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Review of Palaeobotany and Palynology 222 (2015) 116–128

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Phytogeographic, stratigraphic, and paleoclimatic signiﬁcance of Pseudofrenelopsis capillata sp. nov. from the Lower Cretaceous Crato Formation, Brazil

Paula Andrea Sucerquia a,b,⁎, Mary E.C. Bernardes-de-Oliveira a, Barbara A.R. Mohr c a Instituto de Geociências, Universidade de São Paulo, Rua do Lago 562, Cidade Universitária, CEP 05508–080, São Paulo, SP, Brazil b Departamento de Geologia, Universidade Federal de Pernambuco, Avenida Acadêmico Hélio Ramos s/n, Cidade Universitária, CEP 50740–530, Recife, PE, Brazil c Museum of Natural History, Collections, Invalidenstrasse 43, 10115 Berlin, Germany article info abstract

Article history: Coniferales are represented during the Early Cretaceous in northern South America both by macrofossils and Received 9 September 2013 palynomorphs of the families Araucariaceae and Cheirolepidiaceae. Fossils of Cheirolepidiaceae are often abun- Received in revised form 1 July 2015 dant in coastal deposits; plants of this family are considered to have grown under semiarid to arid climate con- Accepted 30 July 2015 ditions because of characteristic anatomical features which include several adaptations to aridity and/or Available online 28 August 2015 salinity. Here histologically preserved specimens of Pseudofrenelopsis from laminated limestones of the Crato For- mation (Araripe Basin, NE Brazil) were studied by light and scanning electron microscopy. A new species Keywords: Pseudofrenelopsis capillata Pseudofrenelopsis capillata sp. nov. is described which seems to have grown exclusively at the Early Cretaceous Cheirolepidiaceae (sub)paleoequatorial area of South America and may be therefore endemic. The new taxon may have grown in Histology a riparian environment along the borders of a large lake as a minor constituent of the surrounding vegetation. Climate sensitivity © 2015 Elsevier B.V. All rights reserved. Crato Formation Early Cretaceous

1. Introduction triradiate scar and a distal cryptopore, where the exine is thinner. The pollen also exhibits a circumpolar ridge or rimula just above the equator During the Early Cretaceous, global vegetation was dominated by towards the distal pole. Around the equator, the exine is thickened, like gymnosperms, which were affected by a rapid evolution of the angio- a belt and is usually ribbed on the inside (Srivastava, 1976; Watson, sperms towards the mid- to Late Cretaceous. Several gymnosperm 1988). Classopollis pollen grains bear diversified external sculptures groups became extinct or were dramatically reduced at the end of this and orbicules in the pollen grain surface, which may be of taxonomic period. The conifer family Cheirolepidiaceae did not surpass the relevance (Reyre, 1970). Cretaceous–Paleogene boundary. The possibly youngest member of Abundant Classopollis in palynological assemblages is considered to Cheirolepidiaceae may be Brachyphyllum patens from the Maastricht represent coastal deposition under arid climatic conditions. Thus it is Formation of SE Netherlands and NE Belgium (van der Ham et al., 2003). used to define floristic regions and arid areas (Vakhrameev, 1970, Cheirolepidiaceae have been traditionally defined by a single 1991). Vegetative parts of several taxa have morphologies supporting character: the morphology of pollen grains of the genus Classopollis the hypothesis that they grew in an arid or at least seasonally dry Pflug (Doludenko, 1978; Watson, 1988), formerly named Corollina habitat (Watson, 1988). Reduced leaves, very thick cuticles, sunken Maljavkina or Circulina Maljavkina (Pocock and Jansonius, 1961; stomata, and fleshy appearance of branches and leaves speak for the Traverse, 2004). According to the pollen record, Cheirolepidaceae xeromorphic nature of Cheirolepidiaceae (Upchurch and Doyle, 1981). range from the Late Triassic to the Late Cretaceous (Reyre, 1973; Maximum abundances are related to stratigraphic intervals and regions Srivastava, 1976), with a cosmopolitan distribution, but minor abun- showing lithologic and paleobotanical evidence of aridity expressed as dance at high latitudes (Vakhrameev, 1970; Brenner, 1976). red beds or evaporites, low diversity of ferns and low diversity of large Classopollis is easily recognizable in sporomorph assemblages. This leaved gymnosperms. Its decline at the end of the Cretaceous period pollen type occurs both as single grains as well as in tetrads. When sin- may be related to less severe weather conditions, when the global cli- gle, the grains have an approximately spherical form, with a proximal mate was overall cooler, and at low latitudes with higher precipitation rates. Although representatives of this family show generally a strong ⁎ Corresponding author. Tel.: +5581998008124. xeromorphic appearance, the vegetative morphology is highly variable, E-mail address: [email protected] (P.A. Sucerquia). with two types of leafy branches, the Brachyphyllum–Pagiophyllum type

http://dx.doi.org/10.1016/j.revpalbo.2015.07.012 0034-6667/© 2015 Elsevier B.V. All rights reserved. P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128 117 with adpressed and ﬂeshy or falcate leaves, in spiral arrangement, and the the families Araucariaceae and Cheirolepidiaceae, including vegetative Frenelopsis–Pseudofrenelopsis type with jointed stems, thick internode cu- and reproductive remains, though not found in organic connection. ticles, sheathing leaf bases, and reduced free leaf tips, also known This paper considers vegetative remains of Pseudofrenelopsis from the informally as frenelopsids (Watson, 1988; Axsmith et al., 2004). Crato Formation. Brachyphyllum–Pagiophyllum type twigs are found almost during the entire Mesozoic globally distributed, while the frenelopsids are restricted to 2. Geological setting the Cretaceous of North America and South America, Europe, Africa and Asia, and are frequently used as environmental indicators of tropical to The Crato Formation is an upper Aptian lithologic unit of the subtropical arid climate (Alvin, 1982). Araripe Basin. This basin extends over an area of approximately In South America, frenelopsids are recorded from the Crato and 8000 km2 between 38°30′–40°50′ Wlongitudeand7°05′–7°50′ S Romualdo Formations, Araripe Basin, northeastern Brazil, as Frenelopsis latitude, occupying parts of the States Piauí, Ceará, Pernambuco, sp. (Kunzmann et al., 2006) and Pseudofrenelopsis sp. (Bernardes-de- and Paraiba in a nearly rectangular shape, with a EW longitudinal Oliveira et al., 2013). Records exist also from the Paja and Villeta Forma- axis (Fig. 1). It is formed by Paleozoic and Mesozoic sedimentary tions, Colombia, of the two genera Pseudofrenelopsis and Frenelopsis sequences covering the Precambrian basement. Its origin and evolu- (Moreno-Sánchez et al., 2007), but their preservational state does not tion are related to the tectonic events responsible for the fragmenta- allow a species determination. tion of Gondwana, separating the South American and African plates The ages of these four lithological units range from the Aptian to and the consequent establishment of the South Atlantic Ocean early Albian. They share paleoﬂoras composed of abundant conifers of (Ponte and Ponte-Filho, 1996).

Fig. 1. Outcroping area of Crato Formation (after Martill, 2007) and location of limestone quarries between Nova Olinda and Santana do Cariri, State of Ceará, northeast Brazil. 118 P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128

The Crato Formation is composed of laminated limestones 3. Material and methods interbedded with siltstones deposited in a lacustrine environment. The paleolake, which gave rise to this unit, developed under a tropical–sub- The fossil plants are preserved in light yellow to grayish brown lam- tropical paleoclimatic regime (Neumann et al., 2003). The water body inated limestones, preserved as coalified compressions with cuticles, was permanently stratified with hypersaline and anoxic bottom waters, iron oxides casts with epidermal and anatomical features preserved but well-mixed and productive in the surface waters (Heimhofer and and impressions. Most fossils were presumably found in Pedra Cariri Martill, 2007). Halite pseudomorphs and lack of indicators of benthonic quarries located between the towns of Santana do Cariri and Nova life are interpreted as evidence of a bottom brine in the lacustrine system Olinda in the State of Ceará, Brazil. (Neumann et al., 2003). The studied material is housed in the paleobotanical collection of the The age of the Crato Formation is considered to be late Aptian (Pons Museum für Naturkunde der Humboldt-Universität, Berlin (Mb.Pb. et al., 1990; Heimhofer and Hochuli, 2010), which corresponds to the 2002/1344), in the scientific collection of the Departamento de Geologia Sergipea variverrucata Palynozone (P-270) from the Meso-Alagoas Sedimentar e Ambiental, Instituto de Geociências/Universidade de São Brazilian local stage. This zone also represents the late Aptian (Arai Paulo (GP/3E 9118, GP/3E 9380), and at the scientific collection et al., 2001) and equals the Cytheridea Ostracozone (NRT-011). of the Instituto de Geociências, Universidade Federal de Rio de The fossil assemblage of the Crato Formation contains abundant in- Janeiro (UFRJ Pb 428a). The frenelopsid specimen SM.B.16447 sects, fishes, and plants. Macro- and microfloral remains are diverse (Senckenberg Forschungsinstitut und Naturmuseum, Frankfurt), figured and include ferns, conifers, gnetales, and angiosperms, overall about and described by Kunzmann et al. (2006) as Frenelopsis sp., was also 70–80 taxa. Approximately 60% are gymnosperms, 35% are angio- reviewed. sperms, and approximately 5% are ferns. However, the sporomorph con- The fossils were studied under a ZEISS Stemi SV6 Stereomicroscope tent shows a rather different distribution of taxa: Gymnosperm pollen, with magnifications from 8 to 200×. Photomacrographs were taken including many gnetoid taxa, are dominant, with 52% against 32% of with a Canon EOS Rebel T2i, with 18 MP (Plate I,Figs.1–8; Plate IV, the species richness of ferns and 16% of angiosperms (Lima, 1978). Figs. 1–2). Among the gymnosperms Gnetales and conifers of the families Material with preserved anatomical details was studied on SEM. Araucariaceae and Cheirolepidiaceae are the most significant compo- Little fragments of fossils preserved in iron oxide preservation were nents in both the macro- and microflora of the Crato Formation. Howev- removed from the specimens and mounted on stubs with carbon con- er, megafossils of Cheirolepidiaceae are very rare in comparison with ductive tape, then covered with a 100–200 nanometers gold layer. Pho- Araucariaceae. Cheirolepidiaceae comprise, besides very few specimens tographs were taken at a LEO 440 I Scanning Microscope (Plates II–IV, of frenelopsids, few last order twigs of Tomaxellia (Kunzmann et al., Figs. 3–4). 2006; Mohr et al., 2007) and branches of Duartenia (Mohr et al., Cuticles were removed from fossils with needle and treated with

2012), both most likely endemic to South America (Archangelsky and 100% nitric acid (HNO3) at 100%, for about 24 hours, later with 10% del Fueyo, 2010; Mohr et al., 2012). While the branches of Duartenia potassium hydroxide (KOH). After washing in distilled water, a are usually very abraded and may thus come from the hinterland, the dehydratation with ethylic alcohol was necessary for staining with saf- rare specimens of Pseudofrenelopsis and Tomaxellia are usually some- ranin in alcoholic solution. These cuticles were mounted on slides with what better preserved. Entellan. The cuticles were observed in a Carl Zeiss Axiophot II

Plate I.

1. Pseudofrenelopsis capillata sp. nov. Branched shoot with spiral phyllotaxy. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 2 cm. 2. Shoot fragment with long internodes and leaves in 2/5 spiral phyllotaxy. Numbers 1–5, leaves of the same helix. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 1 cm. 3. Shoot fragment with short internodes and leaves in 2/5 spiral phyllotaxy. Numbers 1–5, leaves of the same helix. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 1 cm. 4. Detail of free tip (t) of a leaf on a large internode. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 1 mm. 5. Detail of free tip (t) of a leaf on a short internode. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 1 mm. 6. Pseudofrenelopsis capillata sp. nov. Branched shoot with spiral phyllotaxy. Specimen UFRJ Pb 428a. Scale bar = 4 cm. 7. Detail of internode with leaves (l) and stele (s) with 1/3 of the total width of shoot. Specimen UFRJ Pb 428a. Scale bar = 5 mm. 8. Pseudofrenelopsis capillata sp. nov. Non-branched shoot with preserved cuticles. Specimen GP/3E 9118. Scale bar = 2 cm.

Plate II. (see on page 120)

1. Leaf apex showing rows of stomata and hairs at the edge. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 1 mm. 2. SEM detail of hairs at the apical edge of a leaf. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 100 μm. 3. Outer abaxial cuticle with stomata arranged in uniseriate rows and ordinary epidermal cells with rounded papillae. Specimen GP/3E 9118. Scale bar =100μm. 4. Outer abaxial cuticle with stomata arranged in uniseriate rows and rounded papillae of epidermal cells. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 100 μm. 5. Inner abaxial cuticle showing uniseriate rows of circular stomata, with elongated epidermal cells between rows and polygonal epidermal cells whitin them. Stomatal apertures oriented mostly oblique. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 100 μm. 6. Outer abaxial cuticle with two adjacent stomata, subsidiary cells with papillae. Specimen GP/3E 9118. Scale bar = 50 μm.

Plate III. (see on page 121)

1. Inner abaxial cuticle with circular stomata and surrounding epidermal cells. Stomata with ﬁve subsidiary cells (sc) and guard cells (gc) with ledges (arrow). Anticlinal walls of epidermal cells thicker than those of subsidiary cells. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 20 μm. 2. Outer abaxial cuticle showing stomatal aperture with sunken guard cells and papillae protruding from subsidiary cells closing the aperture. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 20 μm. 3. Outer abaxial cuticle showing stomatal aperture closed by papillae protruding from subsidiary cells. Rounded papillae at cuticle surface. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 20 μm. 4. Inner abaxial cuticle showing circular stomata in rows and elongated epidermal cells between the rows and polygonal shape within the stomata. Stomatal apertures oriented obliquely to the rows. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 60 μm. 5. Inner abaxial cuticle in the basal area of the leaf with circular stomata arranged in rows. Towards the base of the leaf (lower part of the picture), stomata frequency lower and stomata more spaced, epidermal cells between the stomata rows more elongated if compared with those of the middle part of the leaf. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 100 μm. 6. Abaxial cuticle in cross section. Specimen MB.Pb.2002/1344 (holotype). Scale bar = 20 μm. P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128 119 microscope, and photomicrographs were taken with a digital camera 4. Systematic paleobotany Sony Cyber Shoot DSC-S75 of 3.3 megapixels attached to the microscope. Unstained cuticles were examined with the SEM following the Order Coniferales Jussieu same procedure as described for the iron oxide fragments. Family Cheirolepidiaceae Takhtajan

Plate I. 120 P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128

Plate II. (caption on page 118). P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128 121

Plate III. (caption on page 118). 122 P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128

Plate IV.

1. Outer abaxial cuticle with an isolated stoma (arrow) and hairs on epidermal cells. Specimen GP/3E 9118. Scale bar = 100 μm. 2. Outer abaxial cuticle showing long hairs on periclinal walls of epidermal cells. Specimen GP/3E 9118. Scale bar = 100 μm. 3. Wood with helical thickenings and uniseriate areolate pits in tracheids. Specimen UFRJ Pb 428a. Scale bar = 10 μm. 4. Stem, cross ﬁelds with cupressoid type pitting. Specimen UFRJ Pb 428a. Scale bar = 10 μm.

Genus Pseudofrenelopsis Nathorst Synonymes: Pseudofrenelopsis capillata sp. nov. Sucerquia, Bernardes-de-Oliveira et Frenelopsis sp. Kunzmann, Mohr, Bernardes-de-Oliveira and Wilde, Mohr pp. 218, Figs. 3A–C, 4A–E, 5A–G, 2006. P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128 123

Pseudofrenelopsis sp. Bernardes-de-Oliveira, Sucerquia, Mohr, Dino, Stomata at abaxial cuticle are arranged in well-defined longitudinal Antonioli and Garcia, pp. 110, Figs. 5C–E, 2013. rows, separated by 2–3 rows of ordinary epidermal cells. Stomata are adjacent or separated by up to three ordinary epidermal cells (Plate II, Holotype: MB.Pb.2002/1344 (Plate I,1–5) and cuticles extracted from it 3, 5; Plate III, 4). Laterally adjacent stomata may also occur; when they (Plate II,1–5; Plate III). are adjacent, they never share subsidiary cells (Plate II, 6). In general, Repository: The Holotype and its cuticles are housed in the Paleobotani- 7–9 rows of stomata occur per millimeter, with a density of 70 stoma- cal Collection of the Museum für Naturkunde der Humboldt-Universität, ta/mm2. The upper surface of the cuticle shows epidermal cells, each Berlin. bearing one rounded papilla in periclinal walls (Plate II,3–4). Papillae Paratypes: GP/3E 9118, GP/3E 9380 (Departamento de Geologia are 14–18 μmwideand10–13 μm high. Sedimentar, Instituto de Geociências/Universidade de São Paulo), UFRJ The stomata have circular outline and are 66–91 μm in diameter, Pb 428a (Instituto de Geociências, Universidade Federal de Rio de with 5–6 strongly papillate subsidiary cells of trapezoidal to pentagonal Janeiro), SM.B.16447, SM.B.16486 (Senckenberg Forschungsinstitut shape, that are convex in the widest area (Plate III, 1, 4). Subsidiary cells und Naturmuseum, Frankfurt). are 26–34 μm long and 32–53 μm wide. A single level of papillae pro- Type locality: Laminated limestone (Pedra Cariri) quarry between the trude from anticlinal walls of subsidiary cells; they are solid, rounded, Nova Olinda and Santana do Cariri, State of Ceará, Brazil. and often covering completely the stomatal pit (Plate III,2–3). Guard Stratigraphic horizon: Crato Formation cells are elongated, almost rectangular, with 40–53 μm in length, and Age: Late Aptian inner straight ledges of 2 μminthickness(Plate III, 1). Stomatal pits Etymology of the specificepithet:capillata—Latin adjective for organism/ are oriented mostly obliquely, sometimes perpendicularly to the rows bodies covered with hairs. but never parallel (Plate II,5;Plate III, 4). At the leaf apex and base, Diagnosis: Shoots articulated with short and long internodes occurring at the stomata become less frequent and guard cells are preserved closed. the same branch, short internodes in basal position of the branch. One Anticlinal walls of epidermal cells are predominantly 5–10 μmthick.The leaf per node; arrangement of leaves at twigs in a 2/5 spiral phyllotaxy. abaxial cuticle has a thickness ranging between 12–19 μm(Plate III,6). Leaves enclosing the stem, without visible suture and with free Adaxial cuticles have few stomata with closed guard cells (Plate IV, triangularly shaped tip. Apical edges of leaves covered with densely uni- 1), papillae in subsidiary cells were therefore not observed. Epidermal cellular unusually long hairs. Abaxial cuticle with stomata in well-defined cells are tetragonal and bear hairs, one per cell, with up to 180 μmin longitudinal uniseriate rows, adjacent or separated by 1–3 ordinary length (Plate IV,1–2), the hair base extends over the entire area of the epidermal cells. Upper surface of the cuticle composed of papillate periclinal wall. epidermal cells. Stomata circular in outline, 5–6 strongly papillate The stem shows tracheids with uniseriate adjacent areolate pits subsidiary cells of trapezoidal shape. Stomatal pit covered by solid (Plate IV,3).Crossfield pitting is of the cupressoid type with more and rounded papillae. Guard cells elongated with inner straight than 10 pits/per field and 4.5–6 μm in diameter arranged in rows of edges. Stomatal pits oriented mostly obliquely, sometimes perpen- three to five pits (Plate IV,4). dicularly. Stomata at leaf base and apex less frequent that at center. Ordinary epidermal cells elongated between the stomatal rows and 5. Discussion polygonal within them. Abaxial cuticles at internodes remarkably thick. Anticlinal walls of epidermal cells thick. Width of woody axis All specimens from the Crato Formation, described here, are consid- about 1/3 of overall shoot width. Resin ducts generally absent. Tracheids ered to belong to the genus Pseudofrenelopsis.BasedonWatson (1977), with helical thickenings, uniseriate adjacent areolate pits, and cross- this genus has a single leaf per node and the leaves form a single helix field pitting of the cupressoid type. along the branch; Frenelopsis has a whorled arrangement (three leaves Remarks: Pseudofrenelopsis capillata sp. nov, P. papillosa and per whorl) and is rarely distichous. P. parceramosa share (long) hairs on the outer adaxial cuticle. However, Kunzmann et al. (2006) assigned the specimen SM.B.16447 to the in P. capillata and P. parceramosa, the hairs exceed those of P. papillosa genus Frenelopsis based on the number of leaves per node and the clearly in length. The upper margin in leaves of P. capillata develops lon- sutureless leaves which is, however, according to Srinivasan (1995), ger hairs than P. parceramosa. The outer abaxial cuticle in P. parceramosa not a reliable character. is, however, without hair and/or papillae. P. capillata has relatively thick The genus Pseudofrenelopsis currently comprises ten species, cuticles (at the internodes), but P. parceramosa exceeds the cuticle from Berriasian to Albian of the United States, England, Krakow thickness of the new species clearly (see discussion). (Poland), Portugal, Sudan, and China (see Tables 1, 2, 3). Morphological Description: Unbranched and branched shoots (Plate I,1,6,8),preserved characters of leaves and epidermal features of the new material from as compressions with cuticles (MB.Pb.2002/1344 and GP/3E 9118), iron the Crato Formation do not exactly fit those of any of the known oxide casts (GP/3E 9380, UFRJ Pb 428a), and impressions (SM.B.16447). Pseudofrenelopsis species. The main difference is the presence of very Branched shoots comprise up to two orders (Plate I, 1), branches are long hairs at the apical edge of leaves (up to 240 μm), the longest in apparent spiral arrangement. Divergence angles range between 22.5° for the genus. Another unique character is the presence of long and and 53°. The shoots are articulated, internodes range between 3.5– abundant hairs on the adaxial cuticle. Only in P. parceramosa, the pres- 5 mm and 7–9.5 mm in length, and 4–8 mm in width (diameter). Se- ence of very long hairs on the adaxial cuticle was indicated (Watson, quences of short and long internodes are found on the same branch, 1977), but those hairs at the leaf apex are considerably shorter (up to with the short internodes more basal to the branch. There is a single 60 μm). Despite this, a thorough comparison was made with that spe- leaf per node in a 2/5 spiral phyllotaxy (Plate I, 2, 3). Leaves embrace cies because of its substantial character variation and its wide latitudinal the stem completely, without visible suture. Free leaf tips overlap the and longitudinal geographic distribution (Fig. 2, Tables 1, 2, 3). In addi- following ones. These tips are triangular in shape, 1–2 mm high and tion, it is the only taxon formerly recorded at low latitudes, more pre- the apex angle is 70–95° (Plate I, 4, 6). Longitudinal lines converging to- cisely at the Sudan, northern Africa (Watson and Alvin, 1976; Watson, wards the apex on the external leaf surface correspond to stomatal 1983). rows. The stele is about 1/3 of the width of shoot and is three-dimen- When comparing the new species Pseudofrenelopsis capillata with sionally preserved in iron oxide specimens (Plate I, 7). The apical edge P. parceramosa (Watson, 1977), it is obvious that they share several fea- is densely covered with very long hairs, which are unicellular ranging tures. Among them are the distribution of stomata in rows and the no- between 60 and 240 μm in length. Width at the base of individual table thickening of the anticlinal walls in the epidermal cells. Inside hairs is 21–29 μm and gradually tapers towards the tip (Plate I,5; the rows, stomata are partly separated by isodiametric epidermal cells Plate II,1–2). or are adjacent. Papillae are present in anticlinal walls of subsidiary 124 P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128

Table 1 Location, age, and morphology of vegetative remains of various Pseudofrenelopsis species.

Location Age Branching Internode Internode Suture in Maximum References length width leaves length of free tip in leaves

P. varians USA Aptian–Albian Sparse 1.5–17 mm 3–7 mm None 1.5 mm Watson, 1977 P. parceramosa USA, England,Portugal, Berriasian–Aptian Sparse 1–11 mm 2–7.5 mm Suture in some 2mm Reymanówna and Watson, Krakovia, Moravia, Sudan open forms 1976; Watson and Alvin, 1976; Alvin, 1977; Watson, 1977, 1983; Hlustik, 1988; Axsmith, 2006 P. papillosa China Berriasian–Aptian Sparse 5–11 mm 3–7.5 mm None 1.5 mm Zhou, 1995 P. dalatzensis China Aptian–Albian Presumed to 5.5–10 mm 3–6.5 mm None 2 mm Zhou, 1995; Yang et al., be sparse 2009 P. heishanensis China Berriasian–Aptian Presumed 5–6 mm 2.5–4 mm None 2 mm Zhou, 1995 to be sparse P. nathorstiana USA Aptian Not described 1–2.9 mm 1–2mm Yes 1mm Srinivasan, 1995 P. glabra China Albian Not described 6–8 mm 4 mm None 1.5 mm Saiki, 1999 P. gansuensis China Aptian–Albian Not described 7–11 mm 9 mm Not described 1.5 mm Deng et al., 2005 P. guixiensis China Early Cretaceous Not described 5–9mm 4–8 mm Not described 2 mm Sun et al., 2011 P. liupanshanensis China Middle–Late Albian Not described 2–5mm 2–3 mm Not described 1 mm Du et al. 2014 P. capillata Brazil Late Aptian Sparse 3.5–9.5 mm 4–8 mm None 2 mm This work

cells and protrude to the stomatal pit. A dense hair cover is observed at There is a consensus for paleoenvironmental aspects of the free leaf tips and the presence of branches with both long and short Pseudofrenelopsis. In the Lower Cretaceous of Texas, USA, P. varians has internodes. Anatomical features such as areolate uniseriate pits and been generally associated with environments of high salinity and cross fields are very similar to those described for P. parceramosa by evaporation rates, based on the xeromorphic features of their leaves Alvin et al. (1981). Pseudofrenelopsis parceramosa, housed at the (e.g. thick cuticle and sunken stomata), but also on the sedimentological American Museum of Natural History (PAL 192360, PAL 192362, characteristics of the deposits (Daghlian and Person, 1977). This species PAL 192363, PAL 192393), grew – in accordance with the original was reconstructed as a succulent, similar to the extant halophytic angio- species diagnosis – sutureless leaves as seen also in specimens of sperm Salicornia (Watson, 1977, 1988). P. capillata. Branch phyllotaxy, described as alternate and bilateral in The leaf morphology of Pseudofrenelopsis parceramosa from various P. parceramosa, was, howewer, observed to be spiral as in P. capillata. localities is interpreted as a xeromorphic adaptation to arid climates The ratio of the diameter of the main axis and the diameter of side (Watson, 1977, 1988; Alvin, 1982, 1983; Axmith et al., 2004). Moreover, branches of higher order is very remarkable in P. parceramosa,reaching Upchurch and Doyle (1981), based on sedimentological data, fossils, 5:3, while in P. capillata, the main preserved axes and branches are more and palynological diversity of the Potomac Group, indicated a coastal or less of equal thickness. tide influenced environment for P. parceramosa interpreting this taxon Stomata of both species are arranged in uniseriate rows, with usually as a facultative halophyte. The same authors report also Frenelopsis 5–6 subsidiary papillate cells protruding to the stomatal cavity, with cell ramosissima for the Potomac Group, as associated to non-saline environ- walls thinner than those of ordinary epidermal cells. The anticlinal walls ments. Frenelopsids show wide ecological amplitude. Their habitat in- in epidermal cell walls between the rows of stomata are thinner in cludes non-saline environments as recorded in Spain. Xeromorphic Pseudofrenelopsis capillata. Brazilian species lack well-developed and features of Frenelopsis are certainly not always related to a coastal envi- cutinized hypodermal cells observed in P. parceramosa. However, in ronment but to climate-induced water stress (Gomez et al., 2002). specimens of the same species from Arkansas (USA), this feature is Pseudofrenelopsis parceramosa from the Lower Cretaceous of the Isle also absent (Axsmith, 2006). Cuticle thickness in P. capillata is about of Wight (England) occupied the margins of braided rivers (Alvin et al., 16 μm, almost half of the cuticle's thickness (30 μm) of P. parceramosa. 1981). According to the authors, a climate regime with high precipitation prevailed during the formation of those deposits, but the presence 6. Phytogeography, stratigraphic range, and climate of fusinized woods associated to irregular growth rings in stems indicate occasional or periodic dry phases, probably severe enough to allow The occurrence of Pseudofrenelopsis in the Araripe Basin, Brazil, forest fires. Alvin (1983) concludes in a study of material from the constitutes the southernmost record of this genus, extending its latitu- same locality that the morphological features of P. parceramosa are dinal distribution (Fig. 2). The approximate geographic locations of most likely due to xeromorphy, not to halophytism, since there is Pseudofrenelopsis species are plotted on an Aptian paleogeographic no evidence of any marine influence. Contrary to this statement, and paleoclimatic map (Chumakov et al., 1995 in Hay and Floegel, Haworth and McElwain (2008), consider that “xeromorphic” features 2012). When compared to the floristic regions of Vakhrameev (1991), in Pseudofrenelopsis parceramosa may be not related to real xeromorphy most of the records of this genus are located in the Euro-Sinian Region, but constitute adaptations to environmental stress of differing origins as while two belong to the (sub) Equatorial Region, Brazil in South can be volcanism, wind, or predators. America and Sudan in Africa and are located in the evaporitic belt within Low diversity of palynological and floristic assemblages in the Holly theAptianaridzone(Fig. 2). Creek Formation in Arkansas, USA (Axmith et al., 2004), are considered The stratigraphic distribution of Pseudofrenelopsis species ranges to represent a highly stressful environment, but it is not clear whether from the Berriasian to Albian. During the Aptian, the genus seems to ex- this is the result of environmental stress caused by drought, saline influ- perience its greatest diversity, with almost all the species coexisting ence, or a combination of both factors. Sedimentological evidence such during this time interval, including P. capillata (Fig. 3). Stratigraphic as red beds in sequences containing P. parceramosa and evaporites in range of P. capillata couldbeextendedthroughAlbianifPseudofrenelopsis stratigraphically nearby strata may confirm xeric conditions. Marine in- occurrences in the Romualdo Formation are confirmed to belong to the fluence was also proven in associated sediments. Fossils from Arkansas, same species as those of Crato Formation. as well as those from Lower Cretaceous of the Isle of Wight, have Table 2 Comparison of epidermal features of adaxial and abaxial cuticles of several Pseudofrenelopsis species.

Hairs in leaf Outer adaxial Inner adaxial Outer abaxial Inner abaxial cuticle Thickness of abaxial Hypodermal cells References upper margin cuticle cuticle cuticle cuticles in internodes ..Scruae l eiwo aaooayadPlnlg 2 21)116 (2015) 222 Palynology and Palaeobotany of Review / al. et Sucerquia P.A. P. varians Hairs up to 60 μm With hairs up Not described With hairs up Cells mostly equidimensional, 50–110 μm Seen only in open Watson, 1977 to 80 μm to 60 μm thick anticlinal walls leaf-base cushions P. parceramosa Hairs up to 80 μm Without or with Cells with distinct Without hairs Cells equidimensional inside 30 μm Well-developed and Reymanówna and Watson, 1976; very long hairs anticlinal walls or papillae and elongate between stomatal cutinized Watson and Alvin, 1976; Alvin, rows, thick anticlinal walls 1977; Watson, 1977, 1983; Hlustik, 1988; Axsmith, 2006 P. papillosa Hairs up to 80 μm With hairs Cells with ± distinct With papillae Elongate cells between stomatal 5–7.5 μm Absent Zhou, 1995 anticlinal walls rows P. dalatzensis Without hairs Without hairs Cells with distinct With papillae Cells equidimensional inside, 5–25, usually Absent Zhou, 1995; Yang et al., 2009 anticlinal walls and elongate between stomatal 7.5–10 μm rows, thick anticlinal walls P. heishanensis Without hairs Without hairs Anticlinal walls thin Without hairs Cells equidimensional inside, 3–5 μm Absent Zhou, 1995 or papillae and elongate between stomatal rows, thick anticlinal walls P. nathorstiana Hairs up to 145 μm With hairs up Cells tetragonal, With hairs up Cells equidimensional inside, 10 μm Absent Srinivasan, 1995 to 65 μm anticlinal walls thin to 200 μm and elongate between stomatal rows, thin anticlinal walls P. glabra Hairs up to 40 μm Without hairs Not described Without hairs Cells equidimensional inside, 3 μm Well cutinized Saiki, 1999 or papillae and elongate between stomatal rows, thick anticlinal walls P. gansuensis Not described Without hairs Not described Without hairs Unknown Not described Not described Deng et al., 2005 or papillae P. guixiensis Not described With hairs up Cells tetragonal, With hairs up Cells equidimensional inside, 6–9 μm Absent Sun et al., 2011 to 30 μm anticlinal walls thin to 30 μm and elongate between stomatal –

rows, thick anticlinal walls 128 P. liupanshanensis Not described Without hairs, but Not described With papillae Cells polygonal inside, and 10–13 μm Not described Du et al. 2014 protuberances rectangular between stomatal rows, thick anticlinal walls P. capillata Hairs with 60–240 μm With hairs up Cells elongated with With papillae Cells equidimensional inside, 16 μm Absent This work to 180 μm thick anticlinal walls and elongate between stomatal rows, thick anticlinal walls 125 126 P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128

Table 3 Comparison of stomatal characteristics of different Pseudofrenelopsis species.

Stomatal Stomatal Stomata size Number of Subsidiary cells Top view of References arrangement in rows subsidiary stomatal pit internodes per mm cells

P. varians Scattered in closed 8–10 70–100 μm4–9, usually With papillae overhanging Rounded with papillae Watson, 1977 form, rows in open 5–8 stomatal pit form P. parceramosa Well-defined rows 6–10 50–80 μm4–7, usually With or without papillae Rounded with papillae Reymanówna and Watson, 5–6 protruded to stomatal pit 1976; Watson and Alvin, 1976; Alvin, 1977; Watson, 1977, 1983; Hlustik, 1988; Axsmith, 2006 P. papillosa Longitudinal rows 4–940–92.5 μm4–8, usually With papillae overhanging Rounded with papillae Zhou, 1995 with scattered 5–7 stomatal pit stomata P. dalatzensis Well-defined rows 6–10 55–95 μm5–6 With papillae overhanging Stellate Zhou, 1995; Yang et al., stomatal pit 2009 P. heishanensis Well-defined rows 8–10 62.5–100 μm5–7, usually With papillae overhanging Stellate Zhou, 1995 5–6 stomatal pit P. nathorstiana Mostly ill-defined 11–12 50–73 or 4–7, usually With papillae Elliptical to rounded, Srinivasan, 1995 rows 54–62 μm 5–6 with papillae rarely 103 μm P. glabra Well-defined rows 7–980–120 μm6–8 With papillae overhanging Rounded with papillae Saiki, 1999 stomatal pit P. gansuensis Well-defined rows 7–890–100 μm6–9, usually Without papillae Unknown Deng et al., 2005 6–7 P. guixiensis Well-defined rows 8–10 50–80 μm 4-6 With papillae Rounded with papillae Sun et al., 2011 P. liupanshanensis Well-defined rows 8–10 55–80 μm5–6 With single papillae Rounded with papillae Du et al. 2014 P. capillata Well-defined rows 7–966–91 μm usually 5, With papillae protruded Elliptical to rounded This work ocasionally 6 to stomatal pit with papillae xeromorphic features, and moreover, fusinized wood particles and the only one attached to Pseudofrenelopsis parceramosa shoots, while stems with irregular growth rings, suggest wildfires and occasional Classostrobus comptonensis (Alvin et al., 1978) is closely associated and water stress. shares similarities in cuticular characteristics. Apparently, the broad ecological tolerance of Pseudofrenelopsis The sedimentological characteristics of the Crato Formation fit the parceramosa, which led to divergent paleoecological interpretations, interpretation of the ecologic niche in which Pseudofrenelopsis grew. may be the consequence of a low taxonomic resolution. The presence The environmental interpretations for this lithological unit suggests a of at least two types of male cones considered to belong to the same lake with hypersaline conditions at the bottom (Neumann et al., plant that produces branches of P. parceramosa strengthens this as- 2003), and proximity to evaporitic deposits. Also other species of sumption. However, Classostrobus arkansensis (Axmith et al., 2004)is Pseudofrenelopsis, such as P. guixiensis from China, grew most likely in

Fig. 2. Pseudofrenelopsis species plotted on an Aptian paleogeographic and paleoclimatic map (Chumakov et al., 1995 in Hay and Floegel, 2012). Floristic regions deﬁned after Vakhrameev (1991). P. capillata sp. nov. appears as the southernmost occurrence in the Equatorial Region and in the evaporitic belt within the arid zone (Chumakov et al., 1995). Other occurrences of the genus in South America are in Villeta and Paja Formations in Colombia, and Romualdo Formation in Brazil. P.A. Sucerquia et al. / Review of Palaeobotany and Palynology 222 (2015) 116–128 127

Fig. 3. Stratigraphic range of Pseudofrenelopsis species during the Early Cretaceous (based on Cohen et al., 2013). The Aptian interval is characterized by the highest species diversity of the genus.

hyperhaline soils based on the association with gypsum of beds contain- Dr. Isaac Jamil Sayeg for support in the SEM examination at the Instituto ing P. guixiensis and the lack of evidence of long-distance transport for de Geociências (Universidade de São Paulo) and also to Dr. Ismar de those plant remains. Souza Carvalho (Instituto de Geociências, Universidade Federal de Rio Pseudofrenelopsis capillata may have been the only species growing de Janeiro) for the loan of the specimen UFRJ Pb 428a. John Wingerath most likely not directly at a coastal line, but at the shores of a large (Paleobotany Collections of the American Museum of Natural History, lake, with relatively little precipitation coming from the ocean, a phe- Washington) was so kind to provide access to North American and nomenon known as the Super Continent Effect (Hay and Floegel, English specimens and mounted cuticles. We also would like to thank 2012) and therefore arid conditions may have prevailed during much to Dr. Brian Axsmith (University of South Alabama, Mobile) for the pos- of the year. In any case, the climate regime was, based on various prox- sibility to study North American vegetative and reproductive specimens ies, certainly at least seasonally dry with episodes of high precipitation and for the supply of cuticular material for detailed comparisons. The and restricted (brackish) bottom water conditions (Martill et al., 2007; first author would like to acknowledge the financial support for a schol- Heimhofer et al., 2009). arship and research funds provided by the Fundação de Amparo a Therefore it is not clear if the xeromorphic morphology and anatomy Pesquisa do Estado de São Paulo (FAPESP 2008/02884-5). The second of Pseudofrenelopsis capillata is conditioned by aridity or salinity, or both. author also want to acknowledge financial support of CNPq scholarship (304978/2013-2) and FAPESP reasearch funds (2003/09407-4). 7. Conclusions

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