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Preliminary account of plant mesofossils from the Maastrichtian Budurone microvertebrate site of the Haţeg Basin, Romania
Palaeogeography, Palaeoclimatology, Palaeoecology 293 (2010) 353–359
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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Preliminary account of plant mesofossils from the Maastrichtian Budurone microvertebrate site of the Haţeg Basin, Romania Sandra May Lindfors a,1, Zoltán Csiki b, Dan Grigorescu b, Else Marie Friis a,⁎ a b
Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden Department of Geology and Geophysics, Bucharest University, Bd. Bălcescu 1, RO-010041 Bucharest, Romania
a r t i c l e
i n f o
Article history: Received 7 May 2009 Received in revised form 18 October 2009 Accepted 19 October 2009 Available online 24 October 2009 Keywords: Angiosperms Dispersal Fossil fruits Fossil seeds Mesofossils Cretaceous
a b s t r a c t The Maastrichtian Budurone mesofossil flora includes 19 different types of angiosperm fruits and seeds. All fruits and seeds are small, 0.6–2.6 mm long and 0.5–1.9 mm broad, with calculated fruit volume ranging between 0.08 and 3.59 mm3 and seed volume between 0.08 and 0.79 mm3. The fossils show great similarity with other Cretaceous angiosperm fossils regarding their dimension and organisation. However, comparison with other Late Cretaceous and Early Cenozoic floras from Europe shows that surprisingly few of the Budurone fossils can be assigned to taxa previously described from Europe, and so far only a few taxa appear to be shared with other mesofossil floras. This indicates that the Budurone flora may have been isolated from the other European floras or represents a different kind of depositional environment. Fruits are mainly indehiscent nuts and drupes, and seeds are mostly anatropous without special ornamentation indicating a mixture of biotic and unassisted dispersal. This together with the small size of the fruits and seeds indicates that the Budurone plants grew in typical Late Cretaceous open vegetation perhaps under a seasonally dry climate. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Numerous mesofossil floras rich in angiosperm flowers, fruits and seeds have been discovered from Late Cretaceous strata of Europe (e.g., Knobloch and Mai, 1986; Friis et al., 2006a). Together with rich palynological assemblages these plant remains are the primary source for understanding terrestrial ecosystems in Europe during this time interval. Sites including terrestrial faunas are less common and terrestrial biota including both animal and plant fossils are almost absent from the latest Cretaceous of Europe (Csiki et al., 2008). The discovery of mesofossils at the Budurone microvertebrate site in the Haţeg Basin, Romania, is therefore of great interest in providing direct information of the plant community co-occurring with the rich and diverse continental fauna. The Budurone mesofossils are also important in representing the best dated mesofossil assemblage from the latest Cretaceous and thus providing insight into the Cretaceous vegetation immediately before the K/T boundary events. We here give a preliminary account of the Budurone mesofossil flora. The flora is angiosperm dominated. The fruits and seeds included in the flora are in general appearance similar to other Late Cretaceous floras from Europe, but it is remarkable that there are
⁎ Corresponding author. E-mail address: [email protected] (E.M. Friis). 1 Present adress: Enskedevägen 106 122 63 Enskede, Sweden. 0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.10.018
almost no taxa shared with other Late Cretaceous floras and most of the Budurone plant fossils are new to science.
2. Material and methods 2.1. Geological setting The plant material was discovered and extracted from the Budurone locality near the village of Vălioara (Fig. 1) while sieving for microvertebrate fossils in the Densuş-Ciula Formation of the Haţeg Basin, Transylvania, Romania. The locality was first identified in the late 1990s and has been collected intermittently from that time. The Budurone fossil locality is situated in the unnamed middle member of Maastrichtian continental Densuş-Ciula Formation, exposed in the northwestern part of Haţeg Basin, Romania (Grigorescu, 1992, 2005). The Maastrichtian fluvial sediments in this area, in the neighborhood of the Vălioara village, are represented by alternating red and green coloured, coarse-grained, poorly sorted conglomerate beds dominated by metamorphic rock fragments, with medium to fine-grained sandstones and silty mudstones. A relatively high proportion of the coarser deposits, compared to other outcropping areas of the Densuş-Ciula Formation, characterizes the Maastrichtian deposits around Vălioara. This is due to the close proximity of their source area to the northwest: the uplifted metamorphic basement of the Poiana Ruscă Mountains bordering the Haţeg Basin. Fine-grained deposits in the sequence vary from red and brown-red in colour
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Fig. 1. A. Simplified geological map of the Haţeg Basin, showing the location of the Budurone fossil site (star). B. Lithological column along the Budurone creek, with the fossiliferous level indicated by arrow. Column to the left indicates approximate colour changes.
(when associated with diffuse layers of small, irregular calcareous concretions) to green-grey and to blackish dark grey, indicating shifting palaeoenvironmental conditions between well-drained and more poorly drained floodplain environments. Several microvertebrate bone beds have been identified around Vălioara, in the fine-grained drab-coloured, greenish silty mudstones (Grigorescu et al., 1999; Vasile, 2008). The Budurone locality, located in the bed of the homonymous creek, a small, seasonal tributary of the Vălioara Brook, is of particular interest because of its unique lithology and peculiar fossil content (Csiki et al., 2008). The Maastrichtian beds of the Budurone valley are poorly exposed because the steep valley sides are heavily vegetated; the outcrop is restricted to the narrow bed of the creek and is usually partly submerged or covered by mud. Accordingly, the observations concerning the local lithology are very patchy. Correlations with other Maastrichtian deposits near Vălioara are also impeded by the isolated location of the Budurone valley, surrounded by grass-covered hills and cultivated fields. However, it has been possible to measure a short lithological succession that includes the Budurone site (Fig. 1B). The local lithological column (Fig. 1B) is characterized by a complete lack of red-coloured deposits, suggesting locally extensive reducing conditions. The coarse-grained deposits are represented by microconglomerates that grade vertically into well-sorted medium sandstones; occasionally, coarser conglomerates also occur, but the maximum size of the ruditic clasts is smaller than observed elsewhere around Vălioara. The base of the coarser beds is usually clear-cut, often irregular, erosional; their thickness is usually less than 50 cm. Transition to the overlying finer-grained deposits is sharp, less commonly transitional. The fine-grained beds are dominantly wellsorted, massive silty mudstones and mudstones, varying in colour between grey, bluish-grey and dark blackish grey. Their thickness is greater than the coarser beds, normally surpassing 50 cm and sometimes reaching 1 m. The fossiliferous level is located in the upper part of the measured section, and is a 1-m thick bed of dark, blackish-bluish massive, micaceous silty mudstone. X-ray diffractometry suggests that the composition of the bed is dominated largely by smectitic clay minerals; the swelling character of the wetted rock is consistent with these data. The microvertebrate remains are concentrated in the upper part of the
bed, close to the erosional boundary with the overlying conglomeratic sandstones. The microvertebrate bone bed that also includes the plant fossils described here is dominated by the skeletal elements of mainly aquatic taxa (fishes, frogs, albanerpetontids), with less frequent remains of semi-aquatic (turtles, crocodilians) or purely terrestrial (lizards, dinosaurs) taxa. This abundance spectrum is unique among reported Maastrichtian microvertebrate accumulations from the Haţeg Basin, and suggests the preservation of a largely autochtonous, locally derived aquatic–peri-aquatic community (Csiki et al., 2008). Another unusual feature of the Budurone locality is the occurrence, along with the vertebrate remains, of a diverse plant mesofossil assemblage represented by a variety of small-sized plant fossils, mostly fruits and seeds, which is not yet reported from any other contemporaneous microvertebrate bone bed from Haţeg. The preservation of the plant remains was probably due to the low-energy depositional setting, supported by the sedimentary features of the host rock as well as taphonomic features of the associated vertebrate remains. It has been, however, enhanced by the highly reducing nature of the fossiliferous bed, as suggested by the presence of small, framboidal pyrite concretions and common presence of charred wood fragments; both of these are again reported only from the Budurone site. 2.2. Preparation of material The plant mesofossil was recovered when searching for microvertebrates. The sediment samples were air dried till dry, then soaked in water with a low-concentration of hydrogen peroxide until the complete break-down of the matrix. The dry sediment was then coarsely screen-washed at the site (in the river) using two mesh sizes (1.5 mm and 0.7 mm) followed by drying in the air. Subsequently, the screened material was soaked and screen-washed in the laboratory using a 1 mm, a 0.6 mm, and occasionally also a 0.35 mm screen. Matrix adhering to the surface of the fossils was removed using HF and HCl and rinsing in water. The plant mesofossils are generally well preserved and coalified. The fossils were studied and sorted into roughly similar groups using reflected light microscope. For investigation of cellular details the material was mounted on aluminium stubs with nail polish as glue, sputtercoated with gold and studied using a Hitachi S-4300 Field Emission Scanning Electron Microscope.
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All specimens were measured using reflected light microscope and SEM pictures. Typically only length (L) and breadth (B) were measured, while thickness (T) was often difficult to measure, either due to compression or difficulties in handling the specimens. Seed volumes were calculated assuming an ellipsoid shape of all seeds following Eriksson et al. (2000a) with volume V = 4/3π(ab2) where a = L/2 and b = (B + T)/4; thickness was estimated to be 0.66B. Because of the restricted material the calculations were simplified to include only one measurement (largest) for each taxon. This is justified by the fact that the size range where more than one specimen was present per taxon was small. Figures were manipulated in Photoshop to make the background evenly black. 3. Results 3.1. Organisation and systematic position of Budurone fruits and seeds The Budurone mesofossil flora comprises 19 different taxa. Fruits are mostly indehiscent, nuts or drupes, but there are also two different kinds of capsular fruits. The seeds are mainly anatropous, but one kind of seed is campylotropous. Both fruits and seeds are minute (see Section 3.2), typically with a smooth surface without elaborate ornamentation. None of the fossils can be assigned with certainty to species or genera described previously from other Cretaceous floras of Europe and most of them probably represent new taxa. The number of specimens available for each taxon is, however, small and no formal naming or description is given for any of the fossils. In the following section we describe the diversity of forms by giving an overview of the fruits and seeds identified so far. Sizes for all taxa are given in Table 1. 3.1.1. Fruits Among the small indehiscent fruits is one fruit probably related to the Normapolles complex (Taxon 1, Fig. 2A). The fruit is ellipsoidal, 1.2 mm long and 0.7 mm broad, and broadly triangular in crosssection. The fruit is most probably formed from an inferior ovary as indicated by a faint depression close to the apex that shows the extension of the hypanthium. Narrow longitudinal ridges extend from the base of the fruit to the apex of the hypanthium rim. The surface is almost smooth with faint outlines of the small, slightly longitudinally extended epidermal cells. The fossil is very similar in external morphology and structure to species of the Normapolles genus Antiquocarya, first described from
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the Late Santonian–Early Campanian flora of Åsen, southern Sweden (Friis, 1983). It also shows similarities with other members of the Normapolles complex placed systematically in the “core” Fagales (Friis et al., 2006b). Most likely this fruit is a member of this group, but the fossil does not show remains of stamens or perianth, and no Normapolles pollen was observed on the surface of the fruit. A more precise assignment of the fossil is therefore not possible with the material currently available. Two other small indehiscent fruits that may have been derived from inferior ovaries are present in the Budurone mesofossil flora. They have a thinner, almost smooth fruit wall and faint longitudinal ridges on the surface. One of them (Taxon 2, Fig. 2B) is also triangular in cross-section, while the other (Taxon 3) is rounded. Both taxa may also belong to the Normapolles complex, but they are more fragmentary and do not show features critical for an assignment to any of the Normapolles genera currently described. There are several other indehiscent fruits with a smooth sclerenchymatic fruit wall. Taxon 4 (Fig. 2C) is bilocular and is one of the largest fruits in the assemblage. It has a thick sclerenchymatic fruit wall and resembles in several respects drupes of Cornaceae. Taxon 5 is smaller, but is otherwise similar in general construction, bilocular with a thick endocarp, and probably also represents a drupe. Three other probably drupaceous fruits (Taxon 6, Taxon 7, Taxon 8, Fig. 2E–H) are unilocular with a single thin-walled seed. All these fruits had a smooth or only slightly rugulate endocarp. One fruit, however, has a distinctly pitted endocarp wall characteristic for some drupaceous fruits (e.g., in the Rosaceae, Sabiaceae and Icacinaceae). This Taxon (Taxon 9, Fig. 2I) comprises several fragments of rather large endocarp. The endocarp wall is thick, about 0.4 mm, composed of sclereid extensively pitted sclerid cells. The outer surface of the endocarp wall has several circular depressions of roughly equal size, about 0.8 mm in diameter, as well as numerous tiny perforations. The inside of the endocarp wall shows two layers, one smooth external layer and an inner layer of polygonal, slightly convex cells. Two different capsular fruits are present in the Budurone mesofossil flora. One taxon (Taxon 10, Fig. 2J) comprises five-locular capsules that are ovoid with a truncate apex. The outer layer is cracked, but shows raised papillate epidermal cells in some areas. The fruits are very similar to capsular fruits described from other Maastrichtian floras of Europe that have been included in the Ericales (Knobloch and Mai, 1986) and an ericalean affinity is also suggested for the Budurone capsules. The other capsular fruit (Taxon 11) from Budurone is more fragmentary preserved, but also five-locular. It is distinguished from the other capsular fruit by its circular outline, but is probably also of ericalean affinity.
Table 1 Fruit and seed size in the Budurone mesofossils.
Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Length (mm)
Breadth (mm)
Thickness (mm)— approx
Volume mm3
1.2 1.4 2 2.6 1.1 1.5 1.9 1.3
0.70 0.40 1.00 1 0.8 1.1 1.9 1
0.462 0.264 0.660 0.660 0.528 0.726 1.900 0.660
0.21209583 0.08079841 0.72141439 0.93783871 0.25393787 0.65468356
1.5
1.5
1.500
1.76714587
0.6 0.9
0.60 0.5
0.396 0.330
0.07791275 0.08115912
0.7 1.1 1.3 0.7 1.5
0.6 0.8 1.3 0.9 1.2
0.396 0.528 0.858 0.594 0.792
0.09089821 0.25393787 0.79247371 0.20452098 0.77912754
0.46891936
EMF
V = 4/3π(ab2)
0.212095832 0.080798412 0.721414393 0.937838711 0.253937866 0.654683562 3.591364002 0.468919355 0 1.767145868 0 0.077912754 0.081159119 0 0.090898214 0.253937866 0.792473711 0.20452098 0.779127544
3.1.2. Seeds Eight different kinds of isolated seeds were observed in the Budurone mesofossil flora. All seeds are small and most of them are smooth without any special surface ornamentation. Most are anatropous, but one taxon (Taxon 12, Fig. 3A, B) is campylotropous. The campylotropous seeds (Taxon 12) are disc-shaped, flattened and with a circular to kidney-shaped outline. There is a shallow depression in the central part of each seeds. Micropyle and hilum are close together. The epidermal cells have raised anticlinal walls that give the seed surface an undulate to reticulate ornamentation. The cells are arranged in semicircular rows around the central depression. The seed wall is thick, formed mostly of the outer epidermal cells that have deep, strongly thickened anticlinal and inner periclinal walls. These seeds are very similar in shape and general construction to seeds of extant and fossil Eurya (Ternstroemiaceae: Ericales) and they are particularly similar to seeds assigned to the fossil species Eurya crassa from the Late Cretaceous of central Europe (Knobloch and Mai, 1986). None of the fossils, however, show characters of the inner walls of epidermal cells or the inside of the seed that are typically used for
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Fig. 3. Fruits from the Budurone mesofossil flora. A, B. Taxon 12, aff. Eurya crassa, campylotropous seeds (Ternstroemiaceae). C, D. Taxon 13, seeds of possible buxaceous affinity. E. Taxon 14, angular seed with papillate surface. F. Taxon 18, barrel-shaped seed with crystal cells. G, H. Taxon 17, seeds with circular to ovoid outline, a distinct groove close to the apex, and crystal cells. I. Taxon 19, aff. Klikovispermum, larger anatropous seeds. All pictures SEM.
determining fossil Eurya seeds, and with the material currently available we hesitate to place the fossil in the modern genus. Among the most characteristic seeds from Budurone mesofossil flora are small ovoid, anatropous seeds with an apical and lateral depression and a distinct incurved stalk (Taxon 13, Fig. 3C, D). The stalk has a truncate tip. The seed surface is smooth and uniform over whole specimen. The seed wall is thick and composed of small thickwalled, almost isodiametric cells with finely undulate anticlinal walls. Similar seed morphology is known for extant Buxaceae, but the seeds of extant genera in this family typically have a thinner seed wall. Two other characteristic seed types from Budurone are anatropous and have polygonal and isodiametric epidermal cells with raised periclinal wall that give the seed surface a papillate appearance. One of them (Taxon 14, Fig. 3E) has angular to spherical seeds that sometimes split open from the apex. The other (Taxon 15) has ovoid seeds with longitudinal ridges. The mesofossil flora also includes two different kinds of seeds with imprints of crystals in the epidermal cells. One of these (Taxon 17, Fig. 3G, H) has a circular to ovoid outline and a distinct groove close to the apex, the other kind (Taxon 18, Fig. 3F) is barrel-shaped with an apical depression at the micropylar area. Taxon 19 (Fig. 2I) is an anatropous seed and is the largest seed recognized in the Budurone assemblage. It is most similar to Late Cretaceous seeds assigned to the extinct genus Klikovispermum (Knobloch and Mai, 1986). This genus is a heterogeneous, probably unnatural assemblage of seeds of uncertain affinity.
3.2. Size of fruits and seeds The fruits and seeds are all very small ranging in length from about 0.6 to 2.6 mm (Table 1). The smallest seeds are the Eurya-like seeds (Taxon 12) with a diameter of about 0.6 mm and the largest seed is the Klikovispermum-like seed (Taxon 19), about 1.5 mm long and 1.2 mm broad. The smallest fruit is the Normapolles type fruit of Taxon one, about 1.2 mm long and 0.7 mm broad, and the largest entire fruit is bilocular drupaceous fruit of Taxon 4 that is about 2.6 mm long and 1.0 mm broad. One fruit type (Taxon 9) is larger, but preserved only as fragments. Based on the size and shape of the fragments this fruit would have been up to about 5 mm long. Volumes of fruits and seeds were calculated using the formula and assumptions in Eriksson et al. (2000a) (see Material and methods) resulting in the following size ranges for the Budurone flora: fruit volume: 0.08– 3.59 mm3 and seed volume: 0.08–0.79 mm3 (Table 1). 4. Discussion 4.1. Systematic assignment of the Budurone mesofossils The fossil fruits and seeds identified from the Budurone mesofossil are all of angiosperm affinity. They have been compared to other fruits and seeds described from Late Cretaceous and Palaeogene floras of Europe, but in most cases the Budurone specimens appear to represent new taxa not previously recorded for Europe. Many of the
Fig. 2. Fossil fruits from the Budurone mesofossil flora. A. Taxon 1, indehiscent fruit probably related to the Normapolles complex. B. Taxon 2, indehiscent fruit, perhaps related to the Normapolles complex. C. Taxon 4, bilocular fruit with thick sclerenchymatic fruit wall. D. Taxon 5, bilocular fruit with a thick endocarp. E. Taxon 6, unilocular drupaceous fruit with a single thin-walled seed. F. Taxon 7, unilocular drupaceous fruit with a single thin-walled seed. G, H. Taxon 8, unilocular drupaceous fruit with a single thin-walled seed. I. Taxon 9, endocarp with strongly pitted wall, fragment. J. Taxon 10, five-locular capsule probably related to Ericales. All pictures SEM.
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fruits and seeds are of very general construction. Drupaceous fruits are one or two-locular without special features that would allow a more detailed systematic assessment and a systematic assignment for the fossils was in most cases not possible. One type (Taxon 1) is most likely assignable to the Normapolles complex. The Normapolles complex is an extinct group of angiosperms that produced distinctive, mostly oblate pollen grains of triangular shape (Stemma Normapolles of Pflug, 1953). The group experienced an enormous diversification during the mid- and Late Cretaceous (Góczán et al., 1967; Batten and Christopher, 1981; Friis et al., 2006b). The plants are known mostly from their dispersed pollen grains that are collectively referred to as Normapolles. Their first appearance in the fossil record is in the midto Late Cenomanian and the latest occurrences are from the Early Oligocene. Normapolles pollen grains have now also been found in situ in fossil flowers (e.g., Friis, 1983; Friis et al., 2006b). Although a considerable diversity of Normapolles flowers are known already, systematic studies show that they all belong to extinct taxa related to the subgroup of the modern order Fagales that includes Betulaceae, Rhoipteleaceae, Juglandaceae and related families. Most of the Normapolles flowers described so far are epigynous and bisexual. The fossil fruit from Budurone was also derived from an inferior ovary, but whether it was bisexual or unisexual is unknown. The presence of Normapolles plants in the Budurone vegetation conforms with the results of previous palynological investigations that documented the occurrence of several different kinds of dispersed Normapolles pollen in palynofloras of the Haţeg Basin (Antonescu et al., 1983; Van Itterbeeck et al., 2005), and more specifically for the Budurone site itself (Csiki et al., 2008). Two other taxa (Taxon 2, Taxon 3) have features suggesting affinity with the Normapolles complex, but they are not sufficiently well preserved for a secure identification. Another systematic group that is most likely represented in the flora is the Ericales with the two capsular fruits (Taxon 10 and Taxon 11) and Eurya-like seed (Taxon 12). This is in line with our knowledge of other Late Cretaceous mesofossil floras that often include a great diversity of Ericales, and a variety of Ericales are also reported for other Maastrichtian floras of Central Europe (Knobloch and Mai, 1986). 4.2. Comparison of the Budurone mesofossil with other Late Cretaceous– Palaeogene floras Compared with other Maastrichtian or Paleocene floras the proportion of fossils that can be attributed to modern families or orders is very low. For the two rich Maastrichtian mesofossil floras from Walbeck and Eisleben, Germany, 22 modern families were reported (Knobloch and Mai, 1986). More material and a more detailed systematic work on Budurone mesofossils would most likely result in the identification of more modern taxa, but the preliminary studies do not indicate a strong systematic similarity with other contemporaneous floras. This diversity recorded in the Budurone floras is lower than that known from other fossil floras from the latest Cretaceous (e.g., Knobloch and Mai, 1986) and from the earliest Cenozoic (Mai, 1987). For example, the Eisleben flora has 48 taxa and the Walbeck flora has 67 taxa. However, these mesofossil floras are based on a much larger sample of specimens than the Budurone flora (sometimes several hundred fossils). A greater sample from Budurone would most likely yield a higher number of taxa. Despite these differences the Budurone flora does show great similarity with other Cretaceous mesofossil floras in terms of the dimension of the fruits and seeds (see below) and organisation. Both the Eisleben and Walbeck floras also show the same general composition with a diversity of seeds, nuts, drupes and capsules. Surprisingly few of the Budurone fossils can be assigned to taxa previously described from Europe, and so far only a few taxa appear to
be shared with other mesofossil floras. This may indicate that the Budurone flora was isolated from other European floras by geographical barriers, but the alternative possibility, that the Budurone locality represents a different kind of depositional environment also needs to be considered in view of the unusual co-occurrence of microvertebrate and plant remains. 4.3. Ecological signal from the Budurone plant mesofossils Most of the vertebrate fossils from the Budurone fossiliferous bed represent semi-aquatic or aquatic habitats, but distinctive wetland and aquatic taxa appear to be absent from the mesofossil flora. At least such families as Cabombaceae, Cyperaceae, Najadaceae, Nymphaeaceae, Potamogetonaceae, Sparganiaceae, and Typhaceae have not been observed. All these families are common in wetlands and lakes today. They typically have seeds and fruits that fossilize well and are easy to recognize, and they also occur abundantly in many Palaeogene and Neogene fruit and seed floras. Previous studies of seeds and fruits from the Cretaceous and Cenozoic from the mid-palaeolatitudes have shown that angiosperm fruits and seeds are generally very small in the Cretaceous, typically with a volume of about 1 mm3 and that larger fruit and seeds are not common until the Palaeogene (Tiffney, 1984; Eriksson et al., 2000a,b; Eriksson, 2008). The fruits and seeds from Budurone are all very small, ranging in length being between 0.6 and 2.6 mm (5 mm infer for Taxon 9). The calculated volumes range between 0.08 and 3.59 mm3. This corresponds well to seed and fruit volumes calculated for other fossil floras from the Cretaceous (Eriksson et al., 2000a). The other Maastrichtian mesofossil floras show a comparable size range for seeds, but fruits are generally larger. Several hypotheses have been put forward to explain the mechanism behind the radical changes in fruit and seed size from the Cretaceous to the Cenozoic (e.g., Tiffney, 1984; Eriksson et al., 2000a; Tiffney, 2004; Moles et al., 2005). One hypothesis suggested that large seeds were developed only in the Cenozoic as a response to the radiation of frugivorous vertebrates in the Palaeogene (Tiffney, 1984). Because potential dispersers, as well as fruits apparently adapted to animal dispersal, were already present in the Early Cretaceous (Eriksson et al., 2000a) it has been suggested that the distinct increase in seed and fruit sizes around the K/T boundary was more likely driven by environmental changes (Eriksson et al., 2000a; Eriksson, 2008). Specifically, the change in vegetational structure that resulted from a warm probably seasonally dry climate in the Cretaceous, which supported open vegetation, being replaced by a more humid climate, which supported closed vegetation in the Early Cenozoic, although associated changes in seed dispersing animals would have also had an impact (Eriksson, 2008). The presence of drupaceous fruits in the Budurone mesofossil assemblage indicates that some of the fossils may have had biotic dispersal, but the small nuts and seeds without specialized ornamentation suggest unassisted dispersal. This together with the small size of the fruits and seeds from the Budurone locality suggests that typical Late Cretaceous open vegetation probably growing under seasonally dry conditions was present in Europe until the very end of the Cretaceous contrasting the closed multilayered canopy forests that took over in Europe during the Early Cenozoic. 5. Conclusion The Budurone mesofossil flora is important in providing direct information of the plant community co-occurring with the rich and diverse terrestrial fauna. It is also important in providing insight into the Cretaceous vegetation in Europe immediately before the K/T boundary events. The flora comprises 19 taxa of angiosperm fruits and seeds. They are in general appearance similar to other Late Cretaceous floras from Europe, but it may be significant that there are perhaps no
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taxa or only few shared taxa with other Late Cretaceous floras from Europe. The size range of the fossils is also in accordance with other Late Cretaceous floras and indicates that open vegetation prevailed in Europe till the end of the Cretaceous. Acknowledgements We are grateful to a number of students of the University of Bucharest (and foremost to Romeo Limberea, Oana Pupaza and Stefan Vasile) for their help in collecting, processing and hand-picking the Budurone fossil material, to Yvonne Arremo, Stockholm, for help with preparation of material for SEM, as well as Peter R. Crane, Chicago, and an anonymous reviewer for helpful comments to the manuscript. We also thank the Swedish Research Council for financial support (to EMF). Grants of the Romanian Academy of Sciences (GAR 167/1997 and 39/2001 to DG) supported the discovery and early collection at the Budurone site; more recent fieldwork was supported by the National University Research Council grants 436/2007 and 1930/2009 (to ZCS). References Antonescu, E., Lupu, D., Lupu, M., 1983. Correlation palinologique du Crétacé terminal du sud — est des Monts Metaliferi et des Depressions de Haţeg et de Rusca Montană. Annuaire de l'Institute de Géologie et Géophysique 59, 71–77. Batten, D.J., Christopher, R.A., 1981. Key to recognition of Normapolles and some morphologically similar genera. Review of Palaeobotany and Palynology 35, 359–383. Csiki, Z., Ionescu, A., Grigorescu, D., 2008. The Budurone microvertebrate site from the Maastrichtian of the Haţeg Basin-Flora, fauna, taphonomy and paleoenvironment. Acta Palaeontologica Romaniae 6, 49–66. Eriksson, O., 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169, 863–870. Eriksson, O., Friis, E.M., Löfgren, P., 2000a. Seed size, fruit size and dispersal spectra in angiosperms from the Early Cretaceous to the Late Tertiary. American Naturalist 156, 47–58.
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Eriksson, O., Friis, E.M., Pedersen, K.R., Crane, P.R., 2000b. Seed size and dispersal systems of Early Cretaceous angiosperms from Famalicão, Portugal. International Journal of Plant Sciences 161, 319–329. Friis, E.M., 1983. Upper Cretaceous (Senonian) floral structures of juglandalean affinity containing Normapolles pollen. Review of Palaeobotany and Palynology 39, 161–188. Friis, E.M., Pedersen, K.R., Crane, P.R., 2006a. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232, 251–293. Friis, E.M., Pedersen, K.R., Schönenberger, J., 2006b. Normapolles plants: a complex of extinct fagalean lineages. Plant Systematics and Evolution 260, 107–140. Góczán, F., Groot, J.J., Krutzsch, W., Pacltová, B., 1967. Die Gattungen des “Stemma Normapolles Pflug 1953b” (Angiospermae) — Neubeschreibungen und Revision europäischer Formen (Oberkreide bis Eozän). Paläontologische Abhandlungen B 2, 427–633. Grigorescu, D., 1992. Nonmarine Cretaceous formations of Romania. In: Chen, P.-J., Matter, N.J. (Eds.), Aspects of Nonmarine Cretaceous Geology. China Ocean Press, Beijing, pp. 142–164. Grigorescu, D., 2005. Rediscovery of a “forgotten land”. The last three decades of research on the dinosaur-bearing deposits from the Hateg Basin. Acta Palaeontologica Romaniae 5, 191–204. Grigorescu, D., Venczel, M., Csiki, Z., Limberea, R., 1999. New microvertebrate fossil assemblages from the Uppermost Cretaceous of the Haţeg Basin (Romania). Geologie en Mijnbouw 78, 301–314. Knobloch, E., Mai, D.H., 1986. Monographie der Früchte und Samen in der Kreide von Mitteleuropa. Rozpravy ústredního ústavu geologickénho. Praha 47, 1–219. Mai, D.H., 1987. Neue Fruchte und Samen aus paläozänen Ablagertungen Mitteleuropas. Feddes Repertorium 98, 197–229. Moles, A.T., et al., 2005. Factors that shape seed mass evolution. Proceedings of the National Academy of Sciences 102, 10540–10544. Pflug, H.D., 1953. Zur Entstehung und Entwicklung des angiospermiden Pollen in der Erdgeschichte. Palaeontographica B 95, 60–171. Tiffney, B.H., 1984. Seed size, dispersal syndromes, and the rise of the angiosperms: evidence and hypothesis. Annals of the Missouri Botanical Garden 71, 551–576. Tiffney, B.H., 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology and Systematics 35, 1–29. Van Itterbeeck, J., Markevich, V.S., Codrea, V., 2005. Palynostratigraphy of the Maastrichtian dinosaur- and mammal sites of the Râul Mare and Bărbat Valleys (Haţeg Basin, Romania). Geologica Carpathica 56, 137–147. Vasile, S., 2008. A new microvertebrate site from the Upper Cretaceous (Maastrichtian) deposits of the Hateg Basin. Sargetia. 21, 4–14.
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Preliminary account of plant mesofossils from the Maastrichtian Budurone microvertebrate site of the Haţeg Basin, Romania Sandra May Lindfors a,1, Zoltán Csiki b, Dan Grigorescu b, Else Marie Friis a,⁎ a b
Department of Palaeobotany, Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden Department of Geology and Geophysics, Bucharest University, Bd. Bălcescu 1, RO-010041 Bucharest, Romania
a r t i c l e
i n f o
Article history: Received 7 May 2009 Received in revised form 18 October 2009 Accepted 19 October 2009 Available online 24 October 2009 Keywords: Angiosperms Dispersal Fossil fruits Fossil seeds Mesofossils Cretaceous
a b s t r a c t The Maastrichtian Budurone mesofossil flora includes 19 different types of angiosperm fruits and seeds. All fruits and seeds are small, 0.6–2.6 mm long and 0.5–1.9 mm broad, with calculated fruit volume ranging between 0.08 and 3.59 mm3 and seed volume between 0.08 and 0.79 mm3. The fossils show great similarity with other Cretaceous angiosperm fossils regarding their dimension and organisation. However, comparison with other Late Cretaceous and Early Cenozoic floras from Europe shows that surprisingly few of the Budurone fossils can be assigned to taxa previously described from Europe, and so far only a few taxa appear to be shared with other mesofossil floras. This indicates that the Budurone flora may have been isolated from the other European floras or represents a different kind of depositional environment. Fruits are mainly indehiscent nuts and drupes, and seeds are mostly anatropous without special ornamentation indicating a mixture of biotic and unassisted dispersal. This together with the small size of the fruits and seeds indicates that the Budurone plants grew in typical Late Cretaceous open vegetation perhaps under a seasonally dry climate. © 2009 Elsevier B.V. All rights reserved.
1. Introduction Numerous mesofossil floras rich in angiosperm flowers, fruits and seeds have been discovered from Late Cretaceous strata of Europe (e.g., Knobloch and Mai, 1986; Friis et al., 2006a). Together with rich palynological assemblages these plant remains are the primary source for understanding terrestrial ecosystems in Europe during this time interval. Sites including terrestrial faunas are less common and terrestrial biota including both animal and plant fossils are almost absent from the latest Cretaceous of Europe (Csiki et al., 2008). The discovery of mesofossils at the Budurone microvertebrate site in the Haţeg Basin, Romania, is therefore of great interest in providing direct information of the plant community co-occurring with the rich and diverse continental fauna. The Budurone mesofossils are also important in representing the best dated mesofossil assemblage from the latest Cretaceous and thus providing insight into the Cretaceous vegetation immediately before the K/T boundary events. We here give a preliminary account of the Budurone mesofossil flora. The flora is angiosperm dominated. The fruits and seeds included in the flora are in general appearance similar to other Late Cretaceous floras from Europe, but it is remarkable that there are
⁎ Corresponding author. E-mail address: [email protected] (E.M. Friis). 1 Present adress: Enskedevägen 106 122 63 Enskede, Sweden. 0031-0182/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2009.10.018
almost no taxa shared with other Late Cretaceous floras and most of the Budurone plant fossils are new to science.
2. Material and methods 2.1. Geological setting The plant material was discovered and extracted from the Budurone locality near the village of Vălioara (Fig. 1) while sieving for microvertebrate fossils in the Densuş-Ciula Formation of the Haţeg Basin, Transylvania, Romania. The locality was first identified in the late 1990s and has been collected intermittently from that time. The Budurone fossil locality is situated in the unnamed middle member of Maastrichtian continental Densuş-Ciula Formation, exposed in the northwestern part of Haţeg Basin, Romania (Grigorescu, 1992, 2005). The Maastrichtian fluvial sediments in this area, in the neighborhood of the Vălioara village, are represented by alternating red and green coloured, coarse-grained, poorly sorted conglomerate beds dominated by metamorphic rock fragments, with medium to fine-grained sandstones and silty mudstones. A relatively high proportion of the coarser deposits, compared to other outcropping areas of the Densuş-Ciula Formation, characterizes the Maastrichtian deposits around Vălioara. This is due to the close proximity of their source area to the northwest: the uplifted metamorphic basement of the Poiana Ruscă Mountains bordering the Haţeg Basin. Fine-grained deposits in the sequence vary from red and brown-red in colour
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Fig. 1. A. Simplified geological map of the Haţeg Basin, showing the location of the Budurone fossil site (star). B. Lithological column along the Budurone creek, with the fossiliferous level indicated by arrow. Column to the left indicates approximate colour changes.
(when associated with diffuse layers of small, irregular calcareous concretions) to green-grey and to blackish dark grey, indicating shifting palaeoenvironmental conditions between well-drained and more poorly drained floodplain environments. Several microvertebrate bone beds have been identified around Vălioara, in the fine-grained drab-coloured, greenish silty mudstones (Grigorescu et al., 1999; Vasile, 2008). The Budurone locality, located in the bed of the homonymous creek, a small, seasonal tributary of the Vălioara Brook, is of particular interest because of its unique lithology and peculiar fossil content (Csiki et al., 2008). The Maastrichtian beds of the Budurone valley are poorly exposed because the steep valley sides are heavily vegetated; the outcrop is restricted to the narrow bed of the creek and is usually partly submerged or covered by mud. Accordingly, the observations concerning the local lithology are very patchy. Correlations with other Maastrichtian deposits near Vălioara are also impeded by the isolated location of the Budurone valley, surrounded by grass-covered hills and cultivated fields. However, it has been possible to measure a short lithological succession that includes the Budurone site (Fig. 1B). The local lithological column (Fig. 1B) is characterized by a complete lack of red-coloured deposits, suggesting locally extensive reducing conditions. The coarse-grained deposits are represented by microconglomerates that grade vertically into well-sorted medium sandstones; occasionally, coarser conglomerates also occur, but the maximum size of the ruditic clasts is smaller than observed elsewhere around Vălioara. The base of the coarser beds is usually clear-cut, often irregular, erosional; their thickness is usually less than 50 cm. Transition to the overlying finer-grained deposits is sharp, less commonly transitional. The fine-grained beds are dominantly wellsorted, massive silty mudstones and mudstones, varying in colour between grey, bluish-grey and dark blackish grey. Their thickness is greater than the coarser beds, normally surpassing 50 cm and sometimes reaching 1 m. The fossiliferous level is located in the upper part of the measured section, and is a 1-m thick bed of dark, blackish-bluish massive, micaceous silty mudstone. X-ray diffractometry suggests that the composition of the bed is dominated largely by smectitic clay minerals; the swelling character of the wetted rock is consistent with these data. The microvertebrate remains are concentrated in the upper part of the
bed, close to the erosional boundary with the overlying conglomeratic sandstones. The microvertebrate bone bed that also includes the plant fossils described here is dominated by the skeletal elements of mainly aquatic taxa (fishes, frogs, albanerpetontids), with less frequent remains of semi-aquatic (turtles, crocodilians) or purely terrestrial (lizards, dinosaurs) taxa. This abundance spectrum is unique among reported Maastrichtian microvertebrate accumulations from the Haţeg Basin, and suggests the preservation of a largely autochtonous, locally derived aquatic–peri-aquatic community (Csiki et al., 2008). Another unusual feature of the Budurone locality is the occurrence, along with the vertebrate remains, of a diverse plant mesofossil assemblage represented by a variety of small-sized plant fossils, mostly fruits and seeds, which is not yet reported from any other contemporaneous microvertebrate bone bed from Haţeg. The preservation of the plant remains was probably due to the low-energy depositional setting, supported by the sedimentary features of the host rock as well as taphonomic features of the associated vertebrate remains. It has been, however, enhanced by the highly reducing nature of the fossiliferous bed, as suggested by the presence of small, framboidal pyrite concretions and common presence of charred wood fragments; both of these are again reported only from the Budurone site. 2.2. Preparation of material The plant mesofossil was recovered when searching for microvertebrates. The sediment samples were air dried till dry, then soaked in water with a low-concentration of hydrogen peroxide until the complete break-down of the matrix. The dry sediment was then coarsely screen-washed at the site (in the river) using two mesh sizes (1.5 mm and 0.7 mm) followed by drying in the air. Subsequently, the screened material was soaked and screen-washed in the laboratory using a 1 mm, a 0.6 mm, and occasionally also a 0.35 mm screen. Matrix adhering to the surface of the fossils was removed using HF and HCl and rinsing in water. The plant mesofossils are generally well preserved and coalified. The fossils were studied and sorted into roughly similar groups using reflected light microscope. For investigation of cellular details the material was mounted on aluminium stubs with nail polish as glue, sputtercoated with gold and studied using a Hitachi S-4300 Field Emission Scanning Electron Microscope.
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All specimens were measured using reflected light microscope and SEM pictures. Typically only length (L) and breadth (B) were measured, while thickness (T) was often difficult to measure, either due to compression or difficulties in handling the specimens. Seed volumes were calculated assuming an ellipsoid shape of all seeds following Eriksson et al. (2000a) with volume V = 4/3π(ab2) where a = L/2 and b = (B + T)/4; thickness was estimated to be 0.66B. Because of the restricted material the calculations were simplified to include only one measurement (largest) for each taxon. This is justified by the fact that the size range where more than one specimen was present per taxon was small. Figures were manipulated in Photoshop to make the background evenly black. 3. Results 3.1. Organisation and systematic position of Budurone fruits and seeds The Budurone mesofossil flora comprises 19 different taxa. Fruits are mostly indehiscent, nuts or drupes, but there are also two different kinds of capsular fruits. The seeds are mainly anatropous, but one kind of seed is campylotropous. Both fruits and seeds are minute (see Section 3.2), typically with a smooth surface without elaborate ornamentation. None of the fossils can be assigned with certainty to species or genera described previously from other Cretaceous floras of Europe and most of them probably represent new taxa. The number of specimens available for each taxon is, however, small and no formal naming or description is given for any of the fossils. In the following section we describe the diversity of forms by giving an overview of the fruits and seeds identified so far. Sizes for all taxa are given in Table 1. 3.1.1. Fruits Among the small indehiscent fruits is one fruit probably related to the Normapolles complex (Taxon 1, Fig. 2A). The fruit is ellipsoidal, 1.2 mm long and 0.7 mm broad, and broadly triangular in crosssection. The fruit is most probably formed from an inferior ovary as indicated by a faint depression close to the apex that shows the extension of the hypanthium. Narrow longitudinal ridges extend from the base of the fruit to the apex of the hypanthium rim. The surface is almost smooth with faint outlines of the small, slightly longitudinally extended epidermal cells. The fossil is very similar in external morphology and structure to species of the Normapolles genus Antiquocarya, first described from
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the Late Santonian–Early Campanian flora of Åsen, southern Sweden (Friis, 1983). It also shows similarities with other members of the Normapolles complex placed systematically in the “core” Fagales (Friis et al., 2006b). Most likely this fruit is a member of this group, but the fossil does not show remains of stamens or perianth, and no Normapolles pollen was observed on the surface of the fruit. A more precise assignment of the fossil is therefore not possible with the material currently available. Two other small indehiscent fruits that may have been derived from inferior ovaries are present in the Budurone mesofossil flora. They have a thinner, almost smooth fruit wall and faint longitudinal ridges on the surface. One of them (Taxon 2, Fig. 2B) is also triangular in cross-section, while the other (Taxon 3) is rounded. Both taxa may also belong to the Normapolles complex, but they are more fragmentary and do not show features critical for an assignment to any of the Normapolles genera currently described. There are several other indehiscent fruits with a smooth sclerenchymatic fruit wall. Taxon 4 (Fig. 2C) is bilocular and is one of the largest fruits in the assemblage. It has a thick sclerenchymatic fruit wall and resembles in several respects drupes of Cornaceae. Taxon 5 is smaller, but is otherwise similar in general construction, bilocular with a thick endocarp, and probably also represents a drupe. Three other probably drupaceous fruits (Taxon 6, Taxon 7, Taxon 8, Fig. 2E–H) are unilocular with a single thin-walled seed. All these fruits had a smooth or only slightly rugulate endocarp. One fruit, however, has a distinctly pitted endocarp wall characteristic for some drupaceous fruits (e.g., in the Rosaceae, Sabiaceae and Icacinaceae). This Taxon (Taxon 9, Fig. 2I) comprises several fragments of rather large endocarp. The endocarp wall is thick, about 0.4 mm, composed of sclereid extensively pitted sclerid cells. The outer surface of the endocarp wall has several circular depressions of roughly equal size, about 0.8 mm in diameter, as well as numerous tiny perforations. The inside of the endocarp wall shows two layers, one smooth external layer and an inner layer of polygonal, slightly convex cells. Two different capsular fruits are present in the Budurone mesofossil flora. One taxon (Taxon 10, Fig. 2J) comprises five-locular capsules that are ovoid with a truncate apex. The outer layer is cracked, but shows raised papillate epidermal cells in some areas. The fruits are very similar to capsular fruits described from other Maastrichtian floras of Europe that have been included in the Ericales (Knobloch and Mai, 1986) and an ericalean affinity is also suggested for the Budurone capsules. The other capsular fruit (Taxon 11) from Budurone is more fragmentary preserved, but also five-locular. It is distinguished from the other capsular fruit by its circular outline, but is probably also of ericalean affinity.
Table 1 Fruit and seed size in the Budurone mesofossils.
Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon Taxon
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Length (mm)
Breadth (mm)
Thickness (mm)— approx
Volume mm3
1.2 1.4 2 2.6 1.1 1.5 1.9 1.3
0.70 0.40 1.00 1 0.8 1.1 1.9 1
0.462 0.264 0.660 0.660 0.528 0.726 1.900 0.660
0.21209583 0.08079841 0.72141439 0.93783871 0.25393787 0.65468356
1.5
1.5
1.500
1.76714587
0.6 0.9
0.60 0.5
0.396 0.330
0.07791275 0.08115912
0.7 1.1 1.3 0.7 1.5
0.6 0.8 1.3 0.9 1.2
0.396 0.528 0.858 0.594 0.792
0.09089821 0.25393787 0.79247371 0.20452098 0.77912754
0.46891936
EMF
V = 4/3π(ab2)
0.212095832 0.080798412 0.721414393 0.937838711 0.253937866 0.654683562 3.591364002 0.468919355 0 1.767145868 0 0.077912754 0.081159119 0 0.090898214 0.253937866 0.792473711 0.20452098 0.779127544
3.1.2. Seeds Eight different kinds of isolated seeds were observed in the Budurone mesofossil flora. All seeds are small and most of them are smooth without any special surface ornamentation. Most are anatropous, but one taxon (Taxon 12, Fig. 3A, B) is campylotropous. The campylotropous seeds (Taxon 12) are disc-shaped, flattened and with a circular to kidney-shaped outline. There is a shallow depression in the central part of each seeds. Micropyle and hilum are close together. The epidermal cells have raised anticlinal walls that give the seed surface an undulate to reticulate ornamentation. The cells are arranged in semicircular rows around the central depression. The seed wall is thick, formed mostly of the outer epidermal cells that have deep, strongly thickened anticlinal and inner periclinal walls. These seeds are very similar in shape and general construction to seeds of extant and fossil Eurya (Ternstroemiaceae: Ericales) and they are particularly similar to seeds assigned to the fossil species Eurya crassa from the Late Cretaceous of central Europe (Knobloch and Mai, 1986). None of the fossils, however, show characters of the inner walls of epidermal cells or the inside of the seed that are typically used for
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Fig. 3. Fruits from the Budurone mesofossil flora. A, B. Taxon 12, aff. Eurya crassa, campylotropous seeds (Ternstroemiaceae). C, D. Taxon 13, seeds of possible buxaceous affinity. E. Taxon 14, angular seed with papillate surface. F. Taxon 18, barrel-shaped seed with crystal cells. G, H. Taxon 17, seeds with circular to ovoid outline, a distinct groove close to the apex, and crystal cells. I. Taxon 19, aff. Klikovispermum, larger anatropous seeds. All pictures SEM.
determining fossil Eurya seeds, and with the material currently available we hesitate to place the fossil in the modern genus. Among the most characteristic seeds from Budurone mesofossil flora are small ovoid, anatropous seeds with an apical and lateral depression and a distinct incurved stalk (Taxon 13, Fig. 3C, D). The stalk has a truncate tip. The seed surface is smooth and uniform over whole specimen. The seed wall is thick and composed of small thickwalled, almost isodiametric cells with finely undulate anticlinal walls. Similar seed morphology is known for extant Buxaceae, but the seeds of extant genera in this family typically have a thinner seed wall. Two other characteristic seed types from Budurone are anatropous and have polygonal and isodiametric epidermal cells with raised periclinal wall that give the seed surface a papillate appearance. One of them (Taxon 14, Fig. 3E) has angular to spherical seeds that sometimes split open from the apex. The other (Taxon 15) has ovoid seeds with longitudinal ridges. The mesofossil flora also includes two different kinds of seeds with imprints of crystals in the epidermal cells. One of these (Taxon 17, Fig. 3G, H) has a circular to ovoid outline and a distinct groove close to the apex, the other kind (Taxon 18, Fig. 3F) is barrel-shaped with an apical depression at the micropylar area. Taxon 19 (Fig. 2I) is an anatropous seed and is the largest seed recognized in the Budurone assemblage. It is most similar to Late Cretaceous seeds assigned to the extinct genus Klikovispermum (Knobloch and Mai, 1986). This genus is a heterogeneous, probably unnatural assemblage of seeds of uncertain affinity.
3.2. Size of fruits and seeds The fruits and seeds are all very small ranging in length from about 0.6 to 2.6 mm (Table 1). The smallest seeds are the Eurya-like seeds (Taxon 12) with a diameter of about 0.6 mm and the largest seed is the Klikovispermum-like seed (Taxon 19), about 1.5 mm long and 1.2 mm broad. The smallest fruit is the Normapolles type fruit of Taxon one, about 1.2 mm long and 0.7 mm broad, and the largest entire fruit is bilocular drupaceous fruit of Taxon 4 that is about 2.6 mm long and 1.0 mm broad. One fruit type (Taxon 9) is larger, but preserved only as fragments. Based on the size and shape of the fragments this fruit would have been up to about 5 mm long. Volumes of fruits and seeds were calculated using the formula and assumptions in Eriksson et al. (2000a) (see Material and methods) resulting in the following size ranges for the Budurone flora: fruit volume: 0.08– 3.59 mm3 and seed volume: 0.08–0.79 mm3 (Table 1). 4. Discussion 4.1. Systematic assignment of the Budurone mesofossils The fossil fruits and seeds identified from the Budurone mesofossil are all of angiosperm affinity. They have been compared to other fruits and seeds described from Late Cretaceous and Palaeogene floras of Europe, but in most cases the Budurone specimens appear to represent new taxa not previously recorded for Europe. Many of the
Fig. 2. Fossil fruits from the Budurone mesofossil flora. A. Taxon 1, indehiscent fruit probably related to the Normapolles complex. B. Taxon 2, indehiscent fruit, perhaps related to the Normapolles complex. C. Taxon 4, bilocular fruit with thick sclerenchymatic fruit wall. D. Taxon 5, bilocular fruit with a thick endocarp. E. Taxon 6, unilocular drupaceous fruit with a single thin-walled seed. F. Taxon 7, unilocular drupaceous fruit with a single thin-walled seed. G, H. Taxon 8, unilocular drupaceous fruit with a single thin-walled seed. I. Taxon 9, endocarp with strongly pitted wall, fragment. J. Taxon 10, five-locular capsule probably related to Ericales. All pictures SEM.
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fruits and seeds are of very general construction. Drupaceous fruits are one or two-locular without special features that would allow a more detailed systematic assessment and a systematic assignment for the fossils was in most cases not possible. One type (Taxon 1) is most likely assignable to the Normapolles complex. The Normapolles complex is an extinct group of angiosperms that produced distinctive, mostly oblate pollen grains of triangular shape (Stemma Normapolles of Pflug, 1953). The group experienced an enormous diversification during the mid- and Late Cretaceous (Góczán et al., 1967; Batten and Christopher, 1981; Friis et al., 2006b). The plants are known mostly from their dispersed pollen grains that are collectively referred to as Normapolles. Their first appearance in the fossil record is in the midto Late Cenomanian and the latest occurrences are from the Early Oligocene. Normapolles pollen grains have now also been found in situ in fossil flowers (e.g., Friis, 1983; Friis et al., 2006b). Although a considerable diversity of Normapolles flowers are known already, systematic studies show that they all belong to extinct taxa related to the subgroup of the modern order Fagales that includes Betulaceae, Rhoipteleaceae, Juglandaceae and related families. Most of the Normapolles flowers described so far are epigynous and bisexual. The fossil fruit from Budurone was also derived from an inferior ovary, but whether it was bisexual or unisexual is unknown. The presence of Normapolles plants in the Budurone vegetation conforms with the results of previous palynological investigations that documented the occurrence of several different kinds of dispersed Normapolles pollen in palynofloras of the Haţeg Basin (Antonescu et al., 1983; Van Itterbeeck et al., 2005), and more specifically for the Budurone site itself (Csiki et al., 2008). Two other taxa (Taxon 2, Taxon 3) have features suggesting affinity with the Normapolles complex, but they are not sufficiently well preserved for a secure identification. Another systematic group that is most likely represented in the flora is the Ericales with the two capsular fruits (Taxon 10 and Taxon 11) and Eurya-like seed (Taxon 12). This is in line with our knowledge of other Late Cretaceous mesofossil floras that often include a great diversity of Ericales, and a variety of Ericales are also reported for other Maastrichtian floras of Central Europe (Knobloch and Mai, 1986). 4.2. Comparison of the Budurone mesofossil with other Late Cretaceous– Palaeogene floras Compared with other Maastrichtian or Paleocene floras the proportion of fossils that can be attributed to modern families or orders is very low. For the two rich Maastrichtian mesofossil floras from Walbeck and Eisleben, Germany, 22 modern families were reported (Knobloch and Mai, 1986). More material and a more detailed systematic work on Budurone mesofossils would most likely result in the identification of more modern taxa, but the preliminary studies do not indicate a strong systematic similarity with other contemporaneous floras. This diversity recorded in the Budurone floras is lower than that known from other fossil floras from the latest Cretaceous (e.g., Knobloch and Mai, 1986) and from the earliest Cenozoic (Mai, 1987). For example, the Eisleben flora has 48 taxa and the Walbeck flora has 67 taxa. However, these mesofossil floras are based on a much larger sample of specimens than the Budurone flora (sometimes several hundred fossils). A greater sample from Budurone would most likely yield a higher number of taxa. Despite these differences the Budurone flora does show great similarity with other Cretaceous mesofossil floras in terms of the dimension of the fruits and seeds (see below) and organisation. Both the Eisleben and Walbeck floras also show the same general composition with a diversity of seeds, nuts, drupes and capsules. Surprisingly few of the Budurone fossils can be assigned to taxa previously described from Europe, and so far only a few taxa appear to
be shared with other mesofossil floras. This may indicate that the Budurone flora was isolated from other European floras by geographical barriers, but the alternative possibility, that the Budurone locality represents a different kind of depositional environment also needs to be considered in view of the unusual co-occurrence of microvertebrate and plant remains. 4.3. Ecological signal from the Budurone plant mesofossils Most of the vertebrate fossils from the Budurone fossiliferous bed represent semi-aquatic or aquatic habitats, but distinctive wetland and aquatic taxa appear to be absent from the mesofossil flora. At least such families as Cabombaceae, Cyperaceae, Najadaceae, Nymphaeaceae, Potamogetonaceae, Sparganiaceae, and Typhaceae have not been observed. All these families are common in wetlands and lakes today. They typically have seeds and fruits that fossilize well and are easy to recognize, and they also occur abundantly in many Palaeogene and Neogene fruit and seed floras. Previous studies of seeds and fruits from the Cretaceous and Cenozoic from the mid-palaeolatitudes have shown that angiosperm fruits and seeds are generally very small in the Cretaceous, typically with a volume of about 1 mm3 and that larger fruit and seeds are not common until the Palaeogene (Tiffney, 1984; Eriksson et al., 2000a,b; Eriksson, 2008). The fruits and seeds from Budurone are all very small, ranging in length being between 0.6 and 2.6 mm (5 mm infer for Taxon 9). The calculated volumes range between 0.08 and 3.59 mm3. This corresponds well to seed and fruit volumes calculated for other fossil floras from the Cretaceous (Eriksson et al., 2000a). The other Maastrichtian mesofossil floras show a comparable size range for seeds, but fruits are generally larger. Several hypotheses have been put forward to explain the mechanism behind the radical changes in fruit and seed size from the Cretaceous to the Cenozoic (e.g., Tiffney, 1984; Eriksson et al., 2000a; Tiffney, 2004; Moles et al., 2005). One hypothesis suggested that large seeds were developed only in the Cenozoic as a response to the radiation of frugivorous vertebrates in the Palaeogene (Tiffney, 1984). Because potential dispersers, as well as fruits apparently adapted to animal dispersal, were already present in the Early Cretaceous (Eriksson et al., 2000a) it has been suggested that the distinct increase in seed and fruit sizes around the K/T boundary was more likely driven by environmental changes (Eriksson et al., 2000a; Eriksson, 2008). Specifically, the change in vegetational structure that resulted from a warm probably seasonally dry climate in the Cretaceous, which supported open vegetation, being replaced by a more humid climate, which supported closed vegetation in the Early Cenozoic, although associated changes in seed dispersing animals would have also had an impact (Eriksson, 2008). The presence of drupaceous fruits in the Budurone mesofossil assemblage indicates that some of the fossils may have had biotic dispersal, but the small nuts and seeds without specialized ornamentation suggest unassisted dispersal. This together with the small size of the fruits and seeds from the Budurone locality suggests that typical Late Cretaceous open vegetation probably growing under seasonally dry conditions was present in Europe until the very end of the Cretaceous contrasting the closed multilayered canopy forests that took over in Europe during the Early Cenozoic. 5. Conclusion The Budurone mesofossil flora is important in providing direct information of the plant community co-occurring with the rich and diverse terrestrial fauna. It is also important in providing insight into the Cretaceous vegetation in Europe immediately before the K/T boundary events. The flora comprises 19 taxa of angiosperm fruits and seeds. They are in general appearance similar to other Late Cretaceous floras from Europe, but it may be significant that there are perhaps no
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taxa or only few shared taxa with other Late Cretaceous floras from Europe. The size range of the fossils is also in accordance with other Late Cretaceous floras and indicates that open vegetation prevailed in Europe till the end of the Cretaceous. Acknowledgements We are grateful to a number of students of the University of Bucharest (and foremost to Romeo Limberea, Oana Pupaza and Stefan Vasile) for their help in collecting, processing and hand-picking the Budurone fossil material, to Yvonne Arremo, Stockholm, for help with preparation of material for SEM, as well as Peter R. Crane, Chicago, and an anonymous reviewer for helpful comments to the manuscript. We also thank the Swedish Research Council for financial support (to EMF). Grants of the Romanian Academy of Sciences (GAR 167/1997 and 39/2001 to DG) supported the discovery and early collection at the Budurone site; more recent fieldwork was supported by the National University Research Council grants 436/2007 and 1930/2009 (to ZCS). References Antonescu, E., Lupu, D., Lupu, M., 1983. Correlation palinologique du Crétacé terminal du sud — est des Monts Metaliferi et des Depressions de Haţeg et de Rusca Montană. Annuaire de l'Institute de Géologie et Géophysique 59, 71–77. Batten, D.J., Christopher, R.A., 1981. Key to recognition of Normapolles and some morphologically similar genera. Review of Palaeobotany and Palynology 35, 359–383. Csiki, Z., Ionescu, A., Grigorescu, D., 2008. The Budurone microvertebrate site from the Maastrichtian of the Haţeg Basin-Flora, fauna, taphonomy and paleoenvironment. Acta Palaeontologica Romaniae 6, 49–66. Eriksson, O., 2008. Evolution of seed size and biotic seed dispersal in angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169, 863–870. Eriksson, O., Friis, E.M., Löfgren, P., 2000a. Seed size, fruit size and dispersal spectra in angiosperms from the Early Cretaceous to the Late Tertiary. American Naturalist 156, 47–58.
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Eriksson, O., Friis, E.M., Pedersen, K.R., Crane, P.R., 2000b. Seed size and dispersal systems of Early Cretaceous angiosperms from Famalicão, Portugal. International Journal of Plant Sciences 161, 319–329. Friis, E.M., 1983. Upper Cretaceous (Senonian) floral structures of juglandalean affinity containing Normapolles pollen. Review of Palaeobotany and Palynology 39, 161–188. Friis, E.M., Pedersen, K.R., Crane, P.R., 2006a. Cretaceous angiosperm flowers: innovation and evolution in plant reproduction. Palaeogeography, Palaeoclimatology, Palaeoecology 232, 251–293. Friis, E.M., Pedersen, K.R., Schönenberger, J., 2006b. Normapolles plants: a complex of extinct fagalean lineages. Plant Systematics and Evolution 260, 107–140. Góczán, F., Groot, J.J., Krutzsch, W., Pacltová, B., 1967. Die Gattungen des “Stemma Normapolles Pflug 1953b” (Angiospermae) — Neubeschreibungen und Revision europäischer Formen (Oberkreide bis Eozän). Paläontologische Abhandlungen B 2, 427–633. Grigorescu, D., 1992. Nonmarine Cretaceous formations of Romania. In: Chen, P.-J., Matter, N.J. (Eds.), Aspects of Nonmarine Cretaceous Geology. China Ocean Press, Beijing, pp. 142–164. Grigorescu, D., 2005. Rediscovery of a “forgotten land”. The last three decades of research on the dinosaur-bearing deposits from the Hateg Basin. Acta Palaeontologica Romaniae 5, 191–204. Grigorescu, D., Venczel, M., Csiki, Z., Limberea, R., 1999. New microvertebrate fossil assemblages from the Uppermost Cretaceous of the Haţeg Basin (Romania). Geologie en Mijnbouw 78, 301–314. Knobloch, E., Mai, D.H., 1986. Monographie der Früchte und Samen in der Kreide von Mitteleuropa. Rozpravy ústredního ústavu geologickénho. Praha 47, 1–219. Mai, D.H., 1987. Neue Fruchte und Samen aus paläozänen Ablagertungen Mitteleuropas. Feddes Repertorium 98, 197–229. Moles, A.T., et al., 2005. Factors that shape seed mass evolution. Proceedings of the National Academy of Sciences 102, 10540–10544. Pflug, H.D., 1953. Zur Entstehung und Entwicklung des angiospermiden Pollen in der Erdgeschichte. Palaeontographica B 95, 60–171. Tiffney, B.H., 1984. Seed size, dispersal syndromes, and the rise of the angiosperms: evidence and hypothesis. Annals of the Missouri Botanical Garden 71, 551–576. Tiffney, B.H., 2004. Vertebrate dispersal of seed plants through time. Annual Review of Ecology and Systematics 35, 1–29. Van Itterbeeck, J., Markevich, V.S., Codrea, V., 2005. Palynostratigraphy of the Maastrichtian dinosaur- and mammal sites of the Râul Mare and Bărbat Valleys (Haţeg Basin, Romania). Geologica Carpathica 56, 137–147. Vasile, S., 2008. A new microvertebrate site from the Upper Cretaceous (Maastrichtian) deposits of the Hateg Basin. Sargetia. 21, 4–14.