Morphology of the megaspore Lagenoisporites magnus (Chi and Hills 1976) Candilier et al. (1982), from the Carboniferous (lower Mississippian: mid-upper Tournaisian) of Bolivia

Abstract

Abstract: The morphology and structure of megaspores assigned to Lagenoisporites magnus from the Toregua Formation, Retama Group, mid-upper Tournaisian of Bolivia were studied. The analysis was performed with light, fluorescence and scanning electron microscopy. Megaspores were laterally compressed and presented a spherical body with a proximal gula, of the hologula type. Gula had verrucae ornamentation and the spore body presented complex processes consisting of a bulbous base and an internally partitioned projection with sharp apex. In addition to this main ornamentation, perforations were present throughout the spore surface. Megaspores showed well marked curvaturae perfectae due to the abrupt transition existing between the gula ornamentation and the spore body processes. These megaspores were assigned to heterosporous arborescent lycopsids of the Lepidocarpaceae family, as in section view, exospore structure presented a three-dimensional network of fused elements. Likewise, due to a similarity found between sporoderm and Isoetes L. structure, it is evident that megaspores structure has remained intact inside the heterosporous lycopsids. Therefore; the L. magnus structure not only would confirm its affinity with the Lycophyta fossils but also with the living ones.

Key words
Bolivia; Carboniferous; lycopsids; megaspores; Tournaisian

INTRODUCTION

Heterospory is one of the most important innovations in the history of plants since the Devonian (Traverse 2007). Heterospory earliest megafossil evidence is represented by Chaleuria cirrosaAndrews et al. from the Emsian (Andrews et al. 1974), whereas, in the fossil record of dispersed spores, megaspores are known from the Pragian-Emsian (McGregor and Camfield 1976, Richardson and McGregor 1986). From the Emsian and throughout the Devonian, it is observed an increase in megaspores diversity (Scott and Hemsley 1996), but it is in the Carboniferous that a remarkable rise has been recorded (Braman and Hills 1980).

Compared to Pennsylvanian epoch, there is still limited information available about dispersed megaspores from the Mississippian due to a paucity of described assemblages (Scott and Hemsley 1996, Arioli et al. 2007, Wellman et al. 2009). There are few publications on Tournaisian megaspores from different regions of the world (e.g., Chaloner 1954, Winslow 1962, Alvin 1966, Mortimer et al. 1970, Allen and Robson 1981, Hills et al. 1984, Scott and Meyer-Berthaud 1985, Hemsley et al. 1994, Glasspool et al. 2000).

Taking into consideration Tournaisian assemblages, two groups of megaspores can be differentiated: (1) those linked to the Upper Devonian, dominated by small forms characterized by the presence of grapnel-tipped processes (e.g., Allen and Robson 1981, Candilier et al. 1982, Higgs and Scott 1982), and (2) those linked to the Pennsylvanian, dominated by larger forms (Arioli et al. 2007, Wellman et al. 2009). It is in this second group that the gulate megaspores, which are characterized by having a well-developed apical prominence or gula are found.

Megaspores presenting gula have been studied by certain authors (e.g., Dybová-Jachowicz et al. 1979, 1982, 1984, 1987, Candilier et al. 1982, Archangelsky et al. 1989, Cúneo et al. 1991, Ricardi-Branco et al. 2002, Arioli et al. 2007, Wellman et al. 2009, Steemans et al. 2011) and even principles for their classification have been proposed (Dybová-Jachowicz et al. 1979). There are several genus within the gulate megaspores, Infraturma Gulati (Bhardwaj 1957), such as Lagenicula and Lagenoisporites, which have been well documented and studied at an ultrastructural level. However, only a few species from Upper Devonian-Mississippian have been fully studied (e.g., Glasspool et al. 2000, Arioli et al. 2007, Wellman et al. 2009), as most of them either have only been briefly described (e.g., Candilier et al. 1982), or have been focused on Pennsylvanian species (e.g., Thomas and Blackburn 1987, Scott and Hemsley 1993).

The aim of this work is to study northern Bolivia Lagenoisporites magnus mid- upper Tournaisian gulate megaspore morphology and; to achieve this, optical, fluorescence, and scanning electron microscopy were used. This study on Mississippian megaspore diversity was carried out to contribute with information that was not available, especially because no research on megaspores for this region and time period has ever been made.

MATERIALS AND METHODS

SAMPLES PROVENANCE

Megaspores were recovered in palynological samples from Pando X-1 (11º 36’ 07’’ S, 67º 56’ 45’’ W) and Manuripi X-1 wells (11º 36’ 01’’ S, 68º 08’ 55’’ W), Madre de Dios Basin, Bolivia (Fig. 1). Both boreholes were drilled in 1991 by Mobil Boliviana de Petroleos Inc. and Occidental Boliviana Inc., as continuous crowns from the Devonian/Silurian to the Pennsylvanian. Geological information- including descriptions of wells and palynological and chronological results- has been previously published (Isaacson et al. 1995, Vavrdová et al. 1996, Vavrdová and Isaacson 1996, di Pasquo 2009, 2015, di Pasquo et al. 2015, 2016, Quetglas et al. 2017).

Figure 1
- Map of the study area and boreholes location: 1- Pando X-1 (11º 36’ 07’’ S, 67º 56’ 45’’ W) and 2- Manuripi X-1 (11º 36’ 01’’ S, 68º 08’ 55’’ W).

The studied material consisted of 12 samples obtained between 1360 and 1240 m depth from the Pando X-1 well (CICYTTP 734, 731 and 729) and between 1535 and 1483 m depth from the Manuripi X-1 well (CICYTTP 580, 579, 578, 577, 576, 575, 574, 573 and 572), corresponding to the Toregua Formation (di Pasquo 2015). It is considered that these deposits have been influenced by marine-glacial and deltaic sedimentation (Isaacson and Díaz Martínez 1995). Palynological assemblages that contained the studied megaspores were similar in their composition and preservation in both boreholes (di Pasquo 2015). The presence of dispersed miospores such as Vallatisporites ciliaris, Granulatisporites granulatus, Reticulatisporites waloweekii, Dibolisporites setigerus, Crassispora scrupulosa and Cristatisporites echinatus, indicated a mid-upper Tournaisian age (di Pasquo 2015, di Pasquo et al. 2015).

PREPARATION AND TECHNIQUES

In order to prevent megaspores destruction, samples were exposed to a ‘gentler’ laboratory treatment (see Steemans et al. 2009). For each sample, 20-30 g of sediment were crushed in sizes greater than 5 mm and macerated using 30% HCl for 8 hours followed by 45% HF for 48 hours. To eliminate the acid from the samples (neutralization) several washes with distilled water were carried out. Then, residues were sieved using a 25 µm mesh. Megaspores were picked directly from the residue under a stereoscopic microscope and mounted on glass slides for light microscope (LM) observation as well as with fluorescence. Those megaspores that presented, either ornamentation that could not be determined with LM, or fractures in their wall were selected for a more detailed study with fluorescence and scanning electron microscopy (SEM). For SEM observation, megaspores were mounted with glue on stubs. Two types of microscopes were used, a JEOL JSM 6360 LV from Facultad de Ciencias Naturales y Museo (UNLP) - in this case samples were coated with gold - and a JENCK PHENOM PRO from Centro de Investigaciones Científicas y Transferencia de Tecnología (CONICET-Entre Ríos-UADER) - in this case samples did not require to be coated.

Megaspores size was obtained from the measurements made with LM and through the program ImageJ version IJ 1.46r (Ferreira and Rasband 2012). The maximum and minimum values were expressed in micrometers (µm).

In this contribution, it was followed Paleozoic megaspores classification (Potonié 1893, Dybová-Jachowicz et al. 1979) and it was used Dybová-Jachowicz et al. (1979) and Punt et al. (2007) terminology.

Examined specimens are placed in the Laboratorio de Palinoestratigrafía y Paleobotánica (CICYTTP-CONICET-Entre Ríos-UADER) under the acronyms CICYTTP-M for the megaspores (di Pasquo and Silvestri 2014). The catalogue numbers are as follows: CICYTTP-M112, 119, 122, 129, 130, 136, 139, 140, 141, 144, 151, 152, 162, 163, 380 and 428.

RESULTS

Anteturma SPORITES Potonié 1893

Turma TRILETES (Reinsch 1881) Potonié and Kremp 1954

Subturma LAGENOTRILETES Potonié and Kremp 1954 emend. Bhardwaj 1957

Infraturma GULATI Bhardwaj 1957

Genus LAGENOISPORITES (Potonié and Kremp 1954) Dybová-Jachowicz et al. 1979

Lagenoisporites magnus (Chi and Hills 1976) Candilier et al. 1982

Figures 2-4.

DESCRIPTION

The 16 Lagenoisporites magnus specimens examined were laterally compressed and presented a spherical body (distal surface) with a gula (proximal surface) of the hologula type (Fig. 2a-f). The contact areas were limited proximally by the laesurae and distally by the curvaturae perfectae, a curved line joining the laesurae ends (Fig. 2e-f). The overall length (including gula) ranged from 290-510 µm and the width of the body ranged from 184-390 µm, according to the equatorial axis.

Figure 2
- Lagenoisporites magnus megaspores compressed laterally where the main body, the gula and the curvaturae perfectae can be distinguished. a-e. Megaspores observed with light microscope (LM). a: Specimen CICYTTP-M 139. b: Specimen CICYTTP-M 140. c: Specimen CICYTTP-M 144. d: Specimen CICYTTP-M 151. e: Specimen CICYTTP-M 162. f. Megaspores observed with scanning electron microscope (SEM). Specimen CICYTTP-M 162. Scale bar: 100 μm.

The gula ranged from 80-280 µm in height and from 85-332 µm in width in its base. The gula had a verrucae ornamentation which was 2-7 µm tall (Fig. 3a-b) being either separated from each other or laterally fused. It was only present in contact areas and absent in laesurae lips (Fig. 3b).

Figure 3
- Lagenoisporites magnus. Surface details. a-f. a: Specimen CICYTTP-M 380. Verrucae of the gula (LM). Scale bar: 40 μm. b: Specimen CICYTTP-M 162. Ornamentation of verrucae and laesurae lips (arrow) of the gula (SEM). Note that some verrucae are fused together (star). Scale bar: 20 μm. c: Specimen CICYTTP-M 162. Detail of the complex processes of the spore body, formed by a bulbous base and an internally partitioned projection (arrow) with sharp apex (LM). Scale bar: 20 μm. d: Specimen CICYTTP-M 428. Complex processes of the spore body and detail of the curvaturae perfectae surface (arrow; SEM). Scale bar: 20 μm. e: Specimen CICYTTP-M 144. Complex processes of the spore body and detail of the curvaturae perfectae surface (arrow) observed with fluorescence LM. Scale bar: 20 μm. f: Specimen CICYTTP-M 162. Detail of the spore body surface that shows perforations (arrow; SEM). Scale bar: 2 μm.

The megaspore body surface was covered by complex processes formed by a 5-9 µm diameter bulbous base with a spheroid outline and an internally partitioned projection with an acute apex, which was generally curved like a hook (Fig. 3c-e). These processes were 5-19 µm tall and 4-7 µm width. Ornamentation distribution varied from one specimen to another. Specimens that presented dense ornamentation throughout their megaspore body surface usually had their process basal parts fused together. Other specimens presented a denser ornamentation near the curvaturae perfectae area, which was well marked by the abrupt transition existing between the gula ornamentation verrucae and the main body complex processes. Likewise, in this area, ornamentation constituted a well-differentiated ‘necklace’ formed by complex processes fused together in their base (Fig. 3d-e).

Megaspore gula and the body surface showed perforations of different sizes (Fig. 3f). These perforations did not affect the ornamentation bases and were not present in the laesurae lips.

It was after observing a fracture in one gula specimen (CICYTTP-M 136; Fig. 4a-b) that the exospore outermost layer could be identified. This layer presented a spongy structure formed by a three-dimensional network of fused rodlets, which were circular in section delimiting heterogeneous spaces (Fig. 4c-d). These anastomosed rodlets were arranged in different levels having diverse orientations. Rodlets ranged from 0.2-0.4 µm width.

Figure 4
- Lagenoisporites magnus. Detail of the megaspore fracture observed with SEM. a-d. Specimen CICYTTP-M 136. a: Megaspores compressed laterally with a fracture in the gula. Scale bar: 50 μm. b: Detail of the megaspore fracture. Scale bar: 20 μm. c: Detail of the gula exospore. d: Detail of the exospore which consists of fused rodlets that form a three-dimensional network with heterogeneous spaces of diverse diameters and are arranged at different levels with dissimilar orientations. Scale bar: 5 μm.

DISCUSSION

COMPARISONS AND LYCOPSID BOTANICAL AFFINITY

Lagenoisporites magnus specimens recovered from Toregua Formation, Bolivia, had a similar morphology and wall structure to those described by Chi and Hills (1976) and Candilier et al. (1982). We observed that L. magnus presented an ornamentation formed by verrucae in the gula and by complex processes in the rest of the megaspore body. However, some differences in the ornamentation distribution and in the sculptural elements dimensions were observed (see below). According to Chi and Hills (1976) verrucae are present throughout the megaspore surface, however, they do not mention the presence of spines on the bulbous bases of the body. Candilier et al. (1982) found differences between the gula and the megaspore body ornamentation, whereas the gula presents verrucae, the spore body presents bulbous elements with an acute apex. Although the latter were of a relatively smaller size than those described in this work; they did coincide with the sizes described by Chi and Hills (1976). Size differences and ornamentation distribution in L. magnus could be considered an intraspecific variation- this circumstance had already been described for Lagenicula species (Wellman et al. 2009).

Arioli et al. (2007) described similar sculptural elements for Lagenicula variabilis (Winslow 1962) Arioli et al. (2004), from the Lower Carboniferous of Ohio, USA. According to these authors, L. variabilis presents an ornamentation consisting of large spines with wide bulbous bases. Although L. magnus had a similar ornamentation, the difference in size was important as L. variabilis measured 45-180 µm high (Arioli et al. 2007) while L. magnus did not exceed 20 µm high. These small size processes constitute a diagnostic character of the Lagenoisporites genus (Dybová-Jachowicz et al. 1979). In addition, L. variabilis spine processes may bifurcate or even trifurcate (Arioli et al. 2007), whereas L. magnus spines did not divide, being always discrete. As for the gula ornamentation, Lagenicula variabilis bears verrucae, cones or spines that in several specimens may bifurcate or trifurcate (Arioli et al. 2007), whereas in L. magnus only verrucae were observed. Verrucae presence in the gula was frequently found within the gulate megaspores. However, the body ornamentation described for L. magnus, has not been found in other known gulate megaspores.

Megaspores surface perforations could be determined by the three-dimensional structure of the exospore, as it was previously explained by Wellman et al. (2009). The same characteristic was observed in Lagenicula acuminataDijkstra and Piérart 1957 (Glasspool et al. 2000), Lagenicula variabilis (Arioli et al. 2007) and Lagenicula mixta Winslow 1962 (Wellman et al. 2009).

According to Glasspool et al. (2000), as far as gulate megaspores ultrastructure is concerned, the exospore is divided into an outer, an intermediate, an inner layer and a basal lamina, whereas for Arioli et al. (2007) and Wellman et al. (2009), the exospore presents an outer and an inner layer. In L. magnus, exospore outermost layer was only observed, which was composed of a three-dimensional network of fused rodlets giving it a spongy structure appearance. Thus, this wall structure demonstrated the close phylogenetic relationship that exists with the rest of the Carboniferous gulate megaspores, which allowed us to assign them to heterosporous arborescent lycopsids of Lepidocarpaceae family (Arioli et al. 2007).

BRIEF APPROACHES ON THE EVOLUTION OF GULATE MEGASPORES

Heterospory has evolved once inside the lycopsids (Bateman and Di Michele 1994). The monophyletic heterosporous lycopsids group could have inherited the mode of megaspore wall formation, which evolved from a simple modification of the basic development process in the homosporous lycopsids (Arioli et al. 2007). This megaspore wall formation mode and; therefore, its ultrastructure, persisted relatively without changes in the heterosporous lycopsids and this condition can be determined by the lack of diversity in megaspores ultrastructure, from gulate megaspores up to the living ones (Wellman et al. 2009). Extensive researches made on extant and fossils lycopsids megaspores strongly suggest stasis in wall structure (Arioli et al. 2007, Tryon 1986). According to Arioli et al. (2007), stasis is only present in the Selaginellaceae Willk. However, stasis has been indicated in the Isoetaceae Reichenb in relation to the inner portion of the spore wall, which presents stable structural components in contrast to the outermost portion which would present a variable structure with the ability to differentiate in response to external factors, representing adaptations to special environmental conditions (Tryon 1986).

Numerous fossil megaspores assigned to lycopsids present similarities in their ultrastructure with the Isoetales (Wellman 2002). This is the case of L. magnus in which a spongy exospore coincident with the general scheme described by Lugardon et al. (2000) for extant lycopsids was observed. In addition, it was recognized a structural setup of sporoderm elements similar to those described in extant species of Isoetes L, which present a three-dimensional network of fused rodlets forming heterogeneous spaces (Macluf et al. 2003). Tryon (1986) proposal on stasis in megaspore wall structure is hereby clearly evidenced. Finally, the exospore of L. magnus and the exospore of extant Isoetales were very similar, evidencing that megaspore structure has remained stable over the time.

CONCLUSIONS

This study on Lagenoisporites magnus was carried out to contribute with information about lower Mississippian (Tournaisian) megaspores from Bolivia, especially because no research on megaspores for this region and time period has ever been made. In addition, L. magnus have only been briefly described (Chi and Hills 1976, Candilier et al. 1982), where no descriptions at wall structural level have been done, in contrast with a few species from Upper Devonian- lower Mississippian that have been fully studied (e.g., Glasspool et al. 2000, Arioli et al. 2007, Wellman et al. 2009). Nevertheless, the excellent preservation and the amount of specimens recovered of this species, plus the combination of optical, fluorescence and scanning electron microscopy, allowed us a thorough and detailed study not only of the ornamentation but also of that considered as background, distributed among the main sculptural elements and represented by perforations. This also allowed us to know the sporoderm internal structure, more specifically of the exospore, which was formed by a three-dimensional network of fused rodlets, similar to the ultrastructure described in extant species of Isoetes (Lycophyta).

The morphology and structure of the megaspore studied has allowed to assign it to the Lepidocarpaceae and to determine its botanical affinity with extant lycopsids. Likewise, it has been possible to corroborate the conservative nature of the megaspore wall structure by comparing fossil and extant lycopsids ultrastructure.

Future additional studies using transmission electron microscopy will allow us to deepen the wall ultrastructure to obtain more information about its phylogenetic relationship with the extant lycopsids

ACKNOWLEGMENTS

This study is part of a Ph.D. thesis in development. The authors deeply thank Dra. Marta Morbelli for her valuable contributions, Dr. Di Pietro for reading a preliminary version and two anonymous reviewers whose comments and suggestions have improved the manuscript. The authors also thank Leonardo Silvestri for his assistance in the lab processing, and Patricia Sarmiento of the SEM Unit of the Museo de Ciencias Naturales de La Plata and MSc. Ing. José Félix Vilá of the SEM Unit of CICYTTP-CONICET-ER-UADER in Diamante, for their good predisposition when taking photomicrographs. This work was supported by grants from the Consejo de Investigaciones Científicas y Técnicas (CONICET-PIP 0812) and from the Universidad Nacional de La Plata (UNLPPPID N028).

REFERENCES

• ALLEN KC and ROBSON J. 1981. Megaspores with multifurcate and bifurcate processes from Old Red Sandstone facies of Tournaisian age, from the Taff Gorge, South Glamorgan, Wales. New Phytol 88: 387-397.
• ALVIN KL. 1966. Two cristate megaspores from the Lower Carboniferous of Scotland. Palaeontology 9: 488-491.
• ANDREWS HN, GENSEL PG and FORBES WH. 1974. An apparently heterosporous plant from the Middle Devonian of New Brunswick. Palaeontology 17: 387-408.
• ARCHANGELSKY S, CÚNEO R and VILLAR DE SEOANE L. 1989. Estudios sobre megasporas pérmicas argentinas. I. Sublagenicula brasiliensis (Dijkstra) Dybová-Jachowicz et al. Ameghiniana 26: 209-217.
• ARIOLI C, SERVAIS T and WELLMAN CH. 2004. Morphology and ultrastructure of a Lower Carboniferous megaspore: Lagenicula variabilis (Winslow 1962) nov. comb. Ann Soc Géol Nord 11: 109-111.
• ARIOLI C, WELLMAN CH, LUGARDON B and SERVAIS T. 2007. Morphology and wall ultrastructure of the megaspore Lagenicula (Triletes) variabilis (Winslow 1962) Arioli et al. (2004) from the Lower Carboniferous of Ohio, USA. Rev Palaeobot Palynol 144: 231-248.
• BATEMAN RM and DIMICHELE WA. 1994. Heterospory: the most iterative key innovation in the evolutionary history of the plant kingdom. Biol Rev 69: 345-417.
• BHARDWAJ CD. 1957. The spore flora of Velener Schichten (Lower Westphalian D) in the Ruhrcoal measures. Palaeontogr Abt B 102: 110-138.
• BRAMAN DR and HILLS LV. 1980. The stratigraphic and geographic distribution of carboniferous megaspores. Palynology 4: 23-41.
• CANDILIER AM, COQUEL R and LOBOZIAK S. 1982. Mégaspores du Dévonien terminal et du Carbonifère inférieur des Bassins d’Illizi (Sahara algérien) et de Rhadames (Libyé occidentale). Palaeontogr Abt B 183: 83-107.
• CHALONER WG. 1954. Mississippian megaspores from Michigan and adjacent states. Contrib Mus Palaeontol Univ Mich 12: 23-34.
• CHI BI and HILLS LV. 1976. Biostratigraphy and taxonomy of Devonian megaspores, Artic, Canada. Bull Can Petrol 24: 641-817.
• CÚNEO R, VILLAR DE SEOANE L and ARCHANGELSKY S. 1991. Estudios sobre megasporas pérmicas argentinas. II. Sublagenicula nuda y S. brasiliensis de la Cuenca Chacoparanense, Argentina. Ameghiniana 28: 55-62.1.
• DIJKSTRA SJ and PIÉRART P. 1957. Lower Carboniferous megaspores from the Moscow Basin. Med Geol Sticht, Nieuwe Ser 11: 5-19.
• DI PASQUO M. 2009. The Pennsylvanian palynoflora of the Pando X-1 Borehole, northern Bolivia. Rev Palaeobot Palynol 157: 266-284.
• DI PASQUO M. 2015. First record of Lagenicula mixta (Winslow) Wellman et al. in Bolivia: biostratigraphic and paleobiogeographic significance. Ameghiniana 52: 41.
• DI PASQUO M, ISAACSON PE, GRADER GW, HAMILTON MA and SOREGHAN GS. 2016. Palynostratigraphy of the Yaurichambi and Copacabana formations in the Manuripi X-1 core, Madre de Dios Basin, northern Bolivia: First constraints from U-Pb dating of volcanic ash. Bol de la ALPP 16: 110.
• DI PASQUO M and SILVESTRI L. 2014. Las colecciones de Palinología y Paleobotánica del Laboratorio de Palinoestratigrafía y Paleobotánica del Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción (CICYTTP), Entre Ríos, Argentina. Contribuição à RESCEPP “Rede Sul-americana de Coleções e Ensino em Paleobotânica e Palinologia”. Bol de la ALPP 14: 39-47.
• DI PASQUO M, WOOD G, ISAACSON P and GRADER G. 2015. Palynostratigraphic reevaluation of the Manuripi-x1 (1541-1150 m interval), Madre de Dios basin, northern Bolivia: recycled Devonian species and their implication for the timing and duration of Gondwanan glaciation. Ameghiniana 52: 23.
• DYBOVÁ-JACHOWICZ S, JACHOWICZ A, KARCZEWSKA J, LACHKAR G, LOBOZIAK S, PIÉRART P, TURNAU E and ZOLDANI Z. 1979. Note Préliminaire sur la révision des mégaspores à gula du Carbonifére; les principles de la classification. Acta Palaeontol Pol 24: 411-422.
• DYBOVÁ-JACHOWICZ S, JACHOWICZ A, KARCZEWSKA J, LACHKAR G, LOBOZIAK S, PIÉRART P, TURNAU E and ZOLDANI Z. 1982. Révision des mégaspores à gula du Carbonifére. (Première partie). Pr Inst Geol 107: 1-44.
• DYBOVÁ-JACHOWICZ S, JACHOWICZ A, KARCZEWSKA J, LACHKAR G, LOBOZIAK S, PIÉRART P, TURNAU E and ZOLDANI Z. 1984. Révision des mégaspores à gula du Carbonifére. (Deuxième partie). Pr Inst Geol 115: 1-31.
• DYBOVÁ-JACHOWICZ S, JACHOWICZ A, KARCZEWSKA J, LACHKAR G, LOBOZIAK S, PIÉRART P, TURNAU E and ZOLDANI Z. 1987. Revision of Carboniferous megaspores with gula. Part Three. Pr Inst Geol 121: 1-49.
• FERREIRA T and RASBAND WS. 2012. ImageJ User Guide. Version IJ 1.46r. Available from: https://imagej.nih.gov/ij/docs/guide/
  » https://imagej.nih.gov/ij/docs/guide/
• GLASSPOOL IJ, HEMSLEY AR, SCOTT AC and GOLITSYN A. 2000. Ultrastructure and affinity of Lower Carboniferous megaspores from the Moscow Basin, Russia. Rev Palaeobot Palynol 109: 1-31.
• HEMSLEY AR, CLAYTON G and GALTIER J. 1994. Further studies on a late Tournaisian (Lower Carboniferous) flora from Loch Humphrey Burn, Scotland; spore taxonomy and ultrastructure. Rev Palaeobot Palynol 81: 213-231.
• HIGGS K and SCOTT AC. 1982. Megaspores from the uppermost Devonian (Strunian) of Hook Head, County Wexford, Ireland. Palaeontogr Abt B 181: 79-108.
• HILLS LV, HYSLOP K, BRAMAN DR and LLOYD S. 1984. Megaspores from the Tuttle Formation (Famennian-Tournaisian) of the Yukon, Canada. Palynology 8: 211-224.
• ISAACSON PE and DÍAZ MARTÍNEZ E. 1995. Evidence for Middle-Late Paleozoic foreland basin and significance paleolatitudinal shift, Central Andes. In: Tankard AJ et al. (Eds), Petroleum Basins of South America, Tulsa: AAPG Memoir 62, p. 231-249.
• ISAACSON PE, PALMER BP, MAMET B, COOKE JC and SANDERS DE. 1995. Devonian-Carboniferous stratigraphy in the Madre de Dios Basin, Bolivia: Pando X-1 and Manuripi X-1 Wells. In: Tankard AJ et al. (Eds), Petroleum Basins of South America, Tulsa: AAPG Memoir 62, p. 501-509.
• LUGARDON B, GRAUVOGEL-STAMM L and DOBRUSKINA I. 2000. Comparative ultrastructure of the megaspores of the Triassic lycopsid Pleuromeia rossica Neuburg. C R Acad Sci, Ser IIa: Sci Terre Planets 330: 501-508.
• MACLUF CC, MORBELLI MA and GIUDICE GE. 2003. Morphology and ultrastructure of megaspores and microspores of Isoetes savatieri Franchet (Lycophyta). Rev Palaeobot Palynol 126: 197-209.
• MCGREGOR DC and CAMFIELD M. 1976. Upper Silurian? to Middle Devonian spores of the Moose River Basin, Ontario. Geol Surv Canada, Bull 263: 1-63.
• MORTIMER G, CHALONER WG and LLEWELLYN PG. 1970. Lower Carboniferous (Tournaisian) miospores and megaspores from Breedon Cloud Quarry, Leicestershire. Mercian Geol 3: 375-385.
• POTONIE H. 1893. Die Flora des Rothliegenden von Thüringen. Kgl Preuss Geol L-A 9: 1-298.
• POTONIE R and KREMP G. 1954. Die Gattungen der palaozoischen Sporae dispersae und ihre Stratigraphie. Geol Jahrb 69: 111-193.
• PUNT A, HOEN PP, BLACKMORE S, NILSSON S and LE THOMAS A. 2007. Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143: 1-81.
• QUETGLAS MA, DI PASQUO M and MACLUF CC. 2017. Diversidad de megasporas en los pozos Pando X1 y Manuripi X1, Bolivia: primera etapa de estudio. Ameghiniana 54: 45-46.
• REINSCH PF. 1881. Neue Untersuchungen uber die Mikrostruktur der Steinkole des Carbon, der Dyas und Trias. Leipzig.
• RICARDI-BRANCO F, ARAI M and ROSLER O. 2002. Megaspores from coals of the Triunfo Member, Rio Bonito Formation (Lower Permian), northeastern Paraná State, Brazil. An Acad Bras Cienc 74: 491-503.
• RICHARDSON JB and MCGREGOR DC. 1986. Silurian and Devonian spore zones of the Old Red Sandstone Continent and adjacent regions. Geol Surv Canada, Bull 364: 1-79.
• SCOTT AC and HEMSLEY AR. 1993. The spores of the Dinantian lycopsid cone Flemingites scottii from Pettycur, Fife, Scotland. Spec Pap Palaeontol 49: 31-41.
• SCOTT AC and HEMSLEY AR. 1996. Paleozoic megaspores. In: Jansonius J and Mcgregor DC (Eds), Palynology: principles and applications, Dallas: Amer Assoc Stratigr Palynol Found, p. 629-639.
• SCOTT AC and MEYER-BERTHAUD B. 1985. Plants from the Dinantian of Foulden, Berwickshire, Scotland. Trans R Soc Edinb Earth Sci 76: 13-20.
• STEEMANS P, BREUER P, JAVAUX EJ, LE HÉRISSÉ A, MARSHAL CP and DE VILLE DE GOYET F. 2009. Description and microscale analysis of some enigmatic palynomorphs from the Middle Devonian (Givetian) of Libya. Palynology 33: 101-112.
• STEEMANS P, BREUER P, PETUS E, PRESTIANNI C, VILLE DE GOYET F and GERIENNE P. 2011. Diverse assemblages of Mid Devonian megaspores from Libya. Rev Palaeobot Palynol 165: 154-174.
• THOMAS BA and BLACKBURN V. 1987. An ultrastructural study of some Carboniferous in situ megaspores assignable to Lagenicula horrida and Lageniosporites rugosus. Pollen Spores 29: 435-448.
• TRAVERSE A. 2007. Paleopalynology, 2nd ed., Dordrecht: Springer, 813 p.
• TRYON AF. 1986. Stasis, diversity and function in spores based on an electron microscope survey of the Pteridophyta. In: Blackmore S and Ferguson IK (Eds), Pollen and Spores: Form and Function, London: Linn Soc Symp Ser, 12, Academic Press, p. 233 249.
• VAVRDOVÁ M, BEK J, DUFKA P and ISAACSON PE. 1996. Palynology of the Devonian (Lochkovian to Tournaisian) sequence, Madre de Dios Basin, northern Bolivia. Vestnik Ceského geologického ústavu 71: 333-350.
• VAVRDOVÁ M and ISAACSON PE. 1996. Affinities of Late Devonian Acritarchs from the Madre de Díos Basin, Northern Bolivia: Evidence for Plate Tectonic Interaction between Eastern Laurentia and Western Gondwana? Acta Universitatis Carolinae Geologica 40: 683-693.
• WELLMAN CH. 2002. Morphology and wall ultrastructure in Devonian spores with bifurcate-tipped processes. Int J Plant Sci 163: 451-474.
• WELLMAN CH, ARIOLI C, SPINNER EG and VECOLI M. 2009. Morphology and wall ultrastructure of the megaspore Lagenicula (Triletes) mixta (Winslow 1962) comb. nov. from the Carboniferous (Early Mississippian: mid Tournaisian) of Ohio, USA. Rev Palaeobot Palynol 156: 51-61.
• WINSLOW MR. 1962. Plant spores and other microfossils from Upper Devonian and Lower Mississippian rocks of Ohio. Geo Surv, Prof Pap 364: 1-93.

Publication Dates

• Publication in this collection
  22 July 2019
• Date of issue
  2019

History

• Received
  24 July 2018
• Accepted
  6 Dec 2018