AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 ARTICLES ISSN 0002-7014 RECONSTRUCTION AND PHYLOGENETIC SIGNIFICANCE OF A NEW EQUISETUM LINNAEUS SPECIES FROM THE LOWER JURASSIC OF CERRO BAYO (CHUBUT PROVINCE, ARGENTINA) ANDRÉS ELGORRIAGA1, IGNACIO H. ESCAPA2, BENJAMIN BOMFLEUR3, RUBÉN CÚNEO2 AND EDUARDO G. OTTONE4 1 Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón nº 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina. aelgorriaga@gmail.com 2 Consejo Nacional de Investigaciones Científicas y Técnicas, Museo Paleontológico Egidio Feruglio, Avenida Fontana 140, U9100GYO Chubut, Argentina. iescapa@mef.org.ar; rcuneo@mef.org.ar 3 Department of Palaeobiology, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden. benjamin.bomfleur@nrm.se 4 Instituto de Estudios Andinos Don Pablo Groeber-Consejo Nacional de Investigaciones Científicas y Técnicas, Departamento de Ciencias Geológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón n° 2, Ciudad Universitaria, C1428EHA Buenos Aires, Argentina. ottone@gl.fcen.uba.ar Abstract. We describe Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Patagonia, Argentina. This new species is based on fertile and vegetative remains preserved as impressions of stems, leaves, strobili, transversal sections of the stems showing their anatomy, and terminal pagoda-like structures. The fine-grained sedimentary matrix also preserved detailed impressions of epidermal features. The morphological characters allow a whole-plant reconstruction and assignment to Equisetum. Equisetum dimorphum sp. nov. shows a mosaic of morphological characters that are commonly present in other Mesozoic forms and representatives of the two extant Equisetum subgenera, e.g., sunken stomata and a blunt strobilus apex. Compared to other well-known Mesozoic equisetalean taxa, Equisetum dimorphum sp. nov. appears to be most closely related to a group of Jurassic Equisetum-like plants including Equisetum laterale Phillips and Equisetites ferganensis Seward. Additional evidence for the morphological stasis of the fertile and vegetative organs of extant horsetails is supplied with this new material, adding further support to the hypothesis that the extant horsetails are a successful group that has undergone only little morphological changeover time and that has been present, nearly worldwide, since Jurassic times. Key words. Equisetales. Equisetum. Systematic. Jurassic. Patagonia. Resumen. RECONSTRUCCIÓN E IMPLICANCIAS FILOGENÉTICAS DE UNA NUEVA ESPECIE DE EQUISETUM LINNAEUS DEL JURASICO INFERIOR DE CERRO BAYO (PROVINCIA DEL CHUBUT, ARGENTINA). En el presente trabajo se describe Equisetum dimorphum sp. nov., una nueva equisetal del Jurásico Inferior de la Provincia del Chubut, Patagonia, Argentina. Esta nueva especie está basada tanto en restos vegetativos como fértiles, preservados como impresiones y moldes de ejes, hojas, estróbilos, secciones transversales de los ejes mostrando su anatomía y estructuras terminales de tipo “pagoda”. El grano fino del sedimento ayudó a preservar también impresiones detalladas de caracteres epidérmicos. Los caracteres morfológicos preservados permiten la reconstrucción de la planta y su asignación a Equisetum. La relación de E. dimorphum sp. nov. con otras equisetales del Mesozoico es discutida. Equisetum dimorphum sp. nov. muestra un mosaico de caracteres morfológicos que comúnmente se encuentran presentes en distintos representantes de los dos subgéneros de Equisetum, e.g., estomas hundidos y un ápice estrobilar romo. En comparación con otros taxones bien conocidos de equisetales del Mesozoico, Equisetum dimorphum sp. nov. parece estar más cercanamente emparentado con un grupo de plantas de tipo Equisetum del Jurásico, que incluye a Equisetum laterale Phillips y Equisetites ferganensis Seward. Se aporta evidencia adicional acerca del estasis morfológico de los órganos fértiles y vegetativos de Equisetum actuales, añadiendo de esta manera mayor sustento a la hipótesis que sugiere que Equisetum es un género exitoso que no ha cambiado mucho morfológicamente a través del tiempo y que ha tenido una distribución prácticamente global desde el Jurásico. Palabras clave. Equisetales. Equisetum. Sistemática. Jurásico. Patagonia. EQUISETALEANS are a group of plants with a worldwide dis- and in the Jurassic there were only a reduced number of tribution since Paleozoic times (see Boureau, 1964). Their equisetalean plants, of which only one lineage survived origins are traceable to the Late Devonian with the Ar- through the Cenozoic up to the present days (Des Marais et chaeocalamitaceae (Taylor et al., 2009), showing a major di- al., 2003). versification in the Pennsylvanian (Bierhorst, 1971). By the The genus Equisetum Linnaeus 1753, which includes 15 end of the Paleozoic this diversity was dramatically reduced species according to the most widely accepted taxonomic (Behrensmeyer et al., 1992; Stewart and Rothwell, 1993) treatment (Hauke, 1963, 1978), is the single extant repre- AMGHB2-0002-7014/12$00.00+.50 135 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 sentative of the equisetalean clade. Equisetum has a nearly fossils with non-strobilar arrangements of sporangio- worldwide distribution, with Australia, Antarctica, New Zea- phores that are virtually identical to those seen in certain land and several South Pacific islands being the only regions teratologies of extant horsetails (Tschudy, 1939; Naugol- without natural populations of the genus (Hauke, 1963). nykh, 2004). Fossil representatives of Equisetum have been variously Living species of Equisetum have been traditionally suggested to occur in deposits as old as the Jurassic (Gould, grouped into two subgenera: Equisetum and Hippochaete. 1968), with some Mesozoic species being practically in- This division is supported by numerous morphological distinguishable from their extant counterparts in either characters, such as: (1) stomatal position and ornamenta- anatomy nor morphology (Channing et al., 2011). tion, (2) branching pattern, (3) chromosome size, (4) stro- Recent phylogenetic analyses of extant species using bilus apex, (5) stem dimorphism, (6) antheridial morphology, both molecular and morphological data support the position (7) lamellae type, (8) endodermis type, (9) cell wall texture of of Equisetum as part of the Moniliformopses clade, a lineage root hairs and (10) free leaf tips persistence (Milde, 1867; first instituted by Kenrick and Crane (1997) based on the Hauke, 1963, 1978; Page, 1972a,b; Duckett, 1979; Emons, analysis of stelar patterns of fossil species. Within this 1986). Molecular phylogenetic analyses recovered the mo- group, Equisetum was suggested as sister group of the nophyly of the Hippochaete clade, but not that of the Equi- marattioid ferns (Pryer et al., 2001, 2004). Subsequent setum clade (Des Marais et al., 2003; Guillon, 2004, 2007) studies placed Equisetum as the sister group of the due largely to the inconsistent placement of Equisetum bo- Ophioglossidae+Psilotidae clade (Karol et al., 2010; Grewe gotense Kunth, 1815 in different studies (see Guillon, 2007 et al., 2013; Christenhusz and Chase, 2014), which had and references therein). been previously suggested on the basis of ultrastructural The date for the diversification of the Equisetum crown features of their spores (Grauvogel-Stamm and Lugardon, group remains controversial. It has been estimated, using 2009). On the other hand, phylogenetic analyses also in- molecular data, to have occurred in the Cenozoic (Des Marais cluding extinct equisetaleans suggest that the genus Equi- et al., 2003). In contrast it also has been estimated as 136 setum is not contained within the ferns (Rothwell, 1999). Ma. (Early Cretaceous) from the fossil record (Stanich et al., Rather, those studies resolve Equisetales as the sister 2009) and possibly extending far back into the Jurassic, group to zygopterids+cladoxylopsids, a view that is less at since nearly all synapomorphies that define the crown group odds with traditional phylogenetic reconstructions for the Equisetum already occur in the anatomically preserved Equi- overall pattern of euphyllophyte evolution (Rothwell and setum thermale Channing, Zamuner, Edwards and Guido, Nixon, 2006). 2011 from the Jurassic of Argentina (see Channing et al., Another question that remains unresolved concerning 2011). Nonetheless, a phylogenetic analysis including both the origins and evolution of modern Equisetum is to which living and fossil representatives of the genus is required in clade of fossil sphenopsids they are most closely related; order to confirm the position of fossil Equisetum species as and, as a consequence, whether the characteristically part of the crown group, and therefore, the diversification peltate sporangiophores appeared just once in the evolu- minimum age for that group. tionary history of these plants. The traditional view is that A great number of equisetalean remains have been the peltate sporangiophores of Equisetum are homologous found in Mesozoic rocks of Gondwana, the vast majority of to those of the calamitaleans, and that those are, in turn, them have been assigned to the genera Neocalamites Halle, homologous to the cruciate sporangiophores of the ar- 1908, Equisetites Sternberg, 1833 or Equisetum (see Villar chaeocalamiteans (Good, 1975). An alternative view is that de Seoane, 2005; Channing et al., 2011; Bomfleur et al., peltate sporangiophores appeared independently, once in 2013). Differences between the latter two genera have the lineage that gave rise to calamitalean plants, and a been extensively discussed (e.g., Harris, 1961; Gould, 1968; second time in the lineage that gave rise to modern equi- Stanich et al., 2009), and many of their representatives have setaleans including Equisetum (Cúneo and Escapa, 2006). been suggested to belong to the same evolutionary lineage The latter hypothesis is based on Angaran and Gondwanan leading to the extant horsetails (Boureau, 1964; Gould, 1968). 136 ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM In this contribution we describe a new equisetalean details, and organic attachments allowed an almost com- plant from the Lower Jurassic of Argentina, preserved as im- plete reconstruction of the aerial parts of the plant, provid- pressions and casts. The large number of organs (e.g., axes, ing important information about its paleobiological features leaf whorls, nodal diaphragms, strobili), the fine epidermal and the evolution of ancient Equisetum representatives. Figure 1. 1. Location and geology of the Equisetum dimorphum sp. nov. fossil localities; 2. Simplified stratigraphic section showing the main lithostratigraphic units cropping out in the Cerro Bayo area. Radioisotopic dates on the Cañadón Asfalto Formation are indicated: (i) 177.37 ± 0.12 Ma; (ii) 176.15 ± 0.12 (see Cúneo et al., 2013). The star indicates the fossiliferous beds. 137 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 Institutional abbreviations. MPEF-Pb, Museo Paleontológico tum site”) occurs in light-gray to pale yellowish orange, par- Egidio Feruglio, Trelew, Chubut, Argentina, paleobotanical tially silicified mudstones, and consists of vegetative stems, collection. foliar whorls, nodal diaphragms, stem apices, and strobili preserved in the form of impressions, molds, and casts. MATERIALS AND METHODS Owing to the fine-grained matrix and presumably early ce- The material was collected at the Cerro Bayo locality mentation with silica, many impressions and casts preserve near Gastre, northwest Chubut Province, Argentina (Fig. a very fine relief of epidermal and other fine-structural de- 1.1). Fossiliferous horizons at this locality belong to an un- tails. Organic remains are generally not preserved, but some named unit of fluvial deposits, stratigraphically equivalent specimens are stained in reddish-brown colours probably to the Las Leoneras Formation in the Las Leoneras and due to precipitation of iron oxides. The material from the Zaino canyons further south, that are overlain by a succes- other plant-bearing bed is overall similar in preservation, sion of agglomerates and lava flows (Lonco Trapial Forma- but occurs in dark-gray mudstones and does not show pre- tion) and lacustrine deposits (Cañadón Asfalto Formation) served of fine-structural details. (Fig. 1.2). Recent radiometric dating of ash layers from the Macroscopic images were taken with a Canon (EOS 7D) Cañadón Asfalto Fm. and Las Leoneras Fm. have yielded U- camera under halogen lighting projected at different angles. Pb (CA-TIMS method) zircon average ages of 177.4 +/- 0.1 Cellular and other fine-structural details were analysed Ma (early Toarcian) and 188.9 +/- 0.1 Ma respectively, and photographed using a Nikon SMZ1000 stereoscope mi- suggesting an Early Jurassic (most likely Pliensbachian) age croscope with an attached digital camera. Image stacking for the plant-bearing beds of the unnamed unit underlying technique was performed using Adobe Photoshop CS6 in the Lonco Trapial Formation (Cúneo et al., 2013). The taxo- order to obtain one well-focused composite image from nomic composition of the plant-fossil assemblages with several individual images captured at successive focal abundant Goeppertella Oishi and Yamasita, 1936, Dictyophyl- planes (Bercovici et al., 2009). lum Lindley and Hutton, 1834, and Sagenopteris Presl in Sternberg emend Rees, 1993 (see Escapa et al., 2008a) pro- SYSTEMATIC PALEONTOLOGY vides further support for an Early Jurassic age assignment (see Escapa et al., 2008b; Escapa and Cúneo, 2012). The majority of the specimens described here were Order EQUISETALES sensu Boureau, 1964 Family EQUISETACEAE sensu Good, 1975 collected from a single plant-bearing bed at a site informally named Equisetum site (GPS coordinates are available upon Genus Equisetum Linnaeus, 1753 request to the authors). The plant-fossil assemblage of this bed is strongly dominated by Equisetum, with only few Type species. Equisetum fluviatile Linnaeus, 1753. subordinate occurrences of the conifer Austrohamia minuta Escapa et al. 2008b also the dipteridaceous ferns Dic- Section and subgenus indet. tyophyllum and Goeppertella and the osmundaceous ferns Equisetum dimorphum sp. nov. Osmundopsis rafaelii and Todites cacereii Escapa and Cúneo, Figures 2–8 2012. Additional Equisetum specimens were collected from another plant-bearing bed at a site in close proximity. In Derivation of name. The specific epithet (gr. dimorphos= addition to Equisetum the assemblage of this second bed having two forms) is chosen in reference to the distinctly contains Dictyophyllum, Goeppertella, the marattiaceous fern different morphology of apical leaf whorls of fertile stems; Marattiopsis patagonica, various seed-fern taxa and subor- it furthermore appropiately describes the two different dinate occurrences of Austrohamia minuta and the two os- preservational aspects of the nodal region. mundaceous ferns mentioned above (Escapa, 2009; Escapa Diagnosis. Stems unbranched, externally smooth, and inter- et al., 2014). nally hollow except at the nodes. Complex nodal septa, with Most of the studied material (i.e., that from the “Equise- 138 external diaphragm portion circular, flat, bearing pitted ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM Figure 2. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1, MPEF-Pb 6472; 2, MPEF-Pb 5931. Abbreviations: cf, commissural furrows; lw, leaf whorls; pd, pitted diaphragm; pg, pagoda structure. Scale bars 1= 10 mm; 2= 5 mm. microrelief in a vague radial arrangement, surrounded by Internodal epidermal cells are square to rectangular, in an internal ring of carinal canals and an external ring of longitudinal rows; stomata usually sunken and distributed in vallecular canals; internal diaphragm part with robust broad bands. Strobili single, terminal, cylindrical to oblong, tissues forming an upwardly convex structure resembling a with whorls of densely arranged sporangiophores bearing cart-wheel, with a central hub, radiating spokes, and a thin penta- or hexagonal distal shields with a central umbo and peripheral rim of scalloped appearance; polygonal cells with abaxial sporangia; strobili subtended by heteromorphic leaf thickened walls occur at the hub and the spokes. Nodal leaf whorls with their tips at least three to four times longer whorls consisting of a fused basal sheath and free, lanceo- than those of regular leaf whorls. late, usually spreading, distal leaf tips; sheath portion Holotype. MPEF-Pb 5894a,b. comprising usually 75–80% of the total leaf-length, with bi- Paratypes. MPEF-Pb 5879–5893, 5895–5940, 6472–6479. carinate commissural furrows composed of a sunken cen- Additional material. MPEF-Pb 2684–2685, 2705 and 2712. tral region with large, transversely oriented cells bounded Geographic occurrence. Cerro Bayo area, NW Chubut by oblique flanks with obliquely oriented cells. Number of Province, Argentina. leaves, vallecular canals, and spokes usually between 12 Stratigraphic occurrence. Unnamed beds conformably over- and 42. Stem apices commonly terminating in pagoda-like lain by the Early Jurassic (early Pliensbachian to early Toar- structures. cian) volcanics of the Lonco Trapial Formation. 139 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 Description gitudinal ridges or furrows (Fig. 2.2). The nodes are indis- Stems. Aerial stems are unbranched, cylindrical, and uni- tinct, and show a gradual transition from internode to leaf- formly wide (i.e., not swollen at the node level) of up to 23 sheath surface. Epidermal cells on the internodes are square mm in compressions and with a diameter of up to 18 mm in to rectangular in shape, about 40–90 µm long and 30–50 transverse stem sections. Internodes are up to 38 mm long µm wide, and uniformly arranged in parallel, straight, longi- (Fig. 2.1) and show a smooth external surface without lon- tudinal rows (Fig. 3.3–4). Figure 3. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1. Epidermal details of the leaf sheath of MPEF-Pb 6473a; 2. Epidermis of MPEF-Pb 5940. 3. Lower portion of the leaf sheath of MPEF-Pb 5939; 4. Epidermis of the internode showing longitudinal columns of quadrangular to rectangular cells of MPEF-Pb 6474. Abbreviations: cf, commissural furrows; fl, free leaves; st, stomata. Scale bars 1= 0.5 mm; 2= 0.1 mm; 3-4= 0.4 mm. 140 ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM Figure 4. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1. Leaf whorl showing spreading free leaves of MPEF-Pb 5884; 2. Lateral view of a leaf whorl showing the fused leaf sheath of MPEF-Pb 5915; 3. Leaf whorl of MPEF-Pb 5916b; 4. Leaf whorl of MPEF-Pb 5907; 5. Leaf whorl with spreading long leaves of MPEF-Pb 5895a; 6. Leaf whorl with numerous leaf tips of MPEF-Pb 5883. Abbreviations: cf, commissural furrows; fl, free leaf tips; ls, leaf sheath; pd, pitted diaphragm; vc, vallecular canals. Scale bars 1–3= 5 mm; 4, 6= 10 mm; 5= 1 cm. The leaf whorls are composed of 12–42 (mean=32; to 20 mm in length (Fig. 4.1–6). In many occasions the free n=35) basally fused, linear leaves with acute apices (Fig. apical parts of the leaves are missing due to either tapho- 4.1–2); they are fused for about 75–80% of their total nomic or developmental causes. In some cases, the free length, forming a basal sheath that is slightly expanding leaf tips show a faint central line, possibly indicating the with respect to the node (Fig. 4.3). On the sheaths, indi- presence of a midvein (Fig. 3.1). The lateral margins of the vidual leaves are separated one from another by commis- leaf tips are composed of a thin membrane showing diago- sural furrows that emerge approximately at the level of the nally oriented cells. Overall, the epidermal cellular pattern node and gradually become wider and deeper towards the on the central to upper parts of the leaf sheaths and on the apex, reaching a width of 0.7 mm at the upper sheath mar- free leaf tips differs markedly from that of the stem surface gin. The central region of the commissural furrows consists and the basal leaf-sheath portions because it is composed of a longitudinal row of transversely elongated, rectangular of considerably narrower cells (only c. 15–30 µm wide). cells, 15–30 µm long and 30–100 µm wide (Fig. 3.1). The The stomata are usually sunken and occur in broad bands central region is delimited on each side by an obliquely on both the internodes and leaf sheaths, but are more com- protruding flange composed of diagonally oriented cells c. mon on the latter (Fig. 3.2). Superficial stomata may also 50–70 µm long and 20–40 µm wide. occur scattered or arranged in short vertical rows (Fig. 3.3), The free leaf tips are usually about 1.7–3 mm long (2.4 but this could be a taphonomic arteifact due to the com- on average; n=35), at apical leaf whorls of fertile stems, pression of the stems. Each stomatal apparatus is elliptical however, leaves are much longer, with free tips reaching up in shape and 55–70 µm long and 35–45 µm wide. The 141 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 sunken stomata are particularly evident on impressions and stomata are surrounded by cells that are distinctly smaller casts of the leaf sheaths, where they occur in the form of than the regular epidermal cells, and whose margins appear elliptical lumps on an otherwise uniform, smooth surface. The curved or bent to accommodate the stomatal apparatus. Figure 5. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1. MPEF-Pb 5886; 2. MPEF-Pb 5906; 3. Cartwheel structure of MPEF-Pb 6475; 4. Pitted diaphragm of MPEF-Pb 5900; 5. Transverse view of stem of MPEF-Pb 5940. Abbreviations: cf, commissural furrows; cs, cart-wheel structure; in, internode; ls, leaf sheath; pd, pitted diaphragms; sp, spokes; vc, vallecular canals. Scale bars 1= 10 mm; 2= 3 mm; 3, 5= 2 mm; 4= 1 mm. 142 ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM The stems are hollow and divided at the nodes by trans- Reproductive organs. Strobili are borne terminally and singly verse septa with a complex organization producing two dis- on the apices of fertile stems. Each strobilus is subtended by tinct types of structures, both occurring commonly isolated modified leaf sheaths with free leaf tips that are at least in the sediment or -more rarely- attached to leaf sheaths three times longer (total leaf length c. 20 mm) than those of or to stem sections at the node level. The more common is regular leaf whorls (Fig. 7.2). Strobili are cylindrical to ob- the former of transversal structure (pitted diaphragms= PD), long, 12–19 mm long and 4–7 mm wide, and formed by a which occurs in the form of flat, circular diaphragms with central axis with 7–12 whorls of sporangiophores (Fig. diameters between 2 and 13 mm (mean= 5.95 mm; n= 48). 7.1). The sporangiophores bear 0.6–1 mm large, penta- These consist of a large, flat, circular central portion with to hexagonal distal shields with straight margins. At the numerous, somewhat radially arranged pits (probably cast center of the shield is an umbo 0.3–0.4 mm in diameter, of parenchymatic cells of the pith, Fig. 5.1–2) that is sur- visible on the casts of the sporangiophores, which has the rounded by a peripheral ring with numerous regularly dis- same shape as the shield (Fig. 7.4). The estimated number tributed rectangular to wedge-shaped segments (vallecular of sporangiophores per whorl is 8 to 10. The sporangia are canals), at the outermost periphery these segments merge preserved as impressions, oblong in shape and 0.5–0.7 mm with the axis, forming a thin circular rim (Fig. 5.4). In a few long by 0.12–0.2 mm wide (Fig. 7.3). Spores are unknown. cases, the central portion appears to be surrounded by an additional narrow ring of small circular lumps (partial molds Generic assignment and comparisons of carinal canals) alternating with the position of vallecular Specimens from Cerro Bayo are here assigned to Equi- canals in the outer ring. The second type of structure is setum based on numerous vegetative and reproductive also circular in outline, 2.3–11.5 mm (mean= 5.48; n= 30) features that are virtually identical to the extant represen- in diameter, upwards convex, and resembles a cart-wheel tatives of the genus, i.e., stems comprising nodes and in- (cart-wheel structure= CS) in that it consists of a small cen- ternodes, internal transverse diaphragms occurring at the tral hub, radiating spokes, and a thin peripheral rim (Fig. 5.3). nodes, absence of secondary growth, partially fused leaf The central hub is 0.5–5 mm wide and bears a small, 0.2–1 whorls and strobilar reproductive organs consisting of mm wide hole in its centre. The spokes are about 0.1–0.3 whorled peltate sporangiophores with polygonal shields mm wide, and their length accounts for approximately 1/4 without intercalated bracts. In addition to the broad mor- to 3/4 of the radius of the structure. The central hub and the phological characters mentioned before, the detailed spokes are composed of polygonal, more or less isodia- preservation in Equisetum dimorphum sp. nov. allowed the metric cells 35–75 µm in diameter; toward the periphery of observation of numerous epidermal features that further the spokes, cells appear to become increasingly radially support the generic assignment. For instance, cellular elongated. Where the spokes merge into the peripheral rim, arrangement of commissural furrows in E. dimorphum sp. they dip slightly downward, giving the periphery of the nov. is identical to the one that is present on extant species whole structure a scalloped appearance. of both modern subgenera, e.g., Equisetum diffusum Don, Vegetative shoot apices are commonly terminated by a 1825, Equisetum telmateia Ehrhart, 1783 and Equisetum distinctive structure that resembles a tiny pagoda (Fig. variegatum Schleicher, 1797 (Hauke, 1963, 1978, 1985). In 6.1). These pagoda structures are 3–7 mm tall and 0.7–3 the leaf whorls of living species of Equisetum, the central mm wide, and consist of up to 16 tightly packed whorls cells of the commissural region (C-cells, Hauke, 1985) of minute, reduced, inwardly-curved leaves (Fig. 6.2). Usu- acquire their particular shape beginning with cuboidal cells ally, the basal whorl of these structures is covered by the that undergo successive divisions to attain rectangular and adhering leaf sheaths and apices of the subtending imma- ultimately tangentially elongated shapes, the divisions of ture regular leaf whorls (Fig. 6.1). the C-cells being always transverse (Hauke, 1985). Based Very rarely, stems dichotomize, with a pair of slender “daughter stems” arising from the leaf sheath of the main stem (Fig. 6.3–4). on the morphological similarities the same developmental pattern is here inferred for the fossil species. Equisetum dimorphum sp. nov. is part of a rather small 143 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 and poorly understood group of Equisetum fossils with species of this complex are Equisetum laterale Phillips, 1829, wheel-like nodal structures and divergent free leaf tips that originally described from the Middle Jurassic of Yorkshire appear to be typical elements of mid-Mesozoic floras (see also Harris, 1931, 1961; Gould, 1968), and Equisetites worldwide. Two common and comparatively well-known ferganensis Seward, 1907 from the Jurassic of Kazakhstan, Figure 6. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1. Pagoda structure connected to the stem, MPEF-Pb 5932; 2. Isolated long pagoda structure, MPEF-Pb 6476; 3–4. Dichotomous stems of MPEF-Pb 5930. Abbreviation: pd, pitted diaphragm. Scale bars 1= 4 mm; 2= 2 mm; 3-4= 5 mm. 144 ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM Madagascar, and China (Appert, 1973; Sun et al., 2010). The features, and are distinguished mainly by a characteristic two species are very similar in most of their morphological “arcaded line” that runs perpendicular to the commissural Figure 7. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. 1–2. Part and counterpart of a strobilus showing the hexagonal sporangiophores and the long leaves of MPEF-Pb 5894a and MPEF-Pb 5894b; 3. Detailed inner view of 1 showing oblong sporangia of MPEF-Pb 5894a; 4. Isolated external cast of sporangiophore showing central umbo of MPEF-Pb 6477a. Abbreviations: le, leaves; s, sporangia. Scale bars 1–2= 3mm; 3= 1 mm; 4= 0.5 mm. 145 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 furrows on the leaf sheaths of E. ferganensis (Appert, 1973). of E. dimorphum sp. nov. In addition, some of the stomata These broad and single zigzagging lines extend around present in E. dimorphum sp. nov. occur sunken in broad each individual leaf sheath. Based on a detailed investiga- bands while others appear to be scattered flush within the tion of macro- and micro-morphological features of well- epidermis (a possible taphonomic artefact) or in short ver- preserved E. ferganensis material from the Upper Jurassic of tical rows, whereas those of E. laterale are described as Madagascar, Appert (1973) concluded that, apart from the being scattered and “usually sunken” (Gould, 1968, p. 159), arcaded line mentioned above, E. laterale and E. ferganensis which, in part, agrees with the ones here described. may represent two preservational types of the same natural species. Nonetheless, E. dimorphum sp. nov. also differs from E. laterale and E. ferganensis in several aspects, including pitted Equisetum dimorphum sp. nov., E. laterale and E. ferga- diaphragms (although there is a mention of a single speci- nensis are similar in the following characters: (1) smooth and men of E. laterale from Antarctica showing a diaphragm with unbranched stems, (2) stem and nodal-diaphragm diame- a pitted surface; Rees and Cleal, 2004); notably shorter ters, (3) internode length, (4) presence of cart-wheel struc- mean length of the leaf tips of E. dimorphum sp. nov., usually tures, (5) spreading leaves, (6) cellular organization of the measuring 1.7–3 mm, while those in the other two species epidermis at commissural furrows and internodes, (7) num- are usually between 3–15 mm; presence of pagoda-like ber of spokes of cart-wheel structures, and (8) number of structures; and the presence of long subtending leaves at leaves of E. laterale and E. ferganensis being within the range the base of the strobili (strobili of E. ferganensis are unknown). In addition, fertile specimens of E. laterale described from Australia (Gould, 1968) have smaller strobili than E. dimorphum sp. nov., while those from Antarctica have helically arranged sporangiophores (Rees and Cleal, 2004). Equisetites patagonica (Herbst, 1965) from the Lower Jurassic of Santa Cruz was synonymized with E. laterale (Rees and Cleal, 2004; see also Gould, 1968). The length of the free leaf tips of the Patagonian specimens, however, is similar to that seen in E. dimorphum sp. nov. Other species can also be compared with E. dimorphum sp. nov. on the basis of either vegetative or reproductive features. Equisetites rajmahalensis Oldham and Morris, 1963 from the Upper Jurassic is commonly found in the Rajmahal Formation, India (see Par and Basu, 2007). It shares characters with E. dimorphum sp. nov. including internode length, number of leaves, presence of pitted nodal diaphragms, and sunken stomata. However, pagoda-like structures, epidermal details, cart-wheel and reproductive structures are unknown in the Indian species. Several equisetalean plants from the Mesozoic of Argentina were described in recent years. Equisetites pusillus Villar de Seoane, 2005 from the Lower Cretaceous of Figure 8. Equisetum dimorphum sp. nov. from the Lower Jurassic of Chubut Province, Argentina. Hypothetical reconstruction of the external and internal morphology of a node and partial internodes of a vegetative axis. Abbreviations: cc, carinal canals; cf, commissural furrows; cs, cart-wheel structure; fl, free leaves; ls, leaf sheath; pd, pitted diaphragm; vc, vallecular canals and vascular system (in brown). 146 Santa Cruz differs from E. dimorphum sp. nov. in having, for instance, much smaller stems (up to 3 mm wide) with external longitudinal ridges and furrows, and in having helically arranged, rhomboidal sporangiophores. Equisetites minimus Falaschi, Zamuner and Foix, 2009 from the Upper ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM Jurassic of Santa Cruz differs from E. dimorphum sp. nov. in of strengthening tissue plus an inner lining of turgid having much smaller stems (1.3 mm in diameter) that are parenchyma as in Equisetum giganteum (Spatz et al., 1998), hexagonal in cross secttion, in having fewer leaves per and, in species with small central cavities under low turgor whorl (usually 6), and in having also smaller strobili without pressures, a single continuous layer of endodermis (Spatz long subtending leaves. The anatomically preserved E. ther- and Emmans, 2004). Unfortunately, because the internal male from the Middle Jurassic of Santa Cruz, Argentina anatomy is of E. dimorphum sp. nov. is preserved only in the (Channing et al., 2011), shares with E. dimorphum sp. nov. form of casts, the stability mechanism of the axes remains the presence of superficial stomata (although, as mentioned unknown. We hope that additional material with more com- above, this could be a taphonomic artefact), the arrange- plete structural details of the stems (e.g., with a preserved ment of the epidermal cells in vertical rows, and the gross endodermis pattern) may provide further information on morphology of the strobili. However, numerous features this subject. also differ between the two species: stems of E. thermale Leaf dimorphism. By far the most common foliage type are again considerably smaller than those of E. dimorphum associated with Equisetum dimorphum sp. nov. bears short sp. nov. (with a mean diameter of 1.65 mm), polygonal in free leaf tips of 1.7–3 mm length. A second foliage type, cross section, the internodes bear 6 to 12 longitudinal which occurs very rarely in the same rock samples as the ridges that are equal in number to leaves per whorl. common type, bears free leaf tips that are at least three Finally, Equisetum dimorphum sp. nov. has numerous fea- times longer. We interpret both foliage types as being part tures comparable in general with extant representatives of of the same natural species. Appert (1973) and Gould (1968) the genus, and in particular with Equisetum hyemale Lin- also illustrated similar leaf whorls types for the species naeus, 1753, such as the unbranched stems and the very Equisetites ferganensis and Equisetum laterale, respectively, characteristic pagoda structures (Hauke, 1963). and interpreted them as part of the same natural plant. In these fossil species, however, the longer leaf type occurs DISCUSSION Reconstruction of the Equisetum dimorphum sp. nov. plant more commonly. In Equisetum dimorphum sp. nov. the leaf whorls with long leaf tips occur at the node(s) immediately below the strobilus, as is demonstrated by a specimen in Even though the studied material is preserved in the which the strobilus is organically attached to the stem form of impressions and casts, a type of preservation that is (Fig. 7.1–2). In this specimen, free leaf tips are approxi- generally believed to provide only little paleobiological in- mately the same size as the strobilus. Similar epidermal formation, the large amount and the fine details identified details such as cells organization and size observed in the on the specimens enables a comprehensive reconstruction two types of leaf tips provide further support for this hy- of the E. dimorphum sp. nov. plant. Herein we will discuss pothesis. certain features of E. dimorphum sp. nov. that we consider At present, it remains unknown whether the whorls to be of particular significance for morphological and phylo- bearing long leaves are present only on the node directly genetic interpretations. below a strobilus, or whether they occur throughout fertile Plant height. Equisetum dimorphum sp. nov. was an unbran- stems. ched plant with stems up to 18 mm in diameter. By analogy Nodal anatomy and cart-wheel structures. Two different kinds with extant species, a height of up to 2 meters can be esti- of morphologically distinct structures are observed on mated for the E. dimorphum sp. nov. plants. Upright stems transversal views of the node region in Equisetum dimor- of E. hyemale, with a similar height range as E. dimorphum, phum sp. nov.: the cart-wheel structures (CS) and the pitted sp. nov. gain their mechanical stability due to specific diaphragms (PD). As noted previously, CS also occur in other strengthening features, such as the presence of a double Mesozoic equisetalean species, such as E. laterale (Gould, continuous layer of endodermis (Spatz and Emanns, 2004). 1968; Rees and Cleal, 2004) in which they are convex up- Other features that contribute to the mechanical stability wards and possess scalloped margins. In both cases the of particularly tall equisetalean stems are an outer ring spokes apparently played some role in the vascular system, 147 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 since their number is directly correlated with the number of ganic connection to the rest of the plant, they can be easily leaves at the nodes, and also, as seen in E. laterale, because confused with abortive strobili (Duval-Jouve, 1863). they appear to be connected to the internodal vascular What particular stimulus triggers the formation of these bundles (Gould, 1968: pl. 1; figs. 4, 5). By contrast, PDs are structures is unknown. Duval-Jouve (1863) stated that the flat and circular in shape and bear numerous pits that may pagoda structures do not appear to have a function in the represent pores on the diaphragms, similar to those of plant, and therefore are rather the result of a particular type living Equisetum species (see illustrations in Barber, 1961). of developmental path. Nevertheless, the presence of these We interpret both types of transversal views of the structures has been considered an important diagnostic node being part of the same species mainly because of their character for taxonomic classification (Schaffner 1928, similar size range and their presence on the same slabs, 1930, 1932; Hauke, 1963; Lubienski and Jäger, 2012; Jep- both attached to the same leaf whorls. They do not appear son et al., 2013), since they are known to occur only in E. hye- to represent a continuous variation of the same structure, male and one of its hybrids, both of them contained within since the CS has no continuous range in the length and the subgenus Hippochaete. number of their spokes perhaps leading to a complete re- There are two other fossil species, Equisetum columnare duction, and therefore to morphology similar to the PD type. from the Jurassic of England (Harris, 1961, p. 19) and Equi- The most likely explanation for the presence of two setites quindecimdentata from the Triassic of Argentina different transversal structures in the stems of a single (Menendez, 1958) that bear organs morphologically similar species is that the CS were contained within the more deli- to pagoda-like structures. However, in both cases these cate, possibly parenchymatic tissue that is preserved in the structures were not interpreted as such, and therefore fur- form of the PD. One specimen that provides some support ther investigation on these species is needed in order to for this hypothesis shows an oblique section of a node with confirm their homology with the ones in E. hyemale and E. part of a CS partially covered by a PD (Fig. 5.5). The inter- dimorphum sp. nov. pretation, originally suggested by Gould (1968, p. 160; fig. The possibility that pagoda apices were in fact located 2A–B), may be further supported by the occurrence of occa- at the tip of underground rhizomes cannot be completely sional pitted diaphragms in association with cart-wheel discarded, but seems implausible since the acroscopic structures in E. laterale from Australia (Gould, 1968) and orientation of the leaf tips below the pagoda would not be Antarctica (Rees and Cleal, 2004). possible on a growing underground rhizome because the Pagoda structures. The pagoda structures of Equisetum di- leaves that are outwardly oriented could not maintain that morphum sp. nov. are remarkably similar to those commonly orientation without bending backwards when the rhizome occurring on the shoot apices of extant E. hyemale and Equi- is horizontally growing through the ground. setum x ascendens, a hybrid of the former species (see Stem dichotomies. Two dichotomous stems (Fig. 6.3–4) have Schaffner, 1932; Lubienski and Jäger, 2012). In extant been found among the specimens of E. dimorphum sp. nov. species, pagoda structures arise during the development of Based on their close proximity on the same rock sample, we the stems, with the successive abscission of the partially infer that they belonged to the same individual plant. In fused leaves that are in contact and contained one below one of the specimens it is possible to observe that the another in the growing stem. The free part of the leaves internodal length of the first internode after the split, on wither away or are torn apart from their sheath with the each stem, is the same. Extant horsetails, including E. hye- elongation of the succeeding internode, and thus carried up- male, occasionally present this abnormal character of di- wards to the apex. In this way, the apical leaf whorl of the chotomizing stems as well (Schaffner, 1933). pagoda derives from a lower leaf sheath than the one located below, and so it is reflecting a stacking order opposite Systematic considerations to the order that the leaf whorls were produced on the stem Character evolution. Detailed reconstruction of E. dimorphum (Duval-Jouve, 1863; Page, 1997). It is interesting to note sp. nov. provides relevant information in terms of the possi- that when the pagoda structures are found without an or- ble early configuration, and therefore evolution, of several 148 ELGORRIAGA ET AL.: A NEW JURASSIC EQUISETUM morphological characters. For instance, the presence of The apical pagoda-like structure, as seen in E. hyemale longer leaf tips in the proximal nodes of the strobili has and its hybrids, which is believed to be an apomorphic been also mentioned for the extant Equisetum pratense character for Equisetum, may actually represent a plesio- Ehrhart, 1784 and Equisetum sylvaticum Linnaeus, 1753 morphic condition for the genus. Nonetheless, the presence (Hauke, 1978). However, the difference in leaf length of re- of leaf whorls subtending the pagoda structure in E. dimor- productive and vegetative whorls in the latter is not as pro- phum sp. nov. might be interpreted as a different develop- nounced as it is in E. dimorphum sp. nov., perhaps suggesting mental scenario, suggesting that further analyses will be a progressive reduction in this character that is completed necessary to confirm its homology with respect to extant in other extant species. One of the theories concerning the species. origin of Equisetum postulates the genus Neocalamites, Equisetum dimorphum sp. nov. in the context of extant sub- which bears whorls of free long leaves, as its sister group genera. The two modern Equisetum subgenera -Equisetum (Stewart and Rothwell, 1993). This hypothesis clearly and Hippochaete- have been historically distinguished based implies that fusion in equisetalean leaf whorls happened on numerous morphological features (Hauke, 1963, 1978; several times in the evolution of the group, and that the Des Marais et al., 2003). However, their morphological morphologically similar leaf sheaths of Equisetum and, for differentiation has been recently questioned on the basis of instance, the late Paleozoic to mid-Mesozoic Phyllotheca molecular phylogenetic inferences (Des Marais et al., 2003; Brongniart, 1828, would not be homologous. An alternative Guillon, 2004, 2007). In these studies, Equisetum bogotense, evolutionary scenario considers the increasing number of a species classically assigned to the subgenus Equisetum herbaceous equisetalean plants described from Gondwana based on morphological features, has been recovered as and Angara (Naugolnykh, 2002, 2004; Escapa and Cúneo, basal to subgenus Hippochaete (Guillon, 2007) or sister to 2005; Cúneo and Escapa, 2006) as possibly closely related both subgenera (Des Marais et al., 2003; Guillon, 2004). This to Equisetum. This is supported by the presence of basally would indicate that morphological character states present fused leaves, together with numerous shared characters in in E. bogotense and species from the Equisetum subgenus their reproductive organs. represent the plesiomorphic conditions in the evolution of TABLE 1 - Morphological characters of Equisetum subgenera and E. dimorphum sp. nov. aerial stems Character Equisetum Hippochaete Equisetum dimorphum sp. nov. Position of stomata Superficial, scattered or in bands Sunken, in single or double lines Sunken in bands/ Superficial Strobili Non-apiculate Usually apiculate Non-apiculate Branching pattern In regular whorls* Regular/Irregular/Absent Irregular/Absent Aerial stem dimorphism Monomorphic/ Dimorphic/ Semi-dimorphic Monomorphic Dimorphic/Semi- dimorphic Free leaf tips Persistent Persistent/Break off/Wither Persistent/Break off Pagoda structure Absent Present (E. hyemale) Present Habit Annual Perennial ? Stem endodermis pattern Single common external Single common external/ Double/Surrounding each bundle ? Micro-relief and surface sculpturing Mamillae and pilulae very numerous Mamillae and pilulae sparse or absent ? * Except in E. fluvatile where unbranched stems are frequently found and occasionally E. palustre. 149 AMEGHINIANA - 2015 - Volume 52 (1): 135 – 152 the genus (see Guillon, 2007). Nonetheless, the fossil REFERENCES record indicates that modern representatives of Equisetum Appert, O. 1973. [Les Ptéridophytes du Jurassique supérieur du massif Manamana au sud-ouest de Madagascar. Universite de Paris VI, Paris, 72 p. Unpublished.]. Barber, D. 1961. Gas exchange between Equisetum limosum and its environment. Journal of Experimental Botany 12: 243–251. Behrensmeyer, A.K., Damuth, J.D., DiMichele, W.A., Potts, R., Sues, H.D., and Wing, S.L. 1992. Terrestrial ecosystems through time: evolutionary paleoecology of terrestrial plants and animals. University of Chicago Press, Chicago, 588 p. Bercovici, A., Hadley, A., and Villanueva-Amadoz, U. 2009. Improving depth of field resolution for palynological photomicrography. Palaeontologia Electronica 12: 1–12. Bierhorst, D.W. 1971. Morphology of vascular plants. Macmillan Inc., New York, 560 p. Bomfleur, B., Escapa, I.H., Serbet, R., Taylor, E.L., and Taylor, T.N. 2013. 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The specimens here described are characterized by a combination of features present in representatives of both extant Equisetum subgenera (see Tab. 1). Similar situations are corroborated for other Mesozoic species such as E. thermale (Channing et al., 2011), Equisetum haukeanum Stanich, Rothwell and Stockey 2009 and Equisetum vancouverense Stanich, Rothwell and Stockey 2009. It is interesting to note that, when Mesozoic fossils are considered, several morphological features generally assumed as synapomorphies for particular living groups are better explained as plesiomorphic conditions (e.g., endodermis pattern). On these grounds, the affiliation of E. dimorphum sp. nov. to one of the two living subgenera is discounted. In addition, the fact that E. dimorphum sp. nov. shares some distinctive anatomical characters (e.g., cart-wheel structures) with some other Jurassic species such as E. laterale and E. ferganensis –both of them present in Gondwana and Laurasia (Harris, 1961; Gould, 1968; Appert, 1973; Sun et al., 2010)– might indicate the presence of an unidentified subgenus that would include several widely distributed species during the Jurassic. A comprehensive phylogenetic analysis integrating extinct and extant forms will be instrumental in order to test this hypothesis, and to identify character polarity in the representatives of the horsetail lineage. ACKNOWLEDGMENTS We cordially thank Wim de Winter for providing images of pagoda structures on Equisetum hyemale. We further thank A. M. Zavattieri, J. Bodnar, J. Dobrandi, C. Monje Dussan, J. Parra, D. Olivera and M. Caffa for their help with the field work season. Don J. 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