Isolated capsule-like reproductive organs from the upper Permian of the Southern Alps, NE Italy, are described as Brinkia gen. nov. Two species have been distinguished, i.e. Brinkia kerpiana sp. nov. and B. cortianensis sp. nov. Brinkia capsules resemble in gross morphology single valves of the Leptostrobus-type, Mesozoic reproductive organs belonging to the Czekanowskiales. A czekanowskialean affinity is reinforced by the fact that the Brinkia remains are found associated with strap-like leaves resembling those of Czekanowskia. This would expand the record of the Czekanowskiales to the Wuchiapingian (early Lopingian) and suggests that, during the arid late Permian climate, representatives of the order could occupy the more humid habitats within the deltaic floodplain formed during a sea-level rise.
The Permian is a period of important innovations and radiations among the gymnosperms including the peltaspermalean and glossopteridalean seed ferns, cycadophytes, ginkgophytes, Vojnovskiales and conifers. The modern aspect of the flora has been increased lately due to the appearance of ‘typical late Permian’ taxa such as voltzian conifers in early Permian successions (e.g. DiMichele et al. 2001; Forte et al. 2017, 2018) and of ‘typical Mesozoic’ plant taxa such as Dioonitocarpidium Rühle von Lilienstern 1928, Swedenborgia Nathorst 1876 and Dicroidium Gothan 1912 in Permian sediments (e.g. DiMichele et al. 2001; Abu Hamad et al. 2008). On the other hand, the botanical affinity of several Permian taxa and even plant groups is under debate. These include, among others, the Vojnovskiales, some putative ginkgophytes or conifers such as Dicranophyllum Grand’Eury 1877 and Trichopitys de Saporta 1875, Rufloriaceae and a considerable part of the Angaran and Gondwanan putative conifers.
The possibility of discovering such ‘abnormal’ taxa in the flora is increased by exceptional preservation (e.g. Abu Hamad et al. 2008), high abundance in collected material (e.g. DiMichele et al. 2001; Forte et al. 2017, 2018) and exceptional preservation potential of the sedimentary succession (e.g. Kustatscher et al. 2017a, b). The Bletterbach Gorge (NE Italy) is one of those areas worldwide that has yielded exceptional late Permian floras, including the well-preserved cuticles of the ‘cuticle horizon’ (Clement-Westerhof 1984, 1986, 1987) and a diverse and articulated flora with plant–animal interactions in the megafossil horizon (Kustatscher et al. 2012, 2014, 2017a, b; Bauer et al. 2014; Labandeira et al. 2016). Thus, it is not surprising that the Bletterbach plant assemblage includes also some scales and strap-like leaves that on first view resemble representatives of the order Czekanowskiales.
The Czekanowskiales include plants with persistent leaves borne on deciduous short shoots, subtended by scale-like leaves (Pant 1957; Krassilov 1968, 1972a, b; Taylor et al. 2009). Representatives of this group range from the Late Triassic to the Cretaceous (Ash 1994). The order includes several fossil genera with highly dissected leaves, such as Czekanowskia Heer 1876, Solenites Lindley and Hutton 1834, Sphenarion Harris et Miller in Harris et al. 1974, Phoenicopsis Heer 1876 and Arctobaiera Florin 1936, distinguished mainly on leaf morphology, arrangement of the leaves on short and/or long shoots and epidermal features. The leaves are hypostomatic or amphistomatic with stomata arranged in short longitudinal lines or bands (e.g. Samylina and Kiritchkova 1993; Kostina 1999). Stomatal distribution and arrangement are used to distinguish three subgenera (Samylina and Kiritchkova 1993), viz. Czekanowskia (amphistomatic leaves with stomata arranged in files), Harrisiella (amphistomatic leaves with stomata arranged in bands) and Vachrameevia (hypostomatic leaves with stomata arranged in files or band).
The reproductive genus Leptostrobus Heer 1876 is also assigned to this order. These ovulate cones were found associated, but never in organic connection, with Czekanowskia, Sphenarion, Phoenicopsis, and Solenites (Clifford and Camilleri 1998; Liu et al. 2006). The ovuliferous organs are flattened, globose and consist of two valves (together called capsules) with often a crenulate outer margin (Harris 1951; Krassilov 1968). The botanical affinity of the Czekanowskiales is still an open question. The various taxa were assigned to the ginkgophytes based on their highly dissected foliage (Harris 1935, 1951; Schweitzer and Kirchner 1995), distantly related to the seed ferns and conifers, or considered to represent a separate group of poorly defined gymnosperms (Meyen 1987; Taylor et al. 2009).
The aim of this paper is to describe these enigmatic plant remains from the Bletterbach and Cortiana (localities in the Southern Alps, NE Italy), including the capsule-like reproductive organs and the strap-like leaves, both macromorphologically and based on their cuticle. We compare them with possible producing plants in order to understand whether these remains could be the oldest representatives of the order Czekanowskiales, or if these organs belong to another group of gymnosperms. Finally, we discuss the putative ecology of these plants.
Materials and methods
Bletterbach Gorge is located at the western edge of the Dolomites, between the villages of Aldein/Aldino and Radein/Redagno (Fig. 1). The succession starts with the Auer/Ora Formation, the uppermost formation of the Athesian Volcanic Group (Morelli et al. 2007), whose activity is dated from 284.9 ± 1.6 to 274.1 ± 1.4 million years ago (Bargossi et al. 2007; Avanzini et al. 2007; Marocchi et al. 2008). The Permian volcanites are overlain unconformably by ~ 210 m of the late Permian (Wuchiapingian) Gröden/Val Gardena Sandstone (Cassinis et al. 1999; Morelli et al. 2007). This formation is characterised by red to greyish fluvial siliciclastics, evaporites and mixed carbonate–siliciclastic deposits, deposited in alluvial fans, braided rivers, shallow channels, coastal sabkhas, evaporitic lagoons and shallow marine shelf environments (Italian IGCP 203 1986; Ori 1988; Massari et al. 1988; Kustatscher et al. 2012, 2017a). A warm to hot, semi-arid to dry–subhumid climate with pronounced seasonality has been interpreted for this sedimentary succession (Cassinis et al. 1999). The Gröden/Val Gardena Sandstone is overlain by the Changhsingian Bellerophon Formation, the Early Triassic Werfen Formation, the late Anisian Richthofen Conglomerate and the Contrin Formation (for more details see Kustatscher et al. 2017a).
The Gröden/Val Gardena Sandstone of the Bletterbach is famous for its abundance and high diversity of tetrapod footprints (e.g. Conti et al. 1975, 1977, 1979; Ceoloni et al. 1988; Wopfner 1999; Bernardi et al. 2017), plant megafossils and mudstones rich in dispersed cuticles (e.g. Clement-Westerhof 1984, 1986, 1987; Poort and Kerp 1990; Visscher et al. 2001; Kustatscher et al. 2012, 2017a, b). The fossils discussed here were collected from a thin (~ 1 m thick) horizon at about 70 m from the base of the succession consisting of medium- to coarse-grained greyish sandstones, sometimes with small, intercalated gypsum nodules, termed the ‘megafossil horizon’ (Kustatscher et al. 2012, 2014, 2017a, b). The age of this plant assemblage is (possibly middle) Wuchiapingian (for more details see Kustatscher et al. 2017a, b).
Additional specimens originate from the transition interval between the Val Gardena Sandstone and the Bellerophon Formation of the Venetian Alps, exposed in a section east of the Village of Cortiana (Municipality of Valli del Pasubio, about 50 km NW of Vicenza; Fig. 1). The interval is characterised by alternating siliciclastic and dolomitic beds. The material did not yield any cuticles, but the carbonaceous impressions in the fine sandstone to siltstone are very well preserved. Other plant fossils from Cortiana mainly include conifer remains (Clement-Westerhof 1984). Comparable to the situation in the Butterloch, the facies transition is usually included in the Bellerophon Formation (Barbieri et al. 1980), and it seems justified to assign a Changhsingian age to these plant fossils.
Cuticles were obtained from most specimens through maceration of small fragments in Schulze’s reagent (KClO3 and 30% HNO3) and neutralised in ammonium hydroxide (NH4OH, 5%). Cuticles were mounted in glycerin jelly on microscope slides for light microscopic analysis and sealed with Paraplast (see Kerp 1990; Kerp and Krings 1999). Hand specimens were photographed with a Canon Eos D550 digital camera according to procedures outlined by Kerp and Bomfleur (2011). Cuticle images were captured with a Leica DMC4500 camera mounted on a Leica DM 2500 LED microscope in transmitted light. Cuticle slides and megafossils from the megafossil horizon at Bletterbach are stored at the Museum of Nature South Tyrol in Bozen/Bolzano (Italy) (specimen numbers preceded by ‘PAL’). Specimens from the Bletterbach cuticle horizons and from Cortiana with the prefix ‘UU’ are from the collections of the Laboratory of Palaeobotany and Palynology, Utrecht University, The Netherlands. One specimen comes from the historical collection of the Museo di Geologia e Palentologia, Dipartimento di Geoscienze—Università di Padova.
Genus Brinkia nov.
Type species. Brinkia kerpiana sp. nov., from the Wuchiapingian of Bletterbach, Dolomites, Northern Italy.
Diagnosis. Isolated, rounded valves with a lobed rim, and a number of radial ridges and furrows originating from a short basal column.
Etymology. In honour of Wies van den Brink, former palynologist and wife of Hans Kerp, who stimulated and supported him during his career.
Comparisons. So far, all female reproductive organs found in association with Czekanowskia, Sphenarion, Phoenicopsis and Solenites, and considered to be czekanowskialean in affinity were assigned to the genus Leptostrobus. These ovuliferous organs are flattened, globose and consist of two valves (called together capsules) arranged along a stout axis as slender cones. Although the specimens of Brinkia from Bletterbach are never found articulated and/or attached to the axis, the single valves resemble those of Leptostrobus in general shape. Both are characterised by globose valves with a distinct margin, a central part divided in ridges and marginal lobes. However, in Leptostrobus, each ridge finds its extension in a lobe on the margin and each capsule is much smaller and has much fewer ridges than in Brinkia.
There are a few female conifer remains that superficially look like czekanowskialean fructifications. Cardiolepis Neuburg 1965 emend. Meyen 1976 (now called Angaropeltis Doweld 2001) from the Permian of western Angara is characterised by large (diameter c. 4 cm) multi-seeded peltate capsules, smooth on the outside, with the ridges and furrows on the inside corresponding to impressions of the seeds (Meyen 1976). In Brinkia, on the other hand, the ridges are visible both on the outside and on the inside. Moreover, the capsule of Cardiolepis is not composed of two valves like in Leptostrobus (and we postulate also for Brinkia) but has a distinct stalk, not visible in our specimens.
The conifer Ullmannia bronnii Göppert 1850 from the upper Permian of Germany has globose scales differing because of the presence of a distinct stalk, and the completely fused single elements, giving origin to a globose scale without ridges (Florin 1944). Glyptolepis Schimper 1872 from the lower–middle Keuper (Ladinian–Carnian) of Germany shows ovuliferous cones with partially fused, stalked scales. The upper part of the scale is expanded and consists of a number of equal-sized lobes with an obtuse apex. Pachylepis Kräusel 1952 from the Schilfsandstein (Carnian) of Germany is a conifer cone with scales divided into five lobes, each bearing a single seed. The missing rim and the composite structure with only partially fused elements distinguish Glyptolepis and Pachylepis from Brinkia. The number of seeds and the three-dimensional organisation of these taxa cannot be compared since these are as yet unknown in Brinkia.
Remarks. The valves were always found isolated in the sediment. This makes it impossible to interpret whether the valves were organised in capsules like in Leptostrobus and how they would be attached and arranged on the axis. This, as well as the differences in dimensions and the presence of the basal column, supports an assignment to a different, new genus.
Brinkia kerpiana sp. nov.
2012 Incertae sedis, valve-like structure—Kustatscher et al.: p. 1, 6, pl. 3, figs. 5, 7.
2017b Leptostrobus-like valves—Kustatscher et al.: p. 50, pl. 3, fig. i.
Etymology. In honour of Hans Kerp, who studied the Bletterbach over several decades.
Type material. Holotype PAL 1465 with its counterpart PAL 1464, Fig. 2a–b, here designated.
Additional material. PAL 832, 865, 922 (several isolated specimens), 1149, 1381, 1383, 1448, 2052.
Repository. Palaeobotanical collection, Museum of Nature South Tyrol, Bozen/Bolzano, Italy.
Type locality. Bletterbach, Dolomites, Bozen/Bolzano Province, Northern Italy.
Type horizon. Megafossil horizon, Gröden/Val Gardena Sandstone, Wuchiapingian, Lopingian, upper Permian.
Diagnosis. Isolated, rounded, globose valves of approximately 11–16 mm, with an up to 2 mm wide marginal lobed rim; central part divided into over 10 radial ridges and furrows originating from a basal short column. Cuticle moderately thick, epidermal cells isodiametric to slightly elongated. Stomata arranged in single, slightly radiating files, often bordering within a file. Stomatal pit surrounded by 6–8 distinctly thickened subsidiary cells bearing a papilla.
Description. The isolated valves are more or less globose, in general a little wider than high. The basal margin is never completely preserved but appears to be straight (PAL 1464; Fig. 2b). The valves are 11 to 16 mm wide and high. They are characterised by an external rim of up to 2 mm width that completely surrounds the central part. The rim shows distinct outer lobes (0.5–1 mm high and 1–2 mm wide) with a rounded apex, both laterally and apically. The central part is well distinguished from the rim, and appears to be raised (or sunken in some specimens) in comparison with the rim (PAL 1448; Fig. 2d). It is divided radially by more than 10 radially arranged ridges and deep furrows that spread from the basal column to the inner margin of the rim. The ridges arise along the outer margin of the oval to almost circular basal column that is 2–3 mm long and 1.0–2.5 mm wide (Fig. 2d). The holotype (PAL 1465; Fig. 2a) is 16 mm wide and 15.5 mm high, with a 2 mm wide lobed rim, a central part that is divided into 11 radial ridges and furrows and an up to 3 mm long and 2.5 mm wide column.
Only one specimen (PAL 865; Figs. 2c, 3a, b) yielded a good cuticle of a valve. It is fairly thick, and the stomata are arranged in single files. Near the base of the valve there are only 3 stomatal files, but new files begin more distally either near the margin or in between other files. In the largest, but still incomplete fragment there are 10 files distally. In the basal part of the fragment there is a thicker margin with protrusions. The ordinary epidermal cells are isodiametric to slightly elongate, strongly papillate in the basal part, less heavily papillate distally. Stomata crowded within the files often bordering but never sharing subsidiary cells. The number of the distinctly thickened subsidiary cells is between 4 and 8 (mean 6), each bearing a papilla. In one cuticle fragment, a possible part of the rim was preserved. This small part was less thick than the valve cuticle, showed more elongated, non-papillate epidermal cells and only a few scattered stomata. The subsidiary cells were bearing small papillae.
Comparisons. This is discussed in a special section after the description of both species.
Remarks. The specimens were already mentioned previously as ‘valve-like structures’ or ‘Leptostrobus-like valves’ from the Gröden/Val Gardena Sandstone of the Bletterbach (Kustatscher et al. 2012, 2017b).
Brinkia cortianensis sp. nov.
Etymology. Based on the locality, Cortiana, where the specimens were collected.
Type material. Holotype UU16882A with its counterpart UU16882C, Fig. 2e, g, here designated (Palaeobotanical collection, Laboratory of Palaeobotany and Palynology, Utrecht, The Netherlands).
Additional material. UU16881A–D, UU16882B.
Repository. Palaeobotanical collection, Laboratory of Palaeobotany and Palynology, Utrecht, The Netherlands.
Type locality. Cortiana, Venetian Alps, Vicenza Province, Northern Italy.
Type horizon. Bellerophon Formation, Changhsingian, Lopingian, upper Permian.
Diagnosis. Isolated, rounded valves, up to 8 mm wide and 10 mm high with an up to 1 mm wide lobed rim with large apical lobes; central part divided into up to 7 radial ridges and furrows originating from a basal short column.
Description. The isolated valves are more or less globose, in general higher than wide. The basal margin is straight and restricted in comparison with the general shape of the valves, being only 4–5 mm wide (UU 16881A; Fig. 2f). The valves are from 7 to 8 mm wide and 7.5–10.0 mm high. They show an external rim of up to almost 2 mm width at the most apical part. The rim decreases in width laterally and disappears for the basal 2 mm of the margin (UU 16881A; Fig. 2f). It is characterised by distinct delicate outer lobes (0.2–0.6 mm high and 1.0–1.5 mm wide) with a slightly smoothed apex, both laterally and apically. At the most apical part there can be a pointed apex (UU 16882A; Fig. 2e). The central part of the valve is well distinguished, and appears to be raised (or sunken in some specimens) in comparison with the rim (UU 16881A; Fig. 2f). It is divided by up to 7 radially arranged ridges and deep furrows that spread from the basal column to the inner margin of the rim. The ridges arise along the outer margin of the subtriangular basal column that is 1–2 mm long and 1.0–1.5 mm wide (UU 16881A; Fig. 2f).
The holotype (UU 16882A; Fig. 2e) is 8 mm wide and 10 mm high, with an up to 2 mm wide rim that extends at the most apical point to 2.5 mm. Basally the scale reduces to 4 mm in width. The central part is divided into 7 radial ridges and furrows and an up to 2 mm long and 1 mm wide triangular column. The base of the triangle corresponds to a roundish area of about 1 mm in diameter.
Comparisons. Brinkia cortianensis sp. nov. differs from Brinkia kerpiana sp. nov. because of the smaller dimensions, the lower number of ridges and furrows, the non-continuous rim, the triangular shape of the column (against roundish) and the restricted base. As no cuticle has been found to date, we cannot compare the two species for this aspect.
Comparison between Brinkia and Leptostrobus species
Liu et al. (2006) gave a clear overview of all Leptostrobus species known so far (Triassic to Cretaceous in age), and we mainly refer to their work. Here we compare only with the type species L. laxiflorus Heer 1876, the best-known species L. cancer (both Jurassic in age), and three Leptostrobus species known from the Triassic, L. longus Harris 1935 from the Rhaetian–Liassic of Jameson Land (Greenland): L. myeongamensis Kim et al. 2002 from the Late Triassic of Korea and L. sphaericus Wang 1984 from Late Triassic of China (see also Table 1). All of these have axes to which the capsules are attached in a more or less loose spiral, although capsules and/or valves can often be found dispersed. Leptostrobus laxiflorus is distinguished from both Brinkia species in having oval capsules (versus almost globose ones), and the generally lower number of ribs (3–7). Moreover, the rim is more strongly lobed than in the Brinkia species (Heer 1876; Harris et al. 1974; Liu et al. 2006). Its cuticle is unknown, as in most Leptostrobus species.
Brinkia kerpiana sp. nov. and B. cortianensis sp. nov. differ from Leptostrobus cancer Harris 1951 because, in the latter, each ridge corresponds to a lobe on the margin and the ridges are slightly increasing in width towards the margin. Moreover, in L. cancer, the ridges run only slightly radially but mostly parallel to each other from the base towards the margin. Each capsule of L. cancer is much smaller (3–5 mm versus 11–16 or 7–10 mm) and has many fewer ridges (3–5) than B. kerpiana (at least 10) or B. cortianensis (up to 7). In L. cancer, each lobe corresponds to a 2 mm long and up to 1 mm wide seed. If the depressions close to the margin of the central part of the valves of B. kerpiana were indeed attachment areas of seeds or depressions of seeds (PAL 1465; Fig. 2a), these would be up to 2.5 mm long and 1.5 mm wide. However, there would not be enough space for each of the ridges to contain a single seed as described in L. cancer.
There are also a few cuticular differences between Leptostrobus cancer and Brinkia kerpiana; the most obvious one is that the stomata in L. cancer are scattered while they are arranged in a number of single, crowded files in B. kerpiana. Moreover, the epidermal cells in B. kerpiana are papillate, versus non-papillate in L. cancer. The number of subsidiary cells is slightly larger in B. kerpiana (6–8), versus 4–7 in L. cancer. And finally, the subsidiary cells in B. kerpiana are thickened and papillate, versus non-thickened and non-papillate in L. cancer. Brinkia cortianensis did not yield a cuticle, just as most Leptostrobus species (see Liu et al. 2006).
Leptostrobus longus from Greenland is the only other Leptostrobus species for which cuticular details are known (Harris 1935, 1951). It is quite close to L. laxiflorus in gross morphology but smaller in capsule size. Its cuticle is similar to that of L. cancer in having polygonal epidermal cells and scattered stomata. It is different in being thinner and having more thickly cutinised subsidiary cells in an irregular ring. Oishi and Takahashi (1996) described one Leptostrobus cone fragment from the Rhaetian of Japan as cfr. Leptostrobus laxiflorus, but noted in the paper that, after seeing Harris’s L. longus from Greenland, they thought their material more closely related to the latter. Too few details of the specimen are known to include in Table 1.
Leptostrobus myeongamensis from the Late Triassic of Korea (Kim et al. 2002; Kim 2010) differs considerably from all other species in showing a scale leaf below each capsule along the axis. Other species often show a few scale leaves below the whole fructification but never below a capsule (Kim 2010). For a close comparison between these species, see Table 1.
Both in the Bletterbach and at Cortiana, strap-like, elongated leaf fragments (up to 30 mm long and 2 mm wide) were found (Fig. 2h–k). Sometimes they show a bifurcation (e.g. PAL 858, 1394; Fig. 2h, j, k). In some cases, they may even cover entire bedding planes (e.g. Leonardi specimen, PAL 1394, 2014, Fig. 2h, i, k).
The cuticle is fairly thick and amphistomatic with stomata arranged in short, irregular files (Fig. 3e–g). The epidermal cells are isodiametric to elongate (Fig. 3c, d), sometimes papillate (Fig. 3d). Stomata within the files never share subsidiary cells, and the distance between 2 stomata is generally at least 2–3 epidermal cells. The distal and anticlinal walls of the subsidiary cells are thickened; the ends of the anticlinal walls may be interrupted by small pits or extensions into the lumina of the cells. The stomatal pit is roundish to square, sometimes covered by overarching papillae of the subsidiary cells. The stomata are typically haplocheilic with (4) 5 to 6 (8) monocyclic subsidiary cells with the anticlinal and distal walls thickened (Fig. 3e–g). In some stomata with only 4 subsidiary cells, these are arranged in 2 polar and 2 lateral cells; the two polar cells small and square to rectangular, the two lateral subsidiary cells half-moon shaped (Fig. 3e, g).
These strap-like, elongated leaves of incertae sedis (Kustatscher et al. 2012: p. 1, 5, pl. 2, figs. 4, 6) were considered to resemble leaf fragments of Dicranophyllum Grand’Eury 1877 (Bauer et al. 2014: p. 276, fig. 3G; Bernardi et al. 2017: p. 23, fig. 4K; Kustatscher et al. 2017b: p. 45, pl. 2, fig. f), or even leaves of the Czekanowskiales group, although some fragments were in the past interpreted as leaves of ‘Lepidodendron cfr. sternbergi Lind. et Hutt. vel Schizolepis permensis Heer’ (Leonardi 1948: p. 6–7, pl. 1, fig. 6).
Discussion on leaves
Strap-like leaves were produced by several Permian and Mesozoic plant genera. These include Dicranophyllum, Trichopitys de Saporta 1875, Polyspermophyllum Archangelsky and Cúneo 1990 and all the leaf genera of the order Czekanowskiales. They are mostly distinguished by their width, the presence or absence of bifurcations of the leaves and their organisation in fascicles and/or attachment to short or long shoots. The fragmentary preservation of our leaves impedes any information regarding the way of attachment or three-dimensional organisation on short or long shoots. Thus, a good comparison can only be made with taxa that both bifurcate and for which the cuticle is known.
Bifurcated strap-like leaves of late and middle Permian age are relatively rare. One specimen from the Estérel, SE France, called ‘late Permian plant species A’ has been figured by Boersma and Visscher (1969: p. 58, pl. 2, fig. 3). The age of the fragment should now be regarded as middle Permian (probably Wordian; Durand 2006). It shows a stem with perpendicularly arising fascicles of elongated leaves that might be characterised by bifurcations. Unfortunately, no cuticles are preserved from this specimen, but our dispersed leaves could well represent parts of this plant. More strap-like, bifurcated leaves are known from the early Permian. The leaves of Trichopitys, Polyspermophyllum and Dicranophyllum are also dissected several times (Zalessky 1932; Florin 1949, 1951; Barthel 1977; Archangelsky and Cúneo 1990; Barthel et al. 1998). However, the fact that these forms have not yet yielded any cuticles makes a comparison with these genera impossible.
Krassilov and Karasev (2009) mentioned and figured a fragment of a bifurcated leaf fragment from the upper Permian of Russia as ‘comparable with the Mesozoic Czekanowskiales, also on account of their stomatal structures’. Although not identical (epidermal and subsidiary cells less papillate), this fossil and its cuticle resemble the leaves associated in the Bletterbach with Brinkia kerpiana and may indeed have belonged to the Czekanowskiales.
The genera among the Czekanowskiales that include bifurcated or dissected leaves are Czekanowskia and Sphenarion, although occasionally leaves of Arctobaiera bifurcate near their apex. Czekanowskia includes elongated, highly dissected leaves with a single vein that enter the base and dichotomise below each bifurcation. Within the genus, the subgenus Czekanowskia is the most similar to our material because we are dealing with amphistomatic leaves and stomata organised in files, which is the main character for that subgenus (Samylina and Kiritchkova 1993). The stomata of the genus Czekanowskia are very variable, but in most cases two subsidiary cells are polar and 2–4 subsidiary cells lateral, whereas in our specimens most stomata are surrounded by a circle of subsidiary cells. Individual leaves of Sphenarion are narrowly wedge shaped, bifurcate at least once and show no distinction between petiole and lamina (Harris et al. 1974; Huang et al. 2017). In our fragments, bifurcations are only rarely observed. The monocyclic stomata resemble those from our material, but in Sphenarion the stomata are scattered within bands.
The shape and epidermal features of both the female reproductive organs and the associated leaves strongly support their assignment to the order Czekanowskiales. This notably expands the geographic distribution, since this is the first record for this order from the Southern Alps. More importantly, the temporal distribution of the order is extended from the Late Triassic (Liu et al. 2006) into at least the Wuchiapingian (early Lopingian), although a ‘progenitorial czekanowskialean leaf’ was figured previously from the Changhsingian of European Russia (Krassilov and Karasev 2009). This much earlier appearance in the fossil record of czekanowskialean plant remains is in line with a series of ‘typically Mesozoic’ groups in late Palaeozoic sediments, especially at low latitudes (DiMichele et al. 2001; Abu Hamad et al. 2008).
On the other hand, this opens a discussion on the palaeoenvironmental adaptation of the early representatives of the order, since Mesozoic members of the Czekanowskiales are considered to comprise seasonally deciduous trees or shrubs and be one of the dominant elements of the Mesozoic temperate or warm–temperate floras (e.g. Vakharameev 1991; Sun 1992; Zhou and Wu 2006; Li et al. 2015a, b). By contrast, the late Permian successions of Bletterbach and Cortiana were deposited under hot and arid climatic conditions, although sea-level rise may have given origin to a riparian environment, covered by an intrazonal hygrophytic vegetation. This is why the megafossil horizon (Flora A in Kustatscher et al. 2017a) is composed not only of conifers and peltaspermalean seed ferns with thick cuticles, but also of hygrophytic elements such as taeniopterids, sphenopterids and sphenophytes. The latter are characterised by thinner cuticles, although still protected by papillae (for more details see Kustatscher et al. 2017a). The cuticles of Brinkia kerpiana and of the associated leaves are of moderate thickness and demonstrate a papillate nature, similar to other hygrophytic elements found in the Bletterbach flora. This suggests that the plants may have occupied the more humid habitats within the deltaic floodplain that originated during sea-level rise.
Abu Hamad, A., H. Kerp, B. Vörding, and K. Bandel. 2008. A Late Permian flora with Dicroidium from the Dead Sea region, Jordan. Review of Palaeobotany and Palynology 149: 85–130.
Archangelsky, S., and R. Cúneo. 1990. Polyspermophyllum, a new Permian gymnosperm from Argentina, with considerations about the Dicranophyllales. Review of Palaeobotany and Palynology 63: 117–135.
Ash, S.R. 1994. First occurrence of Czekanowskia (Gymnospermae, Czekanowskiales) in the United States. Review of Palaeobotany and Palynology 81: 129–140.
Avanzini, M., G.M. Bargossi, A. Borsato, G.M. Castiglioni, M. Cucato, C. Morelli, G. Prosser, and A. Sapelza. 2007. Note Illustrative della Carte Geologica d’Italia, Foglio 026: Appiano. Servizio Geologico d’Italia, APAT, Roma: Access Publisher.
Barbieri, G., G.P. De Vecchi, V. De Zanche, E. Di Lallo, P. Frizzo, P. Mietto, and R. Sedea. 1980. Note illustrative della carta geologica dell’area di Recoaro alla scala 1:20.000. Memorie di Scienze Geologiche 34: 23–52.
Bargossi, G.M., V. Mair, M. Marocchi, C. Morelli, A. Moretti, and G. Piccin. 2007. A mega volcanotectonic collapse between Bolzano and Trento during the lower Permian. Mitteilungen der Österreichischen Mineralogischen Gesellschaft 153: 1–34.
Barthel, M. 1977. Die Gattung Dicranophyllum Gr. Eury in den varistischen Innensenken der DDR. Hallesches Jahrbuch für Geowissenschaften 2: 73–86.
Barthel, M., E. Bettag, and R. Noll. 1998. Dicranophyllum hallei Remy and Remy im oberen Rotliegend. Veröffentlichungen des Museums für Naturkunde Chemnitz 21: 5–20.
Bauer, K., E. Kustatscher, R. Butzmann, T.C. Fischer, J.H.A. van Konijnenburg-van Cittert, and M. Krings. 2014. Ginkgophytes from the upper Permian of the Bletterbach gorge (Northern Italy). Rivista Italiana di Paleontologia e Stratigrafia 120(3): 271–279.
Bernardi, M., F.M. Petti, E. Kustatscher, M. Franz, C. Hartkopf-Fröder, C.C. Labandeira, T. Wappler, J.H.A. van Konijnenburg-van Cittert, B.R. Peecook, and K.D. Angielczyk. 2017. Late Permian (Lopingian) terrestrial ecosystems: A global comparison with new data from the low-latitude Bletterbach Biota. Earth-Science Reviews 175: 18–43.
Boersma, M., and H. Visscher. 1969. On two Late Permian Plants from southern France. Mededelingen Rijks Geologische Dienst (Nieuwe Serie) 20: 57–63.
Cassinis, G., L. Cortesogno, L. Gaggero, F. Massari, C. Neri, U. Nicosia, and P. Pittau. 1999. Stratigraphy and facies of the Permian deposits between Eastern Lombardy and the Western Dolomites. Field Trip Guidebook 1999: 23–25.
Ceoloni, P., M.A. Conti, N. Mariotti, and U. Nicosia. 1988. New Late Permian tetrapod footprints from the Southern Alps. In Permian and Permian-Triassic boundary in the South-alpine segment of the western Tethys and additional regional reports, ed. G. Cassinis. Memorie della Società Geologica Italiana 34: 45–56.
Clement-Westerhof, J.A. 1984. Aspects of Permian Palaeobotany and Palynology. IV The conifer Ortiseia Florin from the Val Gardena Formation of the Dolomites and the Vicentinian Alps (Italy) with special reference to a revised concept of the Walchiaceae (Göppert) Schimper. Review of Palaeobotany and Palynology 41: 51–166.
Clement-Westerhof, J.A. 1986. Two peculiar types of coniferous ovuliferous Fructifications from the Val Gardena Formation of the Dolomites and the Vicentinian Alps—a preliminary account. Courier Forschungsinstitut Senckenberg 86: 89–100.
Clement-Westerhof, J.A. 1987. Aspects of Permian Palaeobotany and palynology. VII The Majonicaceae, a new family of Late Permian conifers. Review of Palaeobotany and Palynology 52: 357–402.
Clifford, H.T., and N. Camilleri. 1998. A mature cupule of Leptostrobus (Czekanowskiales) from the Late Triassic of Queensland. Memoirs of the Queensland Museum 42: 445–447.
Conti, M.A., G. Leonardi, N. Mariotti, and U. Nicosia. 1975. Tetrapod footprints, fishes and molluscs from the Middle Permian of the Dolomites (N. Italy). Memorie Geopaleontologiche dell’Università di Ferrara 3(2): 139–150.
Conti, M.A., G. Leonardi, N. Mariotti, and U. Nicosia. 1977. Tetrapod footprints of the Val Gardena sandstone (North Italy): their paleontological, stratigraphic and paleoenvironmental meaning. Paleontographica Italica (Nuova Serie) 70: 1–91.
Conti, M.A., G. Leonardi, N. Mariotti, and U. Nicosia. 1979. Nuovo contributo alla stratigrafia delle ‘Arenarie di Val Gardena’. Memorie della Società Geologica Italiana 20: 357–363.
DiMichele, W.A., S.H. Mamay, D.S. Chaney, R.W. Hook, and J. Nelson. 2001. An Early Permian Flora with late Permian and Mesozoic affinities from North Central Texas. Journal of Palaeontology 75: 449–460.
Doweld, A.B. 2001. Prosyllabus Tracheophytorum. Tentamen Systematis Plantarum Vascularium [Prosyllabus Tracheophytorum. Oпыт cиcтeмы cocyдиcтыx pacтeний]. Moskva: GEOS.
Durand, M. 2006. The problem of the transition from the Permian to the Triassic Series in southeastern France: comparison with other Peritethyan regions. Geological Society of London, Special Publications 265: 281–296.
Florin, R. 1936. Die fossilen Ginkgophyten von Franz–Joseph–Land nebst Erörterungen über vermeintliche Cordaitales Mesozoischen Alters: I. Spezieller Teil. Palaeontographica (B: Paläophytologie) 81: 71–173.
Florin, R. 1944. Die Koniferen des Oberkarbons und des Unteren Perms, Siebentes Heft. Palaeontographica (B: Paläophytologie) 85: 458–654.
Florin, R. 1949. The morphology of Trichopitys heteromorpha Saporta, a seed plant of Palaeozoic age, and the evolution of the female flowers in the Ginkgoinae. Acta Horti Bergiani 15: 79–108.
Florin, R. 1951. Evolution in cordaites and conifers. Acta Horti Bergiani 15: 285–388.
Forte, G., E. Kustatscher, J.H.A. van Konijnenburg-van Cittert, and H. Kerp. 2018. Sphenopterid diversity in the Kungurian of Tregiovo (Trento, NE-Italy). Review of Palaeobotany and Palynology 252: 64–76.
Forte, G., E. Kustatscher, J.H.A. van Konijnenburg-van Cittert, C.V. Looy, and H. Kerp. 2017. Conifer diversity in the Kungurian of Europe—evidence from dwarf-shoot morphology. Review of Palaeobotany and Palynology 244: 308–315.
Göppert, H.R. 1850. Monographie der fossilen Coniferen. Natuurkundige verhandelingen van de Hollandsche Maatschappij der Wetenschappen te Haarlem 2(6): 1–73.
Gothan, W. 1912. Über die Gattung Thinnfeldia Ettingshausen. Abhandlungen der Naturhistorischen Gesellschaft Nürnberg 19: 67–80.
Grand’Eury, M.F.C. 1877. Mémoires sur la Flore Carbonifère du department de la Loire et du Centre de la France, étudié aux trois points de vue Botanique, Stratigraphique et Géognostique. Paris: Imprimerie nationale.
Harris, T.M. 1935. The fossil Flora of Scoresby Sound, East Greenland. Meddelelser om Grønland 112: 1–176.
Harris, T.M. 1951. The Fructification of Czekanowskia and its Allies. Philosophical Transactions of the Royal Society of London (B: Biological Sciences) 235: 483–508.
Harris, T.M., W. Millington, and J. Miller. 1974. The Yorkshire Jurassic flora IV. Ginkgoales and Czekanowskiales. London: Trustees of the British Museum (Natural History).
Heer, O. 1876. Beiträge zur Jura-Flora Ost–Sibiriens und des Amurlandes. Mémoires de l’Académie Impérial des sciences de St. Pétersbourg 25: 1–58.
Huang, W., D.L. Dilcher, H. Wang, Y.-L. Na, Y.-F. Li, T. Li, and C.-L. Sun. 2017. First record of Sphenarion (Czekanowskiales) with epidermal structures from the Middle Jurassic of Inner Mongolia, China. Palaeoworld 26: 510–518.
Italian IGCP-203 Group, ed. 1986. Permian and Permian–Triassic boundary in the South-Alpine segment of the western Tethys. Pavia: Tipolitologia Communale Pavese. (= Field Guide-book. Field Conference S.G.I.-I.G.C.P. Project 203, Brescia, Italy).
Kerp, H. 1990. The study of fossil gymnosperms by means of cuticular analysis. Palaios 5: 548–569.
Kerp, H., and B. Bomfleur. 2011. Photography of plant fossils—new techniques, old tricks. Review of Palaeobotany and Palynology 166: 117–151.
Kerp, H., and M. Krings. 1999. Light microscopy of fossil cuticles. In Fossil plants and spores: Modern Techniques, eds. T.P. Jones and N.P. Rowe, 52–56. London: The Geological Society.
Kim, J.H. 2010. New materials of Leptostrobus myeongamensis Kim (Czekanowskiales) from the Upper Triassic Amisan Formation of Nampa Group in Korea. Journal of Korean Earth Science Society 31: 430–436.
Kim, J.H., H.-S. Kim, B.-J. Lee, J.M. Kim, and H.-K. Lee. 2002. A new species of Leptostrobus from the Upper Triassic Amisan Formation of the Nampo Groups in Korea. Journal of Korean Earth Science Society 23: 30–37.
Kostina, E.I. 1999. Czekanowskiales from the Jurassic deposits of the Kansk coal basin, Siberia. Paleontological Journal 33: 577–584.
Krassilov, V.A. 1968. A new group of Mesozoic gymnosperms: Czekanowskiales. Akademiia Nauk SSSR, Doklady Earth Sciences Section 178: 223–226. (in Russian).
Krassilov, V.A. 1972a. Mesozoic Flora from the Bureja River (Ginkgoales and Czekanowskiales). Moscow: Akademii Nauk SSSR. (in Russian).
Krassilov, V.A. 1972b. Morphology and systematics of ginkgos and czekanowskias. Paleontological Journal 6: 98–102.
Krassilov, V., and E. Karasev. 2009. Paleofloristic evidence of climate change near and beyond the Permian-Triassic boundary. Palaeogeography, Palaeoclimatology, Palaeoecology 284: 326–336.
Kräusel, R. 1952. Pachylepis nov. gen., eine neue Koniferen-Gattung aus dem süddeutschen Keuper. Senckenbergiana 32: 343–350.
Kustatscher, E., K. Bauer, R. Butzmann, T.C. Fischer, B. Meller, J.H.A. Konijnenburg-van Cittert, and H. Kerp. 2014. Sphenophytes, pteridosperms and possible cycads from the Wuchiapingian (Lopingian, Permian) of Bletterbach (Dolomites, Northern Italy). Review of Palaeobotany and Palynology 208: 65–82.
Kustatscher, E., M. Bernardi, F.M. Petti, M. Franz, J.H.A. van Konijnenburg-van Cittert, and H. Kerp. 2017a. Sea-level changes in the Lopingian (late Permian) of the northwestern Tethys and their effects on the terrestrial palaeoenvironments, biota and fossil preservation. Global and Planetary Change 148: 166–180.
Kustatscher, E., J.H.A. van Konijnenburg-van Cittert, K. Bauer, R. Butzmann, B. Meller, and T.C. Fischer. 2012. A new flora from the Upper Permian of Bletterbach (Dolomites, N-Italy). Review of Palaeobotany and Palynology 182: 1–13.
Kustatscher, E., J.H.A. van Konijnenburg-van Cittert, C.V. Looy, C.C. Labandeira, T. Wappler, R. Butzmann, T.C. Fischer, M. Krings, H. Kerp, and H. Visscher. 2017b. The Lopingian (late Permian) flora from the Bletterbach Gorge in the Dolomites, Northern Italy: a review. Geo.Alp 14: 39–61.
Labandeira, C.C., E. Kustatscher, and T. Wappler. 2016. Floral assemblages and patterns of insect herbivory during the Permian to Triassic of Northeastern Italy. PLoS One 11(11): 1–49.
Leonardi, P. 1948. Contributo alla conoscenza della flora delle Arenarie di Val Gardena (Permiano medio-inferiore) dell’Alto Adige: La nuova flora di Redagno e una felce di Egna. Memorie dell’Istituto di Geologia e Mineralogia dell’Università di Padova 16: 13–15.
Li, T., Y.F. Li, Y.L. Na, W. Huang, X. Tan, and C.L. Sun. 2015a. First report of subgenus Phoenicopsis (Czekanowskiales) from Middle Jurassic of Ordos, China and its paleoclimatic implications. Global Geology 18(3): 145–154.
Li, Y.F., C.L. Sun, T. Li, Y.L. Na, Y.J. Chen, and D.H. Xing. 2015b. Solenites (Czekanowskiales) from the Late Mesozoic Jehol Biota of southeastern Jilin, China and its paleoclimatic implications. Acta Geologica Sinica (English Edition) 89(4): 1088–1102.
Lindley, J., and W. Hutton. 1834. The fossil flora of Great Britain, vol. 2, no. 2. London: W.J. Ridgeway and Sons.
Liu, X.-Q., C.-S. Li, and Y.-F. Wang. 2006. Plants of Leptostrobus Heer (Czekanowskiales) from the Early Cretaceous and Late Triassic of China, with discussion of the genus. Journal of Integrative Plant Biology 48: 137–147.
Marocchi, M., C. Morelli, V. Mair, U. Klötzli, and G.M. Bargossi. 2008. Evolution of Large Silicic Magma Systems: New U-Pb Zircon Data on the NW Permian Athesian Volcanic Group (Southern Alps, Italy). The Journal of Geology 116: 480–498.
Massari, F., M.A. Conti, K. Helmold, N. Mariotti, C. Neri, U. Nicosia, G.G. Ori, M. Pasini, and P. Pittau. 1988. The Val Gardena sandstone and Bellerophon Formation in the Bletterbach gorge (Alto Adige, Italy): biostratigraphy and sedimentology. Memorie di Scienze Geologiche 40: 229–273.
Meyen, S.V. 1976. Permian conifers of West Angaraland and New Puzzles in the coniferalean phylogeny. Palaeobotanist 25: 298–313.
Meyen, S.V. 1987. Fundamentals of Palaeobotany. London: Chapman and Hill.
Morelli, C., G.M. Bargossi, V. Mair, M. Marocchi, and A. Moretti. 2007. The lower Permian volcanics along the Etsch valley from Meran to Auer (Bozen). Mitteilungen der Österreichischen Mineralogischen Gesellschaft 153: 195–218.
Nathorst, A.G. 1876. Anmärkningar om den fossilen floran vid Bjuf i Skåne. Kungliga Svenska Vetenskapsakademiens förHandlingar 1: 29–41.
Neuburg, M.F. 1965. The Permian Flora of the Petchora Basin. III. Cordaitales, Vojnovskyales annd seeds of gymnosperms. Trudy Geologicheskii Institut Akademiia Nauk SSSR 43: 3–64. (in Russian).
Oishi, S., and E. Takahashi. 1996. The Rhaetic plants from the Province Nagato, A supplement. Journal of the Faculty of Science, Hokkaido Imperial University (Ser. 4: Geology and Mineralogy) 3(2): 113–133.
Ori, G.C. 1988. The nature of Permian Rivers in Southern Alps. In Permian and Permian-Triassic boundary in the South-alpine segment of the western Tethys and additional regional reports, ed. G. Cassinis. Memorie della Società Geologica Italiana 34: 155–160.
Pant, D.D. 1957. The classification of gymnospermous plants. Palaeobotanist 6: 65–70.
Poort, R.J., and J.H.F. Kerp. 1990. Aspects of Permian palaeobotany and palynology. XI. On the recognition of true peltasperms in the Upper Permian of western and central Europe and a reclassification of species formerly included in Peltaspermum Harris. Review of Palaeobotany and Palynology 63: 196–225.
Rühle von Lilienstern, H. 1928. Dioonites pennaeformis Schenk, eine fertile Cycadee aus der Lettenkohle. Paläontologische Zeitschrift 10: 91–107.
Samylina, V.A., and A.I. Kiritchkova. 1993. The genus Czekanowskia Heer: Principles of systematics, range in space and time. Review of Palaeobotany and Palynology 79: 271–284.
Saporta, G. de. 1875. Sur la découverte de deux types nouveaux de Conifères dans les schistes permiens de Lodève (Hérault). Académie des Sciences de Paris, Comptes Rendus 80: 1017–1020.
Schimper, W.P. 1872. Traité de Paléontologie végétale ou la flore du monde primitif dans ses rapports avec les formations géologiques et la flore du monde actuel. Tome second. Paris: Bailliére J.B. et Fils.
Schweitzer, H.-J., and M. Kirchner. 1995. Die rhäto-jurassischen Floren des Iran und Afghanistans: 8. Ginkgophyta. Palaeontographica (B: Paläophytologie) 237: 1–58.
Sun, C.L. 1992. The division of the Early Jurassic floristic province of the Eurasia continent. PhD Dissertation, Changchun: Changchun University of Earth Science (in Chinese).
Taylor, T.N., E.L. Taylor, and M. Krings. 2009. Paleobotany. The biology and evolution of fossil plants, 2nd ed. New York: Elsevier/Academic.
Vakharameev, V.A. 1991. Jurassic and Cretaceous Floras and Climates of the Earth. Cambridge: Cambridge University Press.
Visscher, H., J.H.F. Kerp, J.A. Clement-Westerhof, and C.V. Looy. 2001. Permian floras of the Southern Alps. Natura Bresciana 25: 117–123.
Wang, Z.Q., and X.F. Wang. 1984. Fossil plants. In Palaeontological Atlas of North China II, ed. Tianjin Institute of Geology and Mineral Resources, 223–302. Beijing: Geological Publishing House.
Wopfner, H. 1999. Über Tetrapoden-Fährten, Kohlen und versteinerte Hölzer aus dem Grödner Sandstein Perm) bei Deutschnofen. Der Schlern 73: 23–32.
Zalessky, M.D. 1932. On two new Dicranophyllum from the Artinskian deposits of the Fore-Urals. Bulletin de l’Academie des Sciences de l’USSR 9: 1361–1364.
Zhou, Z., and X. Wu. 2006. The rise of Ginkgoalean plants in the early Mesozoic. Geological Journal 41: 363–375.
The authors wish to thank Francesca Uzzo and Roberta Branz (Museum of Nature South Tyrol) for their help with the photographs of cuticles and macroremains. Hendrik Nowak helped with the geographic figure. The macroflora of the Bletterbach has been collected and partly studied in a joint project of the Museum of Nature South Tyrol and the Geoparc Bletterbach (‘Upper Permian floras from the Bletterbach/Butterloch’). The study of the material has been partly carried out during the project ‘The Permian–Triassic ecological crisis in the Dolomites: extinction and recovery dynamics in Terrestrial Ecosystems’ financed by the Promotion of Educational Policies, University and Research Department of the Autonomous Province of Bolzano–South Tyrol and partly during the project ‘The end-Permian mass extinction in the Southern and Eastern Alps: extinction rates vs taphonomic biases in different depositional environments’ financed by the Euregio Science Fund (call 2014, IPN16) of the Europaregion Euregio Tirol Südtirol Trentino. This paper is also part of the IGCP 630 cooperation project ‘Permian–Triassic climatic and environmental extremes and biotic response’. E.K. acknowledges the financial support of the Alexander von Humboldt Foundation (3.3-ITA/1141759STP) during her stay at the Universities of Münster and Munich (‘Late Permian floras from the Southern Alps and the Germanic Zechstein Basin’). The authors thank the Department of Innovation, Research and University of the Autonomous Province of Bozen/Bolzano for covering the Open Access publication costs.
Handling Editor: Benjamin Bomfleur.
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Kustatscher, E., Visscher, H. & van Konijnenburg-van Cittert, J.H.A. Did the Czekanowskiales already exist in the late Permian?. PalZ 93, 465–477 (2019). https://doi.org/10.1007/s12542-019-00468-9
- Southern Alps
- Reproductive organs