Fig. 4E) and 40–53 μm long by 11–14 μm wide, with apertures that are 17–23 μm long and 7–13 μm wide. One layer of palisade parenchyma, 100–150 μm thick, occurs below the epidermis on the adaxial sides of the leaves (Fig. 4F). Palisade cells are more or less cylindrical (Fig. 4E) with rounded ends, 100–145 μm long by 24–52 μm in diameter. These cells display a primary wall, 2.2–5.2 μm thick (Fig. 4E). The abaxial part of leaves is composed of a spongy parenchyma layer (Fig. 4F), 170–200 μm thick, composed of cells that are disc-like, probably due to the collapse of the parenchyma (Fig. 4F, G). They are 50–100 μm wide and 10–30 μm high. Their primary walls are 2.5–5.6 μm thick. Vascular bundles are poorly preserved and measure about 100–300 μm in diameter (Fig. 4F, H). Paratype. – Institute of Geosciences, University of Sao Paulo, MB. Pb. 1996/1374 (Fig. 2A). Derivatio nominis. – Based on the indigenous people who live in the State of Cearà—“Kipeà” (Quipeà). Systematic affinity within angiosperms. — Spixiarum kipea gen. et sp. nov. is a herbaceous plant with petiolate leaves characterized by several orders of parallel/acrodromous veins converging apically and by finer cross-veins. Pinnules of ferns may show similarities to Spixiarum in gross morphology, displaying a quasi-flabellate venation that is, in fact, dichotomous. The latter pattern is especially well recognizable when this venation displays anastomoses as in Anemia phyllitidis (L.) Sw. (Fig. 3C). However, fern pinnules 4

only display a single order of venation, sometimes two when a midvein exists. More importantly, the pinnules are never more than subsessile in contrast to Spixiarum that displays rather long petioles, reaching or exceeding the length of the blade. Most of the simple-leaved ferns with distinct petioles belong to families that have a pinnate venation, although the higher-order venation can be very complex, as in Microsorum Link (Fig. 3D). Only the dipteridaceous genus Cheiropleuria C. Presl (Fig. 3E) and young plants of Dipteris Reinwardt combine simple blades and flabellate-like (dichotomous) primary venation. However, in Dipteridaceae, the higher-order venation is polygonal reticulate and does not consist of parallel veins interconnected by cross-veins as in Spixiarum. Therefore it is very unlikely that Spixiarum represents a fern. Doyle (1973) considered several orders of parallel/acrodromous veins characteristic for monocots. However, parallel veined leaves are also common in extant and fossil Gnetales (e.g., Welwitschia Hook. f., Drewria P.R. Crane & Upchurch, Cratonia Rydin & al.). Monocots differ from gnetophytes in phyllotaxis, and concerning the venation pattern, by the presence of a mid-vein, as discussed by Gandolfo & al. (2000) and Doyle & al. (2008) when comparing the Early Cretaceous monocot Acacieaephyllum Fontaine with venation patterns of gnetophytes. The authors also discussed the stomatal types of monocots (anomocytic or paracytic) and Gnetales (paracytic stomata). Furthermore the gnetophyte venation pattern is distinct because of the presence of chevron-shaped cross veins. The phyllotaxis of Spixiarum is spiral. This character excludes a close relationship with Gnetales. Venation of Spixiarum differs from the parallel-veined Gnetales by the presence of a mid-vein and by the successive fusion of the outer veins with the inner ones. Spixiarum clearly lacks chevron-shaped cross-veins and has anomocytic stomata. Thus, it is very unlikely that Spixiarum is a member of Gnetales. Gandolfo & al. (2000) pointed out that the characters used by Doyle (1973) to identify monocots may also be present in (basal) non-monocotyledon angiosperms. Among several of the early diverging lineages (excluding the core eudicots), acrodromous veins converge apically and are connected by finer crossveins. These occur among Nymphaeaceae, Piperaceae and Saururaceae. However, Nymphaeaceae are characterized by deeply cordate leaf bases (Taylor, 2008) and hydropotes (Kaul, 1976) that are absent in Spixiarum. Furthermore, Piperaceae and Saururaceae display tetracytic stomata (Kubitzki & al., 1993). In addition, none of these taxa display a higher-order venation composed of numerous parallel veins. For this reason Spixiarum is not connected to early-diverging non-monocot lineages. In summary, Spixiarum’s venation pattern fits best the one of monocots. Most net-veined monocot taxa differ from Spixiarum by their campylodromous venation. Monocots exhibiting a strong multistranded midvein (i.e., a costa sensu Hickey & Peterson, 1978) with recurved lateral primaries are observed in Araceae (Alismatales), Tacca J.R. Forst. & G. Forst. (Taccaceae, Dioscoreales), Pentastemona Steenis (Stemonaceae, Pandanales), Cyanastrum Oliv. and Kabuyea Brummitt (Tecophileaceae,



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Fig. . Spixiarum kipea gen. et sp. nov. A, permineralized leaf (paratype, MB. Pb. 1996/1374); B, leaf with venation of higher order (specimen MB. Pb. 2002/1054); C, line drawing of B showing overall leaf shape and venation pattern; D, overall leaf shape and venation (specimen MB. Pb. 2002/1347); E, folded leaf with venation (specimen MB. Pb. 1999/563); F, reconstruction of specimen in E; the folded part is graphically restored. — Scale bars = 1 cm. Draft version for proof purposes only.

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Asparagales), Hosta Tratt. (Agavoideae, Asparagaceae, Asparagales), and all Zingiberales except Lowiaceae. Among these taxa, Pentastemona and Hosta (Fig. 5A, B) have a single order of parallel veins in contrast to Spixiarum and display numerous thin higher-order transverse veins. Furthermore, Pentastemona differs from Spixiarum by its tetracytic to cyclocytic stomata (Kubitzki, 1998a). Only Araceae, Taccaceae, Tecophileaceae and Zingiberales have several orders of parallel primary veins. Zingiberales display several orders of parallel veins (Hickey & Peterson, 1978) as in Stromanthe sanguinea Sond. (Marantaceae, Fig. 5C, D; BdCdB order veins). Distally, higher-order veins fuse exmedially with lower-order veins. The higher-order veins arise from lower-order veins within or very close to the costa. This order is also characterized by transverse veins that connect only adjacent parallel veins and are mostly unbranched (Fig. 5D).

Net-veined Tecophileaceae display the same pattern of parallel veins as Zingiberales, e.g., in Kabuyea hostifolia (Engl.) Brummitt (Fig. 6A, B; BdCdB orders). Their transverse veins also connect only adjacent parallel veins but in contrast to Zingiberales, they regularly branch and anastomose. Taccaceae are represented by a single genus, Tacca. The simple-leafed species of this genus also display several orders of parallel veins (e.g., Tacca chantieri André, Fig. 6D; AdCdBdCdA orders) but a somewhat different parallel venation. Here, most of the higher-order veins arise directly from the costa but the quaternaries (d) and tertiaries (C) just below a primary tend to arise from this primary within the medial quarter of the blade. Exmedially, the higher-order veins simply decrease in size and disappear. The transverse venation connects only adjacent parallel veins and tends to be more reticulated than in Zingiberales and in Tecophileaceae (e.g., Tacca parkeri Seem., Fig. 6C).

Fig. . Details of venation of extant Orontium aquaticum L. and Spixiarum kipea gen. et sp. nov.; examples of extant ferns with reticulate venation. A, detail of venation of Orontium aquaticum; B, detail of venation of Spixiarum kipea gen. et sp. nov.; C, Anemia phyllitidis (L.) Sw.; D, Microsorum rampans (Baker) Parris; E, Cheiropleuria bicuspis (Bl.) C. Presl. — Scale bars: A, B = 5 mm; C–E = 1 cm.

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Fig. . Spixiarum kipea gen. et sp. nov. leaf anatomy. A, detail of epidermal surface; B, epidermis with papillae; C, SEM of epidermis with stomata; D, epidermis with longitudinally oriented stomata (arrows indicate the poles of the stomata); E, paradermal section of stoma with guard cells and palisade parenchyma; F, blade in cross section showing palisade parenchyma in upper part, collapsed spongy parenchyma in lower part and fragmentary vascular bundle (arrow); lower epidermis missing; G, paradermal section of spongy parenchyma; H, detail of cross section with poorly preserved vascular bundle. — Scale bars = 100 μm. Draft version for proof purposes only.

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In Taccaceae, Tecophileaceae and Zingiberales, the transverse veins are thin and connect only adjacent parallel veins. Furthermore, Zingiberales differ from Spixiarum by their paracytic stomata (Tomlinson, 1969), while the Tecophileaceae display an undiferrentiated mesophyll in contrast to Spixiarum that displays a distinct palisade parenchyma (Kubitzki, 1998a). Only Araceae display the unique combination of a costa, several orders of parallel veins and well-developed transverse veins that cross higher-order parallel veins (e.g., Lysichiton Schott, Fig. 7B). Among Araceae, the stomata are usually paracytic, but anomocytic stomata occur in Aroideae (Biarum Schott, Dracunculus Miller) and are more common in early diverging lineages such as Lemnoideae (all genera) and Orontioideae (Orontium L.) (Keating, 2003) as well as in the closely related family Tofieldiaceae (Kubitzki, 1998b). In most, but

not all cases, Araceae display a mesophyll differentiated into adaxial palisade and abaxial spongy layers (Keating, 2003). Systematic affinity within Araceae. — According to Bogner & al., (2007), Orontioideae are an exception among Araceae owing to their simplified leaf morphology and venation. The combination displayed by Spixiarum, of welldeveloped higher-order parallel venation in association with strong cross primaries and eucamptodromous marginal venation, is very similar to that of extant Orontioideae. This subfamily includes three living genera: Orontium L., Lysichiton Schott and Symplocarpus Salisb. ex Nutt. Along with Gymnostachys R. Br., these Araceae form what is often referred to as the proto-Araceae. Phylogenetic relationships among protaroids are well resolved (Cusimano & al., 2011), Gymnostachys and Orontium being the sister taxa of Lysichiton and Symplocarpus.

Fig. . Examples of extant monocots with well-developed mid-costa. A, Hosta sp.; B, detail of A; C, Stromanthe sanguinea Sond.; D, detail of C. — Scale bars = 1 cm.

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Compared to other protaroids, Spixiarum displays a unique combination of characters. It shares with Lysichiton and Symplocarpus the sigmoid lateral primaries (Fig. 7B) but shares with Orontium the weak development of the mid-costa (Fig. 7A). Otherwise, the higher-order of parallel venation of Spixiarum is similar to Lysichiton (Fig. 7B) and Orontium (Fig. 3A), tending to be acute to primaries. The parallel orientation of stomata may be a symplesiomorphy, shared with Gymnostachys R. Br., which also diplays larger and smaller parallel veins (Keating, 2003). However, Gymnostachys differs from Spixiarum by its parallel venation and by its lack of mesophyll differentiation (Keating, 2003). Furthermore, Spixiarum displays unique characteristics: the obtuse orientation of the cross-primaries and parallel secondaries and tertiaries that branch outside the costa.

DISCUSSION Cretaceous fossil record of Araceae. — The Early Cretaceous record of Araceae consists of only two reports of reproductive structures from Portugal (Friis & al., 2010). These two taxa, “Araceae fossil sp. A” and “Araceae fossil sp. B” show affinities with the unisexual-flowered clade (viz. subfamilies Lasioideae, Zamioculcadoideae and Aroideae), and subfamily Pothoideae respectively, but these fossils may belong to the Monstereae of subfamily Monsteroideae (J. Bogner, pers. comm.). This indicates that subclades as also known in living Araceae were already present during the Late Aptian–Early Albian. Another fossil from Portugal, Mayoa portugallica E.M. Friis & al., is slightly older (Late Barremian–Aptian) and may also represent remains of Araceae (Friis & al., 2004, but see Hofmann & Zetter, 2010).

Fig. . Venation of selected extant monocots with developed mid-costa. A, Kabuyea hostifolia (Engl.) Brummitt; B, detail of A; C, Tacca parkeri Seem.; D, Tacca chantieri André. — Scale bars = 1 cm.


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From the Campanian on, the fossil record of Araceae becomes much richer. Monsteroideae are represented by the permineralized stem Rhodospathodendron tomlinsonii Bonde from the Maastrichtian of India (Bonde, 2000). Aquatic Araceae and relatives are quite common, being represented by the lemnoid Limnobiophyllum scutatum (Dawson) Krassilov from the Latest Cretaceous of North America and East Russia (Kvaček, 1995; Stockey & al., 1997; Bogner, 2009). Cobbania corrugata (Lesq.) Stockey & al., a possible member of Araceae, is also widespread from the Campanian in North America and Far East Russia (Stockey & al., 2007). Orontioideae occur during the Upper Cretaceous, e.g., the reproductive structure Albertarum pueri Bogner & al. from the Campanian of Alberta (Bogner & al., 2005). Leaf fossils that are more comparable to Spixiarum represent three existing genera. The oldest one is Lysichiton austriacus (J. Kvaček & A.B. Herman) Bogner & al. from the Campanian of Grünbach in Austria (Kvaček & Herman, 2004; Bogner & al., 2007). The two other fossils are Maastrichtian in age. Orontium mackii Bogner & al. comes from Mexico and Symplocarpus hoffmaniae Bogner & al. from North Dakota (Bogner & al., 2007). These three fossils show the same venation pattern as the living genera, and thus differ from Spixiarum.

Fig. . Venation in extant Orontioideae. A, Orontium aquaticum L. B, Lysichiton americanus Hultén & H. St. John. — Scale bars: 1 cm.

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Palaeobiogeography. — The age of the fossil (112–115 Ma) is at the upper boundary of the confidence interval found by Nauheimer & al. (2012) for the divergence between Orontioideae and Gymnostachys (73–115 Ma), indicating that the fossil probably just postdates this divergence. The occurrence of Spixiarum in South America thus indicates a north-Gondwanan origin for Orontioideae. This and the extant occurence of Gymnostachys in Australia suggests that proto-Araceae originated in Gondwana during the Early Cretaceous. A Gondwanan origin of Araceae is also supported by the occurrence of “true Araceae” (with more characters of modern Araceae in contrast to “fossil sp. A”) in Aptian strata from Portugal. Palaeogeographically the southern parts of the Iberian Peninsula belong to a transition zone between Laurasia and Gondwana with several shared floral elements (e.g., Klitzschophyllites Lejal-Nicol; Mohr & al., 2006; Gomez & al., 2009). Overall, the new observations support palaeobiogeographic considerations of Bremer & Janssen (2006) who suggested a Gondwanan origin of monocots. The existence of orontioid fossils in Europe and North America during the Late Cretaceous (Bogner & al., 2007) indicates that this dispersal probably took place during the Mid-Cretaceous. During the Late Cretaceous several clades of well-differentiated monocots that seem to appear suddenly are reported from mid-latitudes, especially Arecaceae and Pandanaceae (Coiffard & Gomez, 2010). This may be analogous to the poleward dispersal of eudicots hypothesized by Hickey & Doyle (1977). Both may be caused by the global poleward shift of vegetation during the Cretaceous that apparently played an important role in angiosperm diversification (Coiffard & Gomez, 2012). Palaeoecology. — According to Givnish & al. (2005), all origins of net venation among monocots are associated with shady conditions or broad-leaved emergent or submersed aquatics. This confirms the earlier observations that net venation occurs in several monocot groups in forest understories, including Arisaema Mart., Smilax L., Trillium L. and various tropical gingers (Givnish, 1979), or in broad-leaved forest vines, though the reasons for the development of net-venation is not clear (Conover, 1983; Chase & al., 1995; Roth-Nebelsick & al., 2001). Thus the net-venation of Spixiarum may be seen in connection with its habitat, possibly the understory of forest vegetation or lakes or swamp vegetation (see above). Living Orontioideae are helophytes. This ecology appears to be plesiomorphic among Araceae (Cusimano & al., 2011), and it may be assumed that Spixiarum grew under similar ecological conditions. This assumed ecology of Spixiarum is also supported by the occurrence of truly aquatic plants in the Crato flora, represented by the Nymphaeales, Pluricarpellatia B.A.R. Mohr & al. (Mohr & al., 2008) and Jaguariba Coiffard & al. (Coiffard & al., 2013). Other representatives of the vegetation, however, display adaptations to (seasonal) drought, such as small coriaceous leaves or scales (e.g., the angiosperms Endressinia B.A.R. Mohr & Bernardes-de-Oliveira and Schenkeriphyllum B.A.R. Mohr & al., Gnetophytes, and the conifer Brachyphyllum Brongniart). They correspond most likely to allochtonous



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elements in the taphoflora. Pluricarpellatia and Spixiarum, on the other hand, are probably parautochtonous, having grown along the Crato Lake margins.

ACKNOWLEDGEMENTS The authors would like to thank several staff members of the Museum of Natural History, Berlin for their steady support. Kirsten Born helped with the handling of the SEM, Hwa-Ja Götz took pictures of the macro-fossils, Sarah Löwe did some editorial work, and Dr. David Lazarus improved the English. Dipl. Phys. H.-U. Schenker (Kirchhain) supported our working group by the loan of one specimen. Prof. Dr. Susanne Renner and Dr. Josef Bogner provided living material from the Botanical Garden of Munich, and gave useful comments.

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