Towards a whole plant reconstruction for Austrohamia (Cupressaceae): New fossil wood from the Lower Jurassic of Argentina

Review of Palaeobotany and Palynology 234 (2016) 186–197

Contents lists available at ScienceDirect

Review of Palaeobotany and Palynology journal homepage: www.elsevier.com/locate/revpalbo

Towards a whole plant reconstruction for Austrohamia (Cupressaceae): New fossil wood from the Lower Jurassic of Argentina Josefina Bodnar a,b,⁎, Ignacio Hernán Escapa b,c a b c

División de Paleobotánica, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina Museo Paleontológico Egidio Feruglio. Av. Fontana 140, U9100GYO Trelew, Chubut, Argentina

a r t i c l e

i n f o

Article history: Received 14 April 2016 Received in revised form 15 September 2016 Accepted 19 September 2016 Available online 21 September 2016 Keywords: Fossil wood Mesozoic Conifers Whole-plant reconstruction

a b s t r a c t Early diversification of modern conifer lineages occurred during the Late Triassic and Early Jurassic, and worldwide ecosystems were dominated by conifers throughout the Jurassic. The knowledge about the palaeobiology and palaeoecology of basal representatives of those clades, however, has only recently begun to be developed due to the relative scarcity of complete plant reconstructions for many of these conifer families. In regards to the Cupressaceae sensu lato, some reconstructions have been proposed, although none has linked all plant organs. One of the oldest records of this family is the genus Austrohamia, described from the Lower Jurassic of Argentina and China. The original material consists of impressions of leafy branches, organically attached to ovulate and pollen cones. This conifer has a combination of characters that support its assignation to the Cunninghamioideae subfamily, the most basal member of the Cupressaceae stem group. In this paper, we describe permineralized woods from the same strata where Austrohamia minuta was found in the Cañadón Asfalto Basin, Chubut Province, Argentina. The fossil woods were assigned to the genus Protaxodioxylon, due to homoxylic pycnoxylic secondary xylem, with distinct growth rings, radial tracheid pitting of mixed type, abundant axial parenchyma, taxodioid cross-fields and uniseriate homocellular rays. Consistent with the differences in other Protaxodioxylon species, we propose a new specific taxon for the Patagonian specimens. This genus has often been related to the taxodiaceous Cupressaceae. This linkage, together with the fact that all the conifer impressions from these strata correspond to Austrohamia, reinforces the idea that the wood belongs to the same biological entity as A. minuta. From this interpretation, Austrohamia represents the most complete Mesozoic Cupressaceae to date. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Conifers were the dominant forest trees across the ancient world during the Jurassic period, during which most modern conifer families originated and diversified (Stewart and Rothwell, 1993; Miller, 1977, 1982; Leslie et al., 2012). Most terrestrial Jurassic ecosystems in the Southern Hemisphere were dominated by representatives of the conifer families Araucariaceae (e.g., Stockey, 1978; Rees and Cleal, 2004; Pole, 2008; Falaschi et al., 2011; Panti et al., 2012), Cheirolepidiaceae (e.g., Escapa et al., 2012, 2013; Bodnar et al., 2013), Podocarpaceae (e.g., Townrow, 1967a, 1967b) and basal representatives of Cupressaceae (e.g, Escapa et al., 2008).

⁎ Corresponding author at: División de Paleobotánica, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, Paseo del Bosque s/n, B1900FWA La Plata, Buenos Aires, Argentina. E-mail address: [email protected] (J. Bodnar).

http://dx.doi.org/10.1016/j.revpalbo.2016.09.005 0034-6667/© 2016 Elsevier B.V. All rights reserved.

Despite their crucial role in Jurassic environments, the current understanding of the palaeobiology and palaeoecology in conifer species is limited, due to the scarcity and incompleteness of the Jurassic record. The fossil remains of conifers in the Lower Jurassic of South America is abundant but consists mainly of woods (e.g., Torres and Philippe, 2002; Gnaedinger and Herbst., 2009; Gnaedinger et al., 2015; Bodnar et al., 2013), and isolated pollen and leafy twigs (e.g., Quattrocchio et al., 1996; Zavattieri et al., 2006; Channing et al., 2007; Olivera et al., 2015), with pollen and ovulate cones being very rare (e.g., Escapa et al., 2008). One of the primary goals of palaeobotany, especially in those areas in which the focus of the research is directed at understanding the palaeobiology, palaeoecology and evolution of the organism, is the progressive reconstruction of increasingly complete plant concepts. This is typically accomplished by demonstrating organic connections among different plant parts and different stages of preservation, by repeated and unique co-occurrences and by morphological and anatomical similarities (Bateman and Hilton, 2009). In the case of Cupressaceae sensu

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

lato, reconstructions including a variable degree of interrelated organs (e.g., leaves, pollen cones, seed cones, seeds, pollen, wood) have been proposed (e.g., Yao et al., 1998; Escapa et al., 2008; Shi et al., 2014; Bodnar et al., 2015), but none have yet related all the organs of the plant. It is widely accepted that the earliest unambiguous representative of the Cupressaceae is Austrohamia, known from the Lower Jurassic of Patagonia (Escapa et al., 2008) and Upper Jurassic in China (Zhang et al., 2012). The Patagonian species, Austrohamia minuta Escapa, Cúneo et Axsmith, was originally described based on impressions represented by well-preserved leafy twigs and branches, and attached ovulate and pollen cones. When phylogenetically analyzed, Austrohamia minuta has been consistently found to be part of the basal lineages in the Cupresssaceae, either as sister to a clade including modern Cunninghamia and additional fossil genera (Escapa et al., 2008; Mao et al., 2012), or to Taiwania (Shi et al., 2014). More recently, several in situ and transported permineralized wood remains have been found in the same Early Jurassic strata as those of the original impressions of Autrohamia minuta (see Cúneo et al., 2013; Figari et al., 2015) and are anatomically described in the present paper. Different sources of evidence, such as anatomical characters and close occurrence, suggest that the wood herein described was part of Austrohamia minuta plant, which would represent not just the older reliable basal representative of the Cupressaceae, but also one of the most complete fossil species in the lineage.

2. Materials and methods A total of 12 hand wood specimens were collected at the “Cerro Bayo” area (Chubut province, Argentina) (Fig. 1, A). Plant horizons at this locality have been referred to unnamed siliciclastic and volcaniclastic deposits of fluvial origin, which are succeeded by agglomerates and lavas of the Lonco Trapial Formation, and lacustrine deposits of the Cañadón Asfalto Formation (Fig. 1, B). This lithostratigraphic unit is most likely equivalent to the top of Las Leoneras Formation, since it is transitional with the Lonco Trapial Formation (see Cúneo et al., 2013; Figari et al., in press). The plantbearing sediments have been considered to be Early Jurassic in age based on similarities from nearby palaeofloristic occurrences (Escapa et al., 2008; Escapa and Cúneo, 2012). More recently, radiometric dating from ash beds included in the overlying Cañadón Asfalto Formation have yielded U-Pb zircon mean ages of 176.15 ± 0.1 and 177.4 Ma (Cúneo et al., 2013), which definitely confirms an Early Jurassic age (most likely Pliensbachian) for the plant assemblages. Specimens described here were collected at three nearby sites (GPS coordinates are available from the authors upon request). Two of these localities, informally referred as GT03 and GT14, are placed at the same stratigraphic level, on both sides of a small creek. The third locality is stratigraphically higher and it is here referred to as “Middle Level” (Fig. 1, A). All the specimens have been sectioned and identified as the same taxa, probably indicating a low diversity in the communities of the tree strata (see Section 4.3). They occur in fine-grained, silicified sediments (Plate II, 1) as part of a taphocoenosis dominated by horsetails, ferns, seed ferns and conifers. Horsetails are represented by an extraordinarily preserved Equisetum species, including vegetative and reproductive remains (Elgorriaga et al., 2015). Ferns include the osmundaceous Todites cacereii and Osmundopsis rafaelii (Escapa and Cúneo, 2012), a fertile marattiaceous species (Escapa et al., 2014) along with dipteridaceous species of the genera Clathropteris and Goeppertella (Escapa, 2009). The conifers are represented by the cupressaceous Austrohamia minuta (Escapa et al., 2008) (Plate II, 2–3). Unidentified seed ferns complete the floristic spectrum (Escapa, 2009).

187

Stems were preserved by siliceous cellular permineralization. Specimens were sectioned following standard procedures (see Stockey, 1977). Hillquist's (A/B) thin section epoxy (Ward's Natural Science Establishment, Rochester, NY) was used for mounting specimens on 2 × 3 in. glass slides. Thin sections were cut and ground to approximately 40 μm thickness, on a Hillquist thin-section machine. They were then polished by hand on a glass plate using 600 grit carborundum. Cover slips were affixed with Eukitt (O. Kindler GmbH and Co., Freiburg, Germany). The classic transverse, radial and tangential thin sections were obtained from polished surfaces at the thin section Laboratory of the Museo Paleontológico Egidio Feruglio, Argentina (hereafter MPEF-Pb). A Leica DM2500 microscope and a Nikon Eclipse E400 Epifluorescence Microscope were used. The sections were observed with transmitted light and epifluorescence. Photographs were made with a Canon digital camera and Leica DC 150 system, in the case of Leica microscope, and with Nikon digital camera under tungsten light, in the case of Nikon microscope. Wood fragments were also observed under SEM JEOL JSMT-100 (secondary electron imaging – SEI - signal, at 15 kV) and JEOL JSM6360 LV (back-scattered electrons – BSE - signal, at 4 kV), with gold/palladium coat, at the microscopy service of the Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata. Descriptions were made following standardized terminology of Boureau (1956), Fahn (1990), IAWA Committee (Richter et al., 2004), Philippe and Bamford (2008), and Greguss' wood anatomy atlas (1955). The dimensions of anatomical elements were obtained with 30 measurements in each case. In the description, first the minimum value is mentioned, and second, the maximum value. The average value is cited, between round brackets. Taxonomic determination follows the key proposed by Philippe and Bamford (2008) for mesozoic homoxylic woods. 3. Systematic palaeontology 3.1. Family Cupressaceae Genus Protaxodioxylon Bamford et Philippe 2001. Type species. Protaxodioxylon romanensis (Philippe) Bamford et Philippe 2001; basionym Prototaxodioxylon romanensis, Philippe, Palaeontographica, Abt. B, 236: 73, tables 10 et 11, textfig. 6, 1995. Vide quoque Philippe, Lethaia, 27: 70, Fig. 3, 1994. 3.2. Protaxodioxylon patagonicum Bodnar et Escapa sp nov. Plates II, 1–6; III, 1–10; IV, 1–4; V, 1–3; VI, 1–5. Diagnosis. Pycnoxylic homoxylic secondary wood with distinct growth rings of variable width (20–120 cells), poorly defined, with abrupt transition from early to latewood. Latewood 1–5 cells wide. Tracheid pitting in radial walls of mixed type, predominantly uniseriate, with a separated, contiguous or compressed arrangement. Pits rounded with a circular pore. Septate tracheids present. Axial parenchyma abundant, with resinous contents. Cross-fields of taxoidioid type, with 1–3 oculipores with the aperture wider than one margin. Rays homocellular, uniseriate, 1–22 cells high. Age. Early Jurassic (Cúneo et al., 2013). Type locality. Cerro Bayo, Chubut province, Argentina. Derivatio nominis. The specific name is referred to the geographic region from where the specimens were collected. Holotype. MPEF-Pb 8380, Fossil Collection of the Museo Paleontológico Egidio Feruglio (Trelew, Chubut). Paratypes. MPEF-Pb 8381, 8382. Additional material. MPEF-Pb 8371, 8372, 8373, 8374, 8375, 8376, 8377, 8378, 8379. Description. The studied axes are ca. 30 cm in diameter (Plate I, 1), and exhibit only secondary xylem preserved. Primary vascular

188

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

tissues, secondary phloem and cortex are not preserved in any sample. Secondary xylem shows poorly defined growth rings, with an abrupt reduction of the radial diameter of tracheids towards the ring's outer margin (Plate II, 1–2). Growth ring thickness varies from 20 to 120 cells. Latewood is 1–5 cells thick (Plate II, 1–2). Secondary xylem tracheids are quadrangular to hexagonal in transverse section (Plate II, 1–2; Plate IV, 1). The radial diameter of earlywood tracheids is 22.68–(30.32)–36.34 μm and the tangential diameter is 18.7–(27)–33.57 μm. The thickness of the double wall between two earlywood tracheids is 5.4–(7.3)–10.2 μm in radial section and 5.2–(6.4)–8.1 μm in tangential section. The radial diameter of latewood tracheids is 8.1–(11.3)–15 μm and the tangential diameter of tracheids is 13.7–(20.2)–35 μm. The thickness

of the double wall between two latewood tracheids is 6.4–(7.3)– 10 μm in radial section and 7.03–(8.4)–9.6 μm in tangential section. The mean number of tracheids that separate the rays is five, with a range of 3–9 rows of tracheids. Tracheids show mainly uniseriate (88%), less often biseriate (12%), bordered pits on radial walls (Plate III, 1, 3–6; Plate IV, 3–4). Pits are rounded, with circular apertures (Plate III, 3; Plate VI, 1) and, for the most part (68%), with a spaced or contiguous arrangement (Plate III, 3–4; Plate IV, 3–4, Plate VI, 1), in smaller proportion (32%) with a compressed organization (Plate III, 5–6). When biseriate, they are opposite to sub-opposite (Plate III, 5–6; Plate IV, 3–4). This pattern belongs to mixed or transitional type of radial pitting sensu Philippe and Bamford (2008).

Fig. 1. Location (A) and geology (B) of the Protaxodioxylon patagonicum sp. nov. fossiliferous sites (stars): a, GT03, b = Middle Level, c = GT14. (Modified from Cúneo et al., 2013).

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

189

Plate I. 1. Field photograph of a permineralized stump of Protaxodioxylon patagonicum sp. nov.; 2. Leafy twig of Austohamia minuta found in the same rocks than the previous stump; 3. General aspect of Austrohamia minuta, showing the leafy twigs with terminal clusters of pollen cones (arrows) and megasporangiate cones.

Tracheid wall pits are 12.5–(12.9)–18.75 μm high and 15– (15.4)– 20 μm wide, with pit apertures of 3.2–(4.5)–6 μm in diameter. Tangential tracheid wall pitting is absent. Cross-fields have 1 to 4 bordered pits with oval outline, 5.3 × 8.8–(8.4 × 11.4)–11.2 × 12.5 μm in diameter, placed in vertical or horizontal rows (Plate III, 7–10). Individual pits are of taxodioid type or cupressoid type sensu IAWA Committee (Richter et al., 2004). Pit aperture is horizontal or oblique, and is wider than one margin. Pit arrangement is of taxodioid type crossfield sensu IAWA Committee (Richter et al., 2004) (Plate III, 7–10; Plate VI, 2–3). Secondary xylem rays are homocellular, uniseriate, occasionally partially biseriate, and medium-high with rectilinear trajectory (Plate II, 5–6; Plate IV, 2; Plate VI, 4–5), are 29.5–(129.3)–503.5 μm and 1–(mode 2; mean 6)–26 cells high. They are composed of rectangular parenchyma cells with slightly thickened and smooth walls (Plate III, 2, 9). These cells are 14.5–(23.63)–33.9 μm high, 7.9–(16.9)–26.91 μm wide, and 56.5–(94.39)–129.7 μm long. Axial parenchyma is abundant, diffuse and tangentially zonate (Plate II, 3–4). It is composed of vertically elongate cells 90.5–(255.68)– 455.7 μm in height and 16.2–(26.2)–33.7 μm diameter with resin contents, and slightly thickened and smooth transverse end walls (Plate II, 5–6; Plate III, 2; Plate IV, 2; Plate V, 1–3; Plate VI, 5). Septate axial tracheids are present (Plate II, 6; Plate V, 1). Ray tracheids are absent. 3.3. Generic assignment and specific comparisons According to Philippe and Bamford (2008) homoxylous fossil woods with mixed type of radial tracheid pitting and pits in earlywood cross-fields of the taxodioid type (i.e., with a tangent aperture) wider than one margin, usually nearly horizontal, are assigned to Protaxodioxylon Bamford et Philippe. The diagnosis of this genus comprises tracheidoxyls with radial tracheid pitting of the mixed type and taxodioid cross-fields, which are defined as having 1–5 oculipores in one or more horizontal rows, the diameter of aperture being greater than the width of the border (see Philippe, 1995), and the axis of this aperture being horizontal or slightly oblique (Bamford and Philippe, 2001). Fossil woods with mixed radial pitting and taxodioid cross-fields, were originally named Prototaxodioxylon by Vogellehner (1968). As noted by Nadjafi (1982), who reexamined the original slides, there was an inconsistency between the original diagnosis and the holotype - Prototaxodioxylon chouberti (Attims) Vogellehner - which has cupressoid instead of taxodioid cross-field pits. Following this interpretation, Prototaxodioxylon is then a taxonomical synonym of

either Protocupressinoxylon Eckhold or Brachyoxylon Hollick et Jeffrey (since the first is a junior synonym of the second, see Phillippe and Bamford, 2008). Nadjafi (1982) used the name Metataxodioxylon, for a wood species with taxodioid cross-fields, which however are accompanied by araucarian radial tracheid pitting. In order to fix this taxonomic issue, Bamford and Philippe (2001) proposed the name Protaxodioxylon for wood species with mixed radial pitting and cross-fields of the taxodioid type. To our knowledge this genus comprises four species: Protaxodioxylon romanensis (Philippe) Bamford et Philippe, known from the Lower Jurassic of Doubs and Bas-Rhin, France (Bamford and Philippe, 2001), Protaxodioxylon turolense Vozenin-Serra in Vozenin-Serra et al. from the Lower Cretaceous of the Iberian Range, Spain (Vozenin-Serra et al., 2011); Protaxodioxylon mongolense Ding et al. from the Upper Jurassic to Lower Cretaceous of Southeast Mongolia (Ding et al., 2011) and Protaxodioxylon jianchangense Tian N. et Wang Y.D. recently described for the Middle-Upper Jurassic of Liaoning, China (Tian et al., 2015). Later on, a few more wood specimens were attributed to the genus Protaxodioxylon (see Philippe et al., 2006, 2010 and citations therein), however the anatomy of these woods should be further analyzed in order to define new taxa at the specific level. The new species described here can be distinguished from previously defined Protaxodioxylon taxa, mainly due to the lower percentage of compressed tracheid pitting, the presence of septate tracheids, and the abundance of axial parenchyma in the Patagonian species. Furthermore, P. patagonicum differs from P. romanensis due to the fact that the latter species shows false growth rings, tracheid pitting of a more variable morphology, occasional Sanio bars, and cross-fields with exclusively taxodioid pits. Protaxodioxylon turolense lacks growth rings, has higher wood rays (ranging 7–42 cell high, with a mode of 12–22) which are more frequently biseriate (even triseriate), and shows crassulae and Sanio bars in the tracheid radial walls, in comparison with P. patagonicum. Protaxodioxylon patagonicum, is clearly distinguished from P. mongolense since the latter species has spiral thickenings on the radial walls of the tracheids, mainly alternate radial tracheid pitting, higher wood rays (ranging 1–57 cell high, with a mode of 8–26) which are most commonly partially bi- and triseriate (Ding et al., 2011). Finally, the new species is different from P. jianchangense, because of the presence of spiral thickenings on the radial walls of the tracheids, tangential tracheid pitting and a lower number of pits in the cross-field (rarely more than one) than P. jianchangense (Tian et al., 2015). Following these differences, we proposed a new specific taxon for the Patagonian specimens.

190

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

Plate II. 1–6, Protaxodioxylon patagonicum sp. nov. View under optical microscope (cross and tangential sections); 1, MPEF-Pb 8375, cross section of the growth ring boundary; 2, MPEF-Pb 8380, detail of the latewood band; 3, MPEF-Pb 8374, cross section, showing the diffuse arrangement of axial parenchyma; 4, MPEF-Pb 8374, cross section, showing the tangentially zonate axial parenchyma; 5, MPEF-Pb 8380, tangential section with uniseriate rays and axial parenchyma (arrow); 6, MPEF-Pb 8373, tangential section showing the septate tracheids (ST) and axial parenchyma (AP). Scale bar: 1 = 270 μm; 2 = 100 μm; 3 = 240 μm; 4, 6 = 200 μm, 5 = 220 μm.

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

191

Plate III. 1–10, Protaxodioxylon patagonicum sp. nov. View under optical microscope (radial section). 1, MPEF-Pb 8380, general view of radial section showing the pattern of radial tracheid pitting; 2, MPEF-Pb 8380, general view of radial section showing a row of axial parenchyma cells with resin contents (arrow). 3, MPEF-Pb 8380, spaced to contiguous uniseriate radial tracheid pits; 4, MPEF-Pb 8374, spaced uniseriate radial tracheid pits; 5, 6, MPEF-Pb 8380, compressed to contiguous biseriate radial tracheid pitting, with opposite to subopposite pattern; 7, 8, MPEF-Pb 8380, taxodioid cross-fields with cupressoid individual pits; 9, 10, MPEF-Pb 8380, taxodioid cross-fields with taxodioid individual pits. Scale bar: 1 = 200 μm; 2 = 100 μm; 3, 5, 6, 8 = 50 μm; 4 = 70 μm, 7, 9, 10 = 60 μm.

4. Discussion 4.1. Character discussion Two relevant traits in the wood of Protaxodioxylon patagonicum sp. nov. are represented by the abundance of axial parenchyma and the presence of septate tracheids, a combination that has been rarely reported for conifers. Both axial parenchyma cells and septate

tracheids are derived from fusiform cambial initials (Carlquist, 1988; Evert, 2006; Beck, 2010). Axial parenchyma consists of axially elongate cells or (more commonly) strands of cells, alive at maturity (Carlquist, 1988; Evert, 2006). Each cell in a strand of axial parenchyma is surrounded by a lignified secondary wall, usually thinner than imperforate tracheary element walls (Carlquist, 2001; Evert, 2006). In transverse section, cells of axial parenchyma often look like an axial tracheid, but can be differentiated when they contain

192

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

Plate IV. 1–4, Protaxodioxylon patagonicum sp. nov. MPEF-Pb 8380. View under a fluorescence microscope; 1, general view of secondary xylem cross section; 2, tangential section showing the uniseriate rays and the axial parenchyma with resin contents (arrow); 3, 4, radial tracheid pitting. Scale bar: 1, 2 = 200 μm; 3, 4 = 50 μm.

dark-colored organic substances in the lumen of the cell. In the radial or tangential section they appear as long strands of cells generally containing dark-colored substances (Rowell, 2012). However, its presence must always be confirmed from longitudinal sections by looking for the characteristic transverse end walls, which can be either smooth, irregularly thickened, or beaded/nodular (Richter et al., 2004). The exact function of axial parenchyma is not entirely understood, but its main role is very likely as a secondary conductive system, and

certainly is involved in the transport of chemical signals and other constituents (Hacke, 2015). It may also contribute to the reversal of embolisms, heartwood formation and both induced and constitutive defenses (Tyree et al., 1999; Améglio et al., 2001; Salleo et al., 2004). The presence of axial parenchyma is variable depending of the taxonomic group (Greguss, 1955; Jane, 1956; Carlquist, 1975), however, it usually represents a small proportion of the xylem (Esau, 1977). Presence of axial parenchyma is a frequent feature of Cephalotaxaceae,

Plate V. 1–3, Protaxodioxylon patagonicum sp. nov. MPEF-Pb 8380. Detail of axial parenchyma cells and septate tracheids under optical microscope, in tangential section. 1, one septa in a tracheid (S) and resin contents of an axial parenchyma cells (R); 2, terminal double wall of axial parenchyma cells; 3, detail of resin contents of the axial parenchyma (R), and a septate tracheid (S). Scale bar: 1, 2, 3 = 20 μm.

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

193

Plate VI. 1–5, Protaxodioxylon patagonicum sp. nov. MPEF-Pb 8380. View under scanning Electron Microscope; 1, uniseriate spaced to contiguous radial tracheid pitting; 2, 3, detail of crossfields (20° tilt); 4, uniseriate rays in tangential section; 5, uniseriate ray and axial parenchyma (arrow). Scale bar: 1 = 40 μm; 2, 3 = 30 μm, 4 = 100 μm, 5 = 50 μm.

Cupressaceae s.l. and most Podocarpaceae. However, it seems to be completely absent in Araucariaceae, Phyllocladaceae, Sciadopityaceae, and Taxaceae. In Pinaceae, fusiform, parenchyma cells with axial disposition are restricted to those associated with resin ducts (Richter et al., 2004), and therefore are not strictly comparable with axial parenchyma in other conifer families. The arrangement of the axial parenchyma is also informative (Greguss, 1955; García Esteban et al., 2002; Richter et al., 2004). For instance, in both Podocarpaceae and Cupressaceae, axial parenchyma is occasionally present as single strands in the transition zone between early and latewood. In particular, Protaxodioxylon patagonicum sp. nov. has axial parenchyma with a diffuse to tangentially zonate arrangement, which is a frequent

arrangement in extant representatives of Cupressaceae s.l. (see Farjon, 2001; Richter et al., 2004). Axial parenchyma is abundant in the new species, and has conspicuous dark contents, which seem to be ergastic substances in amorphous form, probably resins (see Section 3). Transverse end walls of axial parenchyma cells are smooth, and slightly thickened. A second feature of interest shown by Protaxodioxylon patagonicum is represented by the septate tracheids, which are rarely mentioned in moderns conifers (e.g., Thomson, 1913; Jeffrey, 1925), but are frequently cited for fossil conifer woods (e.g., Medlyn and Tidwell, 1975; Medlyn and Tidwell, 1975; Alvin et al., 1981; Torres and Biró-Bagóczky, 1986; Tidwell and Thayn, 1986; Cevallos Ferriz, 1992; Bamford and Corbett, 1994; Youssef, 2002; Philippe and Bamford, 2008; Crisafulli and Herbst,

194

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

2011). This fact can be explained by the difficulty of distinguishing the septate tracheids from other cell types, in some fossil samples. Another issue explaining the scarce citation of septate tracheids in living conifers is that research into modern wood anatomy has given greater importance to this type of character in angiosperms, and thus there is much more literature on their hardwood counterparts (see below). Septate tracheids and septate fibers (which are homologous to septate tracheids in angiosperms) are those that have one or more transverse dividing walls inside the cells (Beck, 2010). They usually retain their protoplasts in the mature active wood, where they are concerned with the storage of reserve substances (Frison, 1948; Fahn and Leshem, 1963). Thus these cells are similar to axial parenchyma in both structure and function. The retention of protoplasts by tracheids and fibers has been considered as a derived feature compared to normal tracheids, and therefore may be used as a systematically valuable character (sensu Bailey, 1953; see also Bailey and Srivastava, 1962). In cases in which septate tracheids and fibers are present, axial parenchyma is either scarce or absent (Money et al., 1950). In Gnetum (Gnetales) septate tracheids have, like axial parenchyma cells, thinner walls than non-septate tracheids (Carlquist, 2012). As a result of a study of living and extinct gymnosperms, Jeffrey (1925) concluded that the axial parenchyma evolved from axial tracheids, and the first stage of this evolution is the formation of septa in the tracheids. Despite their close similarities, septate tracheids can be differentiated from axial parenchyma by possessing thinner and simpler septa, than those found in the end walls of individual cells in an axial parenchyma strands, since the former do not include a middle lamella, while the latter are comprised of a middle lamella and a double wall, derived from the adjacent cells (see Plate V). Occasionally, both kinds of cells have been reported in the same species (e.g., roots of Gnetum cuspidatum; Carlquist, 2012), which also seems to be the case for Protaxodioxylon patagonicum sp. nov. The abundant axial parenchyma and/or septate tracheids can be indicative of a response of the plant of some kind of stress and/or particular environmental conditions. Collectively, these types of cells and resins may deter beetle invasion, impede fungal growth, and flush and seal entrance wounds (Klepzig et al., 1995; Trapp and Croteau, 2001). The axial parenchyma has been related to both xeromorphic and hydromorphic adaptations: it has been proposed to be related to oxygenation problems of plants with submerged roots and trunk bases (Carlquist, 1975) and as an important temporary reservoir of water in many desertadapted trees (Mauseth, 2012). The environment where Protaxodioxylon patagonicum sp. nov. lived was interpreted as a zone of fluvial deposits with important ash fall influence. The presence of horsetails and abundant ferns indicates humid, warm-temperate to subtropical climatic conditions; in particular, the occurrence of Dipteridaceae have been used to infer conditions of high storminess and large seasonal rainfall (monsoonal climates) Cantrill (1995). In this manner, the abundant axial parenchyma with resin contents in P. patagonicum could have helped both to heal injuries produced by volcanic ash fall (e.g. breakage of large branches by accumulated weight of ash fall, defoliation, scorching of the bark) and to store water in the dry season of the monsoonal climate. 4.2. Systematic affiliation The general aspect of the tracheids and rays, the presence of taxodioid cross-field pits and the presence of abundant axial parenchyma, indicate that the structure can be related to the taxodiaceous Cupressaceae. Recent phylogenetic analyses based on molecular and morphological data propose the consideration of Cupressaceae and Taxodiaceae as a single family (Cupressaceae s.l.), excluding Sciadopitys Siebold et Zuccarini, the latter being transferred to a monotypic family Sciadopityaceae Luerss. (Gadek et al., 2000; Farjon, 2005). Although convergent characters are frequent in conifer woods, the combination of some traits can help to approximate a taxonomic

affinity. The woods of the Cupressaceae s.l. have numerous features in common with Protaxodioxylon patagonicum: growth rings present, resin channels absent, frequent axial parenchyma occasionally with nodular walls, abietinean tracheid pitting, cross-fields with 1–6 oculipores, uniseriate rays, and parenchyma ray cells sometimes with indentures and/or with nodular walls (Peirce, 1937; Kräusel, 1949; Boutelje, 1955; Greguss, 1955; Boureau, 1956; Bonetti, 1966; Patel, 1968; Vaudois and Privé, 1971; Roig, 1992; De Magistris, 1997; Gadek et al., 2000). Within the family Cupressaceae s.l. the greatest affinities are found within extant genera that have smooth terminal walls of the ray and axial parenchyma cells and taxodioid crossfields, namely Athrotaxis, Cunninghamia, Cryptomeria and Taiwania (Greguss, 1955; García Esteban et al., 2002) which belong to the basal lineages of the Cupressaceae crown (i.e. the former “Taxodiaceae”). In that regard, the genus Protaxodioxylon was previously related to taxodiaceous Cupressaceae (Vozenin-Serra et al., 2011).

4.3. Reconstruction of Austrohamia and the forests of Cerro Bayo For species of woody vascular plants, reconstructing one complete whole-plant species from an admixture of fully disarticulated constituent organs is based on three lines of evidence: association/dissociation, morphological similarity and organic connection (Bateman and Hilton, 2009). In this sense, Anderson and Anderson (1985) proposed a scale to determine the degree of certainty in the linkage of different fossil bodies for reconstruction of a complete plant concept. On this scale, they proposed that the criteria for linking two or more plant organs are (from the most reliable to the least reliable): organic attachment, morphological (and anatomical) similarity, kindred reinforcement and mutual occurrence. Analyzing the first two criteria of Anderson and Anderson (1985) for the case of Austrohamia minuta, leafy twigs and branches were found in connection with the ovulate and pollen cones (Escapa et al., 2008), but not with the permineralized wood of Protaxodioxylon patagonicum sp. nov. Also, the different types of fossilization of Austrohamia minuta leaves, pollen cones and seed cones (impression-compression) and Protaxodioxylon patagonicum wood (permineralization) prevent further anatomical comparison between them. With respect to the kindred reinforcement or “support by affinity” criterion, Austrohamia possesses a combination of characters indicating placement within the basal Cupressaceae (i.e. the former “Taxodiaceae”). This conclusion is supported by a phylogenetic analysis that places the Argentinean fossil close to the extant genera Taiwania and Cunninghamia, and the fossil genera Elatides and Sewardiodendron (Escapa et al., 2008). Similarly, Protaxodioxylon patagonicum sp. nov. has several wood traits that unequivocally link this species to basal Cupressaceae (see above). In particular, P. patagonicum shows the greatest similarity with Athrotaxis, Cunninghamia, Cryptomeria and Taiwania. Finally, the studied trunks were found in the same stratigraphic levels as Austrohamia minuta (Plate I, 2), and all the conifer impressions of these fossiliferous strata belong to Austrohamia minuta; consequently the “mutual occurrence” criterion of Anderson and Anderson (1985) is fulfilled. In view of this evidence, we propose a reconstruction of Austrohamia minuta including the trunks of Protaxodioxylon patagonicum sp. nov. This conifer was an evergreen tree of ca. 16 m tall (according to Niklas, 1994a, 1994b, 1994c; estimation of tree height based on stem diameter of P. patagonicum), profusely branched, with a monopodial growth, three orders of branches, ultimate branches oriented in one plane, alternately or sub-oppositely arranged on penultimate branches and helically arranged leaves. Pollen cones were borne terminally on ultimate branches with megasporangiate cones borne in pairs at the apex of branches. This conifer constituted the tree stratum of dense forests with an understory of abundant ferns and horsetails (Fig. 2).

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

195

Fig. 2. Reconstruction of Cerro Bayo landscape (Early Jurassic, Chubut Province, Argentinean Patagonia). The canopy of the forest is formed exclusively by Austrohamia minuta (Cupressaceae). In the understorey, they can be observed dipteridaceous, osmundaceous and marattiaceous ferns. The dinosaur corresponds to Leonerasaurus taquetrensis Pol et al., 2011, from the Las Leoneras Formation. In the background, a volcano with an ash cloud is observed. Drawn by Jorge Gonzalez.

In the proposed reconstruction of Austrohamia minuta, we decided to maintain the new fossil wood in a separate taxon since, as a consequence of different types of fossilization of A. minuta and Protaxodioxylon patagonicum sp. nov., their vascular anatomy cannot be directly compared. Also, as both were found detached, the reconstruction remains hypothetical, although it is highly supported. Finally, for future cases in which isolated fossil wood is found with the diagnostic traits of P. patagonicum, a specific name for this type of fossils is required.

4.4. The wood in the reconstruction of Triassic and Jurassic conifers The Triassic forests of Gondwana were dominated by the seed ferns known as corystosperms, with conifers playing a subordinate role (Artabe et al., 2007). In those forests, transitional conifers were present, as Cheirolepidiaceae and “Voltziaceae” (Yao et al., 1993; Axsmith et al., 1998; Zamuner et al., 2001; Artabe et al., 2003; Arce and Lutz, 2010; Morel et al., 2011). These conifers have a unique character combination in their wood anatomy. In the first case, Cheirolepidiaceae possess a wood type that does not exist in living conifers (i.e. Brachyoxylon), although it has some similarity to araucariaceous wood (Bodnar et al., 2013). In the second case, the voltzian Telemachus is linked to woods with podocarpaceous traits (Axsmith et al., 1998; Escapa et al., 2010). In both cases, the reproductive characters are transitional to extant families (Bomfleur et al., 2013). This provides evidence that in the Triassic the conifers demonstrated an evolutionary mosaic, with wood traits that resemble modern conifer families while the cones were still very different from them. On the other hand, the reconstruction proposed in this work would confirm that an opposite situation occurs in the Early Jurassic, at least for the basal lineages of Cupressaceae s.l. Austrohamia minuta already exhibited cupressaceous characteristics in every known organ further supporting the relationship of this plant with the basal group of the family, as also suggested by previous phylogenetic studies.

Acknowledgments We would like to specially thank the Family Cáceres for hosting us in the field. We also wish to thank Benjamin Bomfleur, Juan Drovandi, Ana María Zavattieri, Daniela Olivera, Andrés Elgorriaga, Leandro Canessa, Magalí Cardenas, Juan Parra, Mariano Caffa and Pablo Puerta for help during several seasons of fieldwork. Special thanks to M. Caffa for his help with thin section preparation at Museo Paleontológico Egidio Feruglio. We are also grateful to Patricia Sarmiento for his invaluable help with the SEM at Museo La Plata. Editor and anonymous reviewers are also thanked for their helpful comments and suggestions. Financial support has been provided by Agencia Nacional de Promoción Científica y Tecnológica (PICT 1224 and PICT 1520 to IE; PICT 2751 to JB).

References Alvin, K.L., Fraser, C.J., Spicer, R.A., 1981. Anatomy and palaeoecology of Pseudofrenelopsis and associated conifers in the English Wealden. Palaeontology 24, 759–778. Améglio, T., Ewers, F.W., Cochard, H., Martignac, M., Vandame, M., Bodet, C., Cruiziat, P., 2001. Winter stem xylem pressure in walnut trees: effects of carbohydrates, cooling and freezing. Tree Physiol. 21 (6), 387–394. Anderson, J.M., Anderson, H.M., 1985. Palaeoflora of Southern Africa: Prodromus of South African Megafloras Devonian to Lower Cretaceous. A.A. Balkema, Rotterdam. Arce, F.E., Lutz, A.I., 2010. Fructificaciones de la Formación Los Rastros, Triásico Superior, Provincia de San Juan, Argentina. Rev. Mex. Cienc. Geol. 27 (1), 32–42. Artabe, A.E., Morel, E.M., Ganuza, D.G., 2007. Las floras triásicas de la Argentina. In: Archangelsky, S., Sánchez, T., Tonni, E.P. (Eds.), Asociación Paleontológica Argentina Publicación Especial 11 Ameghiniana 50° Aniversario, Buenos Aires, pp. 75–86. Artabe, A.E., Morel, E.M., Spalletti, L.A., 2003. Caracterización de las provincias fitogeográficas triásicas del Gondwana Extratropical. Ameghiniana 40 (3), 387–405. Axsmith, B.J., Taylor, T.N., Taylor, E.L., 1998. Anatomically preserved leaves of the conifer Notophytum krauselii (Podocarpaceae) from the Triassic of Antarctica. Am. J. Bot. 85 (5), 704–713. Bailey, I.W., 1953. Evolution of the tracheary tissue of land plants. Am. J. Bot. 40 (1), 4–8. Bailey, I.W., Srivastava, L.M., 1962. Comparative anatomy of the leaf-bearing Cactaceae, IV. The fusiform initials of the cambium and the form and structure of their derivatives. J. Arnold Arbor. 43, 187–202. Bamford, M.K., Corbett, I.B., 1994. Fossil wood of Cretaceous age from the Namaqualand continental shelf, South Africa. Palaeontol. Afr. 31, 83–95.

196

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197

Bamford, M.K., Philippe, M., 2001. Jurassic - Early Cretaceous Gondwanan homoxylous woods: a nomenclatural revision of the genera with taxonomic notes. Rev. Palaeobot. Palynol. 113 (4), 287–297. Bateman, R.M., Hilton, J., 2009. Palaeobotanical systematics for the phylogenetic age: applying organ–species, form–species and phylogenetic species concepts in a framework of reconstructed fossil and extant whole–plants. Taxon 58 (4), 1254–1280. Beck, C.B., 2010. An Introduction to Plant Structure and Development: Plant Anatomy for the Twenty-First Century. 2nd Edition. Cambridge University Press, Cambridge. Bodnar, J., Escapa, I.H., Cúneo, R., Gnaedinger, S., 2013. First record of conifer wood from the Cañadón Asfalto Formation (Early–Middle Jurassic), Chubut province, Argentina. Ameghiniana 50 (2), 227–239. Bodnar, J., Ruiz, D., Artabe, A.E., Morel, E.M., Ganuza, D.G., 2015. Voltziales y Pinales (= Coniferales) de la Formación Cortaderita (Triásico Medio), Argentina, y su implicancia en la reconstrucción de las coníferas triásicas. Rev. Bras. Paleontol. 18 (1), 141–160. Bomfleur, B., Decombeix, A.-L., Escapa, I.H., Schwendemann, A.B., Axsmith, B., 2013. Whole-plant concept and environment reconstruction of a Telemachus conifer (Voltziales) from the Triassic of Antarctica. Int. J. Plant Sci. 174 (3), 425–444. Bonetti, M.I.R., 1966. Protojuniperoxylon ischigualastensis sp. nov. del Triásico de Ischigualasto (San Juan). Ameghiniana 4 (7), 211–218. Boureau, E., 1956. Anatomie Végétale: L'appareil végétatif des Phanérogames. Tome 2d. Presses Universitaires de France, Paris. Boutelje, J.B., 1955. The wood anatomy of Libocedrus Endl., s. lat., and Fitzroya J. D. Hook. Acta Horti Berg. 17 (6), 177–216. Cantrill, D.J., 1995. The occurrence of the fern Hausmannia Dunker (Dipteridaceae) in the Cretaceous of Alexander Island. Antarctica. Alcheringa 19 (3), 243–254. Carlquist, S., 1975. Ecological Strategies of Xylem Evolution. University of California Press, Berkeley and London. Carlquist, S., 1988. Comparative Wood Anatomy. Springer, Berlin and Heidelberg. Carlquist, S., 2001. Comparative Wood Anatomy. Systematic, Ecological, and Evolutionary Aspects of Dicotyledon Wood. 2nd edition. Springer, Berlin. Carlquist, S., 2012. Wood anatomy of Gnetales in a functional, ecological, and evolutionary context. Aliso 30 (1), 33–47. Cevallos Ferriz, S.R.S., 1992. Tres maderas de gimnospermas cretácicas del norte de México. Anales del Instituto de Biología, Ser. Botánica, pp. 111–137. Channing, A., Zamuner, A.B., Zúniga, A., 2007. A new Middle–Late Jurassic flora and hot spring chert deposit from the Deseado Massif, Santa Cruz province, Argentina. Geol. Mag. 144 (2), 401–411. Crisafulli, A., Herbst, R., 2011. La flora triásica del Grupo El Tranquilo, provincia de Santa Cruz (Patagonia): Leños fósiles. Ameghiniana 48 (3), 275–288. Cúneo, N.R., Ramezani, J., Scasso, R., Pol, D., Escapa, I.H., Zavattieri, A.M., Bowring, S.A., 2013. High-precision U-Pb geochronology and a new chronostratigraphy for the Cañadón Asfalto Basin, Chubut, central Patagonia: implications for terrestrial faunal and floral evolution in Jurassic. Gondwana Res. 24 (3–4), 1267–1275. De Magistris, A.A., 1997. Anatomía de la madera de las especies de Cupressus (Cupressaceae) cultivadas en la Argentina. Bol. Soc. Argent. Bot. 33 (1–2), 91–105. Ding, Q.H., Fu, X.P., Li, Y., Zhang, W., 2011. New species of Late Mesozoic fossil woods from southeastern Mongolia (in Chinese with English abstract). Glob. Geol. 14 (2), 59–66. Elgorriaga, A., Escapa, I.H., Bomfleur, B., Cúneo, N.R., Ottone, G.E., 2015. Reconstruction and phylogenetic significance of a new Equisetum Linnaeus species from the Lower Jurassic of Cerro Bayo (Chubut Province, Argentina). Ameghiniana 52 (1), 135–152. Esau, K., 1977. Anatomy of Seed Plants. 2nd edition. Wiley, New York. Escapa, I.H., 2009. La tafoflora de la Formación Cañadón Asfalto, Jurásico Medio Superior de Chubut Taxonomía, bioestratigrafía y paleofitogeografía PhD thesis Universidad Nacional del Comahue, Bariloche, Argentina. Escapa, I.H., Cúneo, N.R., 2012. Fertile Osmundaceae from the Early Jurassic of Patagonia, Argentina. Int. J. Plant Sci. 173 (1), 54–66. Escapa, I.H., Bomfleur, B., Cúneo, N.R., Scasso, R., 2014. A new marattiaceous fern from the Lower Jurassic of Patagonia (Argentina): the renaissance of Marattiopsis. J. Syst. Palaeontol. 13 (8), 677–689. Escapa, I.H., Cúneo, N.R., Axsmith, B., 2008. A new genus of the Cupressaceae (sensu lato) from the Jurassic of Patagonia: implications for conifer megasporangiate cone homologies. Rev. Palaeobot. Palynol. 151 (3–4), 110–122. Escapa, I.H., Cúneo, N.R., Rothwell, G.W., Stockey, R.A., 2013. Pararaucaria delfueyoi sp. nov. from the Late Jurassic Cañadón Calcáreo Formation, Chubut, Argentina: insights into the evolution of the Cheirolepidaceae. Int. J. Plant Sci. 174 (3), 458–470. Escapa, I.H., Decombeix, A.-L., Taylor, E.L., Taylor, T.N., 2010. Evolution and relationships of the conifer seed cone Telemachus: evidence from the Triassic of Antarctica. Int. J. Plant Sci. 171 (5), 560–573. Escapa, I.H., Rothwell, G.W., Stockey, R.A., Cúneo, N.R., 2012. Seed cone anatomy of Cheirolepidiaceae (Coniferales): reinterpreting Pararaucaria patagonica Wieland. Am. J. Bot. 99, 1058–1068. Evert, R.F., 2006. Esau's Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their Structure, Function, and Development. 3rd Edition. John Wiley & Sons, New Jersey. Fahn, A., 1990. Plant Anatomy. Pergamon Press, Oxford. Fahn, A., Leshem, B., 1963. Wood fibres with living protoplasts. New Phytol. 62 (1), 91–98. Falaschi, P., Grosfeld, J., Zamuner, A.B., Foix, N., Rivera, S.M., 2011. Growth architecture and silhouette of Jurassic conifers from La Matilde Formation, Patagonia, Argentina. Palaeogeogr. Palaeoclimatol. Palaeoecol. 302 (3–4), 122–141. Farjon, A., 2001. A World Checklist and Bibliography of Conifers. 2nd edition. Kew Publishing, London. Farjon, A., 2005. A Monograph of Cupressaceae and Sciadopitys. Kew Publishing, London. Figari, E., Scasso, R., Cúneo, R., Escapa, I., 2015. Estratigrafía y evolución geológica de la Cuenca de Cañadón Asfalto, provincia del Chubut, Argentina. Lat. Am. J. Sedimentol. Basin Anal. 22 (2), 135–169.

Frison, E., 1948. De la présence d'Amidon dans le Lumen des Fibres du Bois. Bull. Agric. Congo Belge 39, 869–874. Gadek, P.A., Alpers, D.L., Heslewood, M.M., Quinn, C.J., 2000. Relationships within Cupressaceae sensu lato: a combined morphological and molecular approach. Am. J. Bot. 87 (7), 1044–1057. García Esteban, L., Palacios de Palacios, P., de Guindeo Casasús, A., García Esteban, L., Lázaro Durán, I., González Fernández, L., Rodríguez Labrador, Y., García Fernández, F., Bobadilla Maldonado, I., Camacho Atalaya, A., 2002. Anatomía e identificación de maderas de coníferas a nivel de especie. Mundi-Prensa, Madrid. Gnaedinger, S., Herbst., R., 2009. Primer registro de maderas gimnospérmicas de la Formación Roca Blanca (Jurásico Inferior), provincia de Santa Cruz, Argentina. Ameghiniana 46 (1), 59–71. Gnaedinger, S., García Massini, J.L., Bechis, F., Zavattieri, A.M., 2015. Coniferous woods and wood-decaying fungi from the el Freno Formation (Lower Jurassic), Neuquen Basin, Mendoza Province, Argentina. Ameghiniana 52 (4), 447–467. Greguss, P., 1955. Identification of Living Gymnosperms on the Basis of Xylotomy. Akádemiai Kiadó, Budapest. Hacke, U.G., 2015. The hydraulic architecture of Populus. In: Hacke, U.G. (Ed.), Functional and Ecological Xylem Anatomy. Springer, Berlin and Heidelberg, pp. 103–131. Jane, F.W., 1956. The Structure of Wood. Black, London. Jeffrey, E.C., 1925. The origin of parenchyma in geological time. Proc. Natl. Acad. Sci. U. S. A. 11 (1), 106–110. Klepzig, K.D., Smalley, E.B., Raffa, K.F., 1995. Dendroctonus valens and Hylastes porculus: vectors of pathogenic fungi associated with red pine decline disease. Great Lakes Entomol. 28 (1), 81–87. Kräusel, R., 1949. Die fossilen Koniferenhölzer (unter Ausschluβ von Araucarioxylon Kraus), II. Kritische Untersuchungen zur Diagnostik lebender und fossiler Koniferen-Hölzer. Palaeontogr. B 89, 81–203. Leslie, A.B., Beaulieu, J.M., Rai, H.S., Crane, P.R., Donoghue, M.J., Mathews, S., 2012. Hemisphere-scale differences in conifer evolutionary dynamics. Proc. Natl. Acad. Sci. U. S. A. 109 (40), 16217–16221. Mao, K., Milne, R.I., Zhang, L., Peng, Y., Liu, J., Thomas, P., Mill, R.R., Renner, S.S., 2012. Distribution of living Cupressaceae reflects the breakup of Pangea. Proc. Natl. Acad. Sci. U. S. A. 109 (20), 7793–7798. Mauseth, J.D., 2012. Botany: An Introduction to Plant Biology. 5th edition. Jones and Bartlett Learning, Sudbury. Medlyn, D.A., Tidwell, W.D., 1975. Conifer wood from the Upper Jurassic of Utah, part I. Xenoxylon morrisonense sp. nov. Am. J. Bot. 62 (2), 203–208. Miller, C.N., 1977. Mesozoic conifers. Bot. Rev. 43 (2), 217–280. Miller, C.N., 1982. Current status of Paleozoic and Mesozoic conifers. Rev. Palaeobot. Palynol. 37 (1–2), 99–114. Money, L.L., Bailey, I.W., Swamy, B.G.L., 1950. The morphology and relationships of the Monimiaceae. J. Arnold Arbor. 31 (4), 372–404. Morel, E.M., Artabe, A.E., Ganuza, D., Zúñiga, A., 2011. La paleoflora triásica del Cerro Cacheuta, provincia de Mendoza. Petriellales, Cycadales, Ginkgoales, Voltziales, Coniferales, Gnetales y Gimnospermas incertae sedis. Ameghiniana 48 (4), 520–540. Nadjafi, A., 1982. Contribution à la connaissance de la flore ligneuse du Jurassique d'Iran. Niklas, K.J., 1994a. Plant Allometry: The Scaling of Form and Process. University of Chicago Press, Chicago. Niklas, K.J., 1994b. The allometry of safety-factors for plant height. Am. J. Bot. 81 (3), 345–351. Niklas, K.J., 1994c. Predicting the height of fossil plant remains: an allometric approach to an old problem. Am. J. Bot. 81 (10), 1235–1242. Olivera, D.E., Zavattieri, A.M., Quattrocchio, M.E., 2015. The palynology of the Cañadón Asfalto Formation (Jurassic), Cerro Cóndor depocentre, Cañadón Asfalto Basin, Patagonia. Argentina: palaeoecology and palaeoclimate based on ecogroup analysis. Palynology 39 (3), 362–386. Panti, C., Pujana, R.R., Zamaloa, M.C., Romero, E.J., 2012. Araucariaceae macrofossil records from South America and Antarctica. Alcheringa 36 (1), 1–22. Patel, R.N., 1968. Wood anatomy of Cupressaceae and Araucariaceae indigenous to New Zealand. N. Z. J. Bot. 6 (1), 9–18. Peirce, A.S., 1937. Systematic anatomy of the woods of the Cupressaceae. Trop. Woods 49, 5–21. Philippe, M., 1995. Bois fossiles du Jurassique de Franche-Comté (nord-est de la France): systématique et biogéographie. Palaeontogr. B 236, 325–343. Philippe, M., Bamford, M.K., 2008. A key to morphogenera used for Mesozoic conifer-like woods. Rev. Palaeobot. Palynol. 148 (2–4), 184–207. Philippe, M., Barbacka, M., Gradinaru, E., Iamendei, E., Iamandei, S., Kázmér, M., Popa, M., Szakmány, G., Tchoumatchenco, P., Zaton, M., 2006. Fossil wood and Mid-Eastern Europe terrestrial palaeobiogeography during the Jurassic–Early Cretaceous interval. Rev. Palaeobot. Palynol. 142 (1), 15–32. Philippe, M., Billon-Bruyat, J.-P., Garcia-Ramos, J.C., Bocat, L., Gomez, B., Piñuela, L., 2010. New occurrences of the wood Protocupressinoxylon purbeckensis Francis: implications for terrestrial biomes in southwestern Europe at the Jurassic/Cretaceous boundary. Palaeontology 53 (1), 201–214. Pol, D., Garrido, A., Cerda, I.A., 2011. A new Sauropodomorph dinosaur from the Early Jurassic of Patagonia and the origin and evolution of the Sauropod-type sacrum. PLoS One 6 (1), e14572. Pole, M., 2008. The record of Araucariaceae macrofossils in New Zealand. Alcheringa 32 (4), 405–426. Quattrocchio, M.E., Sarjeant, W.A.S., Volkheimer, W., 1996. Marine and terrestrial Jurassic microfloras of Neuquén Basin (Argentina): palynological zonation. GeoResearch Forum 1–2, 167–178. Rees, P.M., Cleal, C.J., 2004. Lower Jurassic floras from Hope Bay and Botany Bay, Antarctica. Special Papers in Palaeontology Vol. 72. Blackwell Publishing, London, pp. 1–90.

J. Bodnar, I.H. Escapa / Review of Palaeobotany and Palynology 234 (2016) 186–197 Richter, H.G., Grosser, D., Heinz, I., Gasson, P.E. (Eds.), 2004. International Association of Wood Anatomists list of microscopic features for softwood identificationIAWA J. 25 (1), 1–70. Roig, F.A., 1992. Comparative wood anatomy of Southern South American Cupressaceae. IAWA Bull. 13 (1–4), 151–162. Rowell, R.M. (Ed.), 2012. Handbook of Wood Chemistry and Wood Composites, Second Edition CRC Press, Boca Raton. Salleo, S., Lo Gullo, M.A., Trifilò, P., Nardini, A., 2004. New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis. Plant Cell Environ. 27 (8), 1065–1076. Shi, G., Leslie, A.B., Herendeen, P.S., Ichinnorov, N., Takahashi, M., Knopf, P., Crane, P.R., 2014. Whole-plant reconstruction and phylogenetic relationship of Elatides zhoui sp. nov. (Cupressaceae) from the Early Cretaceous of Mongolia. Int. J. Plant Sci. 175 (8), 911–930. Stewart, W.N., Rothwell, G.W., 1993. Paleobotany and the Evolution of Plants. Cambridge University Press, Cambridge. Stockey, R.A., 1977. Reproductive biology of the Cerro Cuadrado (Jurassic) fossil conifers: Pararaucaria patagonica. Am. J. Bot. 64 (6), 733–744. Stockey, R.A., 1978. Reproductive biology of Cerro Cuadrado fossil conifers: ontogeny and reproductive strategies in Araucaria mirabilis. Palaeontographica 166B, 1–15. Thomson, R.B., 1913. On the comparative anatomy and affinities of the Araucarineae. Philos. Trans. R. Soc. Lond. B 204, 1–46. Tian, N., Xie, A., Wang, Y., Jiang, Z., Li, L., Yin, Y., Zhu, Z., Wang, J., 2015. New records of Jurassic petrified wood in Jianchang of western Liaoning, China and their palaeoclimate implications. Sci. China Earth Sci. 58 (12), 2154–2164. Tidwell, W., Thayn, G.F., 1986. Agathoxylon lemonii sp. nov., from the Dakota Formation, Utah. Gt. Basin Nat. 46 (3), 559–563. Torres, T., Biró-Bagóczky, L., 1986. Xilotomía de coníferas fósiles de la isla Quiriquina, Chile. Universidad de Chile, Comunicaciones Vol. No. 37, pp. 65–80. Torres, T., Philippe, M., 2002. Nuevas especies de Coniferales y Ginkgoales del Lías de La Ligua (Chile) con una evaluación del registro paleoxilológico en el Jurásico de Sudamérica. Rev. Geol. Chile 29 (2), 151–165. Townrow, J.A., 1967a. On Rissikia and Mataia — podocarpaceous conifers from the lower Mesozoic of southern lands. Pap. Proc. R. Soc. Tasmania 101, 103–136.

197

Townrow, J.A., 1967b. On a conifer from the Jurassic of East Antarctica. Pap. Proc. R. Soc. Tasmania 101, 137–146. Trapp, S., Croteau, R., 2001. Defensive resin biosynthesis in conifers. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 689–724. Tyree, M.T., Salleo, S., Nardini, A., Lo Gullo, M.A., Mosca, R., 1999. Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiol. 120 (1), 11–21. Vaudois, N., Privé, C., 1971. Révision des bois fossiles de Cupressaceae. Palaeontogr. B 134 (1–3), 61–86. Vogellehner, D., 1968. Zur Anatomie und Phylogenie mesozoischer Gymnospermenhölzer, 7: Prodomus zu einer Monographie der Protopinaceae. 2. Die protopinoiden Hölzer des Jura. Palaeontogr. B 124, 125–162. Vozenin-Serra, C., Diez, J.B., Ferrer, J., 2011. A new species of Protaxodioxylon (Cupressaceae s.l.) from the late Albian of the Aragonian branch of the Iberian Range (Spain) Palaeoclimatic implications. Geodiversitas 33 (1), 11–24. Yao, X., Taylor, T.N., Taylor, E.L., 1993. The Triassic seed cone Telemachus from Antarctica. Rev. Palaeobot. Palynol. 78 (3–4), 269–276. Yao, X., Zhou, Z., Zhang, B., 1998. Reconstruction of the Jurassic conifer Sewardiodendron laxum (Taxodiaceae). Am. J. Bot. 85 (9), 1289–1300. Youssef, S.G.M., 2002. Xenoxylon wood from Late Jurassic–Early Cretaceous of Gebel Kamil, Egypt. IAWA J. 23 (1), 69–76. Zamuner, A.B., Zavattieri, A.M., Artabe, A.E., Morel, E.M., 2001. Paleobotánica. In: Artabe, A.E., Morel, E.M., Zamuner, A.B. (Eds.), El Sistema Triásico de Argentina, La Plata, Fundación Museo de La Plata “Francisco Pascasio Moreno”, pp. 143–184. Zavattieri, A.M., Rosenfeld, U., Volkheimer, W., 2006. Palynofacies analysis and sedimentary environment of Early Jurassic coastal sediments at the southern border of the Neuquén Basin, Argentina. J. S. Am. Earth Sci. 25 (2), 227–245. Zhang, J.-W., D'Rozario, A., Wang, L.-J., Li, Y., Yao, J.-X., 2012. A new species of the extinct genus Austrohamia (Cupressaceae s.l.) in the Daohugou Jurassic flora of China and its phytogeographical implications. J. Syst. Evol. 50 (1), 72–82.