Brachiopods from the Silberberg Formation (Late Eocene to Early Oligocene) of Atzendorf, Central Germany

Six brachiopod species, i.e., Discradisca sp., Cryptopora sp., Pliothyrina sp. cf. P. grandis (Blumenbach, 1803), Terebratulina tenuistriata (Leymerie, 1846), Rhynchonellopsis nysti (Bosquet, 1862), and Orthothyris pectinoides (von Koenen, 1894), have been identified in the Late Eocene to Early Oligocene Silberberg Formation of Atzendorf, Central Germany. The species R. nysti and O. pectinoides dominate the studied assemblage. Rhynchonellopsis is here transferred from the family Cancellothyrididae to Chlidonophoridae because it has a loop without united crural processes. Orthothyris pectinoides has a brachial skeleton of chlidonophorid type, but its transverse band is incomplete. In species composition, the assemblage from Atzendorf differs from other Paleogene and Neogene European assemblages by the absence of megathyridids and dominance of chlidonophorids, indicating a relatively deep environment.


Introduction
Oligocene brachiopods of Europe, unlike the Eocene and Miocene ones, are still poorly known. Their presence was mentioned in several older papers (e.g., Bosquet 1862;Sandberger 1862Sandberger -1863Vincent 1893Vincent , 1923Sacco 1902;Fabiani 1913;Venzo 1941;Meznerics 1944;Mandruzzato 1970;Nebelsick et al. 2011), but in modern taxonomy they have been so far described only from the Lower Oligocene of Germany (Bitner and Kroh 2011), and from the Upper Oligocene of Austria (Radwańska and Radwański 1989) and France . Recently, a rich assemblage of Oligocene brachiopods, comprising nine genera, was briefly reported from Hungary by Dulai (2010).
The aim of this paper is to describe a brachiopod fauna from the Late Eocene to Early Oligocene Silberberg Formation at Atzendorf, Central Germany. The investigated material, very rich in specimens, allowed examination of the hitherto unknown internal structures of Rhynchonellopsis nysti (Bosquet, 1862) and Orthothyris pectinoides (von Koenen, 1894), and thus to evaluate their systematic position. Some paleoecological and paleobiogeographical aspects are also discussed.

Geological setting
Atzendorf is situated in Central Germany, about 100 km northwest of Leipzig ( Fig. 1), and the specimens were collected from a huge, abandoned gravel pit which was recently investigated in detail by Müller et al. (2014). Paleogeographically this locality is situated on the southeastern margin of the North Sea Basin. The brachiopod-bearing deposits of the Silberberg Formation, which crop out in the Atzendorf gravel pit, lie unconformably on Lower Eocene sands and are overlain by thick Pleistocene gravels (Fig. 2). The Silberberg Formation is represented by clayey and silty deposits with a rich and diverse fauna of sponges, corals, bivalves, gastropods, brachiopods, bryozoans, echinoderms, and fishes, and is interpreted as representing a deep neritic environment (Müller et al. 2014). The formation comprises two parasequences, the lower Marbe and the upper Atzendorf Subformations. Although still under discussion, the age of this formation is considered to be uppermost Priabonian (Late Eocene) and lowermost Rupelian (Early Oligocene).

Materials and methods
All the investigated material was collected at Atzendorf, Central Germany (Fig. 1). The gravel pit was intensively sampled between 2008 and 2010 after exploitation of the Pleistocene gravel ended. The brachiopods come from bulk samples, each of 1.5 kg dry sediment, taken each 15 cm in the seven mining dug holes, and washed in the laboratory on a 0.4-mm mesh. In addition, a few larger samples were taken at intervals of 90 cm. For details of sampling see Müller et al. (2014).
Brachiopods were found in 97 of 120 samples, which contained from 1 to 652 specimens and a total of 3103 specimens. Although most specimens are excellently preserved, there are also many damaged and/or fragmented specimens. Biodiversity indices and rarefraction were calculated using the paleontological statistics software PAST (Hammer et al. 2001).
Specimens selected for scanning electron microscopy were mounted on stubs, coated with platinum, and examined using a Philips XL-20 microscope at the Institute of Paleobiology, Warszawa. The specimens described here are housed at the University of Leipzig, Germany under catalogue numbers AZ_0686-AZ_0738.

Systematic part
Phylum Brachiopoda Duméril, 1805Subphylum Linguliformea Williams, Carlson, Brunton, Holmer, and Popov, 1996Class Lingulata Gorjansky and Popov, 1985Order Lingulida Waagen, 1885 Superfamily Discinoidea Gray, 1840  Remarks The material, very limited and poorly preserved, resembles Discinisca, but ribbed ornamentation indicates its attribution to the related genus Discradisca (see discussion in Dulai 2013). The shell is thin and very small. Its postlarval (brephic) part ( Fig. 3a) is smooth with numerous growth lines. The adult (neatic) shell (Fig. 3b) is covered with fine, tuberculate ribs which increase in number by intercalation. Apart from the ribs, the surface is also ornamented by numerous radial microlines (Fig. 3c). In the character of ribs and microornamentation, the studied specimens resemble Discradisca multiradiata (de Morgan, 1915) from the Miocene of France Dulai 2013); however, the present material prevents any conclusions.
Occurrence Silberberg Formation, Atzendorf, Germany. Several species of Discradisca have been reported from the Paleogene and Neogene deposits of Europe (see Dulai 2013). Today, Discradisca lives in all oceans Bitner 2010Bitner , 2014.

Figure 3d
Material One complete specimen of a young individual.
Remarks The very limited material, i.e., one juvenile individual, prevents identification to species level, but it shows all characters typical of Cryptopora. The shell is very small, thin, and translucent, weakly biconvex with a smooth surface. The beak is high with a large, triangular, hypothyrid foramen flanked by very narrow, slightly raised deltidial plates. The specimen was found in the lower part of the section interpreted as uppermost Priabonian (Upper Eocene), thus this is the first record of Cryptopora from the Eocene of Europe. From the Oligocene of Europe, a doubtful Cryptopora is reported from Alsace; based on description and figures, Muir-Wood (1959) attributed the specimens described as Terebratula (Megerlea) haasi Andreae, 1884 from the Oligocene of Lobsann to the genus Cryptopora.
Occurrence Silberberg Formation, Atzendorf, Germany. The genus Cryptopora is known from the Danian to the Recent, but in the Eocene and Oligocene it is very rare (Andreae 1884;Toulmin 1940;Bitner and Cahuzac 2004   e-h Pliothyrina sp. cf. P. grandis (Blumenbach 1803), Atzendorf; e, f inner view of dorsal valve and enlargement (f) to show mosaic of secondary fibers crossed by punctae, no. AZ_0689; g, h inner view of ventral valve and enlargement (h) of umbonal part to show details of teeth, deltidial plates, and pedicle collar, no. AZ_0690. All SEM Dimensions Length 6.2 mm, width 5.1 mm (AZ_0690). Remarks The investigated specimens are most probably juvenile representatives of Pliothyrina grandis, the only short-looped terebratulide reported so far from the Oligocene of Northern Europe (Davidson 1874;Vincent 1886;von Koenen 1894;Cooper 1983;Müller 2011a;Diedrich 2012). The shell is elongate oval with smooth surface and rectimarginate anterior commissure. The foramen is subcircular, mesothyrid with disjunct deltidial plates. The ventral valve has short, excavate pedicle collar and small, hooked teeth (Fig. 3h). In the dorsal valve, the cardinal process is well developed, semielliptical. The inner socket ridges are long but low; dental sockets are shallow. The loop and crura are not preserved. The shell is composed of two layers, primary and fibrous secondary (Fig. 3f); twolayered shell is characteristic for all species of Pliothyrina (see van Roy 1980). Although usually the shell of articulate brachiopods is built of primary and secondary layers, in the majority of short-looped, smooth terebratulides it is composed of three layers (see MacKinnon and Williams 1974;Bitner 2007Bitner , 2014. Occurrence Silberberg Formation, Atzendorf, Germany. The genus Pliothyrina is restricted to Northern Europe, being recorded from the Oligocene to Pliocene (Cooper 1983).
Superfamily Cancellothyridoidea Thomson, 1926 Family Cancellothyrididae Thomson, 1926 Subfamily Cancellothyridinae Thomson, 1926 Genus Terebratulina d 'Orbigny, 1847 Type species Anomia retusa Linnaeus, 1758 Terebratulina tenuistriata (Leymerie, 1846)   Description Shell small (maximum observed length 6.2 mm), thick, biconvex in young to strongly dorsibiconvex in adults; ventral valve nearly flat (Fig. 6g, j). Shell outline variable from rounded to elongate oval with maximum width at or nearly mid-length (Fig. 6). Shell surface covered with numerous (up to 44) beaded tuberculate ribs which increase in number by bifurcation and intercalation; in young individuals ribs are single (Fig. 6a). Lateral commissure straight, anterior commissure rectimarginate to gently uniplicate (Fig. 6h, k). Hinge line very narrow,  curved. Beak short, suberect; foramen small, oval, bordered by two small, triangular, disjunct deltidial plates. Ventral valve interior with wide pedicle collar close to the valve floor (Fig. 7b, d, g). Teeth small, hooked, with swollen bases. Very low ridge present. Dorsal valve interior with prominent inner socket ridges projecting beyond hinge line, united with cardinal process and crural bases (Fig. 7i). Hinge plates absent. Crura short but massive and converging medially (Fig. 7i, j). Crural processes blunt and short, not united. Loop short with subparallel descending branches and a horizontal to slightly inclined posterodorsally transverse band (Fig. 7j-m). Inner shell margin of both valves strongly crenulated (Fig. 7c, e, f, h).
Remarks Rhynchonellopsis nysti is the commonest species (more than 1800 specimens) in the assemblage under study, and its internal structure has been investigated for the first time. Originally this species was described based on a single ventral valve from Belgium (wrongly interpreted as a dorsal one), by Bosquet (1862) as Terebratulina nysti. Later Vincent (1893) proposed for this species a subgenus Rhynchonellopsis, created by himself. Having only crura preserved, Vincent (1893) offered a loop reconstruction adding a ring that became the basis for attribution of R. nysti to the Cancellothyrididae. However, in the Cancellothyrididae the crural processes are united and, together with a transverse band, form a ring, whereas in Rhynchonellopsis the crural processes are seen to be not united, as in the Chlidonophoridae (Lee et al. 2006). Thus, this genus should be transferred into the latter family.
Rhynchonellopsis nysti was also reported from the Upper Eocene of Ukraine by Zelinskaya (1962Zelinskaya ( , 1975; however, the description clearly negates the attribution of these specimens to R. nysti because the dorsal valve is flat whereas in R. nysti the dorsal valve is strongly convex. Also based on the illustrations it is not possible to confirm the attribution to R. nysti; the figures can represent any cancellothyridoid (see pl. 6, figs. 5, 6 in Zelinskaya 1962, andpl. 12, figs. 10-12 in Zelinskaya 1975).
Inner commissure margin of both valves crenulated (Fig. 10d, g, h). Fibers of secondary layer readily visible on inner surface; punctae (Fig. 10k) arranged in rows associated with the rib region, a feature characteristic for Cancellothyridoidea.
Remarks Orthothyris pectinoides is one of the commonest species (more than 1000 specimens) in the investigated material. The specimens from Atzendorf correspond well to those hitherto described (e.g., Bitner and Dieni 2005;Bitner and Dulai 2008;Dulai 2011), being, however, larger. The specimens from the Early Eocene of Austria described by Dulai et al. (2010) as Argyrotheca sabandensis? (Pajaud and Plaziat, 1972) clearly belong to O. pectinoides, fitting well within the variability range of this species. In addition, the specimens from Austria possess tuberculate ribs, a feature not observed in Argyrotheca.
Occurrence Silberberg Formation, Atzendorf, Germany. This species is widely distributed in the Eocene of Europe, being also reported from the United Arab Emirates (see Fig. 3 in Bitner and Boukhary 2012). In the Oligocene it is noted from Germany. Dulai (2010) mentioned Orthothyris? sp. from the Oligocene of Hungary.

Discussion
The brachiopod fauna collected from the Late Eocene to Early Oligocene deposits at Atzendorf, Central Germany ( Fig. 1) is rich in individuals but of low diversity, containing six species belonging to six genera. Nevertheless, the rarefaction curve (Fig. 11), used to test the effect of sample size upon taxon counts, begins to flatten off, suggesting that further sampling would not substantially increase the number of taxa. Diversity indices show low diversity (Shannon index = 0.82) and medium dominance (Simpson D index = 0.51).
Lingulids and rhynchonellides are represented by one species each, Discradisca sp. and Cryptopora sp., respectively. The terebratulides have four representatives: shortlooped terebratuloid Pliothyrina sp. and three members of the superfamily Cancellothyridoidea, Terebratulina tenuistriata, Rhynchonellopsis nysti, and Orthothyris pectinoides. The two latter species dominate the assemblage, constituting 96 % of the material. Rhynchonellopsis nysti has long been considered as restricted to the Oligocene of the North Sea Basin, but the present finds extend its stratigraphical range to the Upper Eocene. However, the age of the deposits cropping out at Atzendorf is still under discussion (Müller et al. 2014). On the other hand, T. tenuistriata and O. pectinoides belong to the commonest species in the Eocene of Europe; from the Lower Oligocene they are reported from Northern Germany only.
The total absence of megathyridids (i.e., Megathiris, Argyrotheca, Joania), which are usually either common or dominant in other Paleogene and Neogene assemblages of Europe, makes the assemblage from Atzendorf clearly different. Today, megathyridids are commonest in shallowwater environments, preferring cryptic habitats such as overhangs, crevices, and caves (Logan 1975(Logan , 1979Á lvarez and Emig 2005), whereas the clayey deposits at Atzendorf may be interpreted as an originally soft sea bottom. The dominance of Chlidonophoridae, whose extant representatives are deep-water brachiopods (Logan 2007), indicates a deeper environment and supports previous interpretations of the Silberberg Formation (Müller 2011b;Müller et al. 2014).
All brachiopod species recognized in the Atzendorf assemblage have a functional pedicle opening, indicating that they lived attached to the hard substrate. The fauna, dominated by micromorphic species, is very similar to one described by Surlyk (1972) from the Upper Cretaceous white chalk facies. Surlyk (1972) suggested that small size may be considered as an adaptation to the availability of numerous but small hard substrates on a generally soft sea bottom. It is worth mentioning that the larger brachiopod, Pliothyrina sp., is rare and represented only by young individuals.
Traces of gastropod predation are extremely rare (Fig. 12); among 3103 specimens examined 26 (0.84 %) specimens were drilled. Such low predation intensity is a characteristic feature in Cenozoic brachiopod populations where molluscs, being more preferable food for gastropods,  Table 1), but any apparent taxonomic selectivity can be explained by the dominance of those two species. Drill holes were found on both valves of R. nysti but with a preference for the dorsal valve (see Table 1). The boreholes are small (0.23-0.55 mm), rounded in outline and cylindrical (Fig. 12), corresponding to those made by extant muricids.  (Bosquet, 1862); e, f dorsal valves, no. AZ_0726, AZ_0727; g, h dorsal valve and a close-up image of drill hole (h), no. AZ_0728; i ventral valve, no. AZ_0729. All SEM were investigated for the first time. Rhynchonellopsis nysti possesses a loop with disjunct crural processes and therefore has been transferred from the family Cancellothyrididae to the family Chlidonophoridae.
Orthothyris pectinoides also has a loop of chlidonophorid type with an incomplete transverse band. 3. The dominance of chlidonophorid brachiopods and absence of megathyridids indicate a deeper-water environment. 4. Gastropod predation intensity on brachiopods is very low; drillings were observed on fewer than 1 % of specimens.