Wednesday 7 December 2022

Fossil eggshells from the Early Cretaceous Okurodani Formation of Gifu Prefecture, Japan.

The past three decades have seen the discovery of a large quantity of fossil eggs from several Lower Cretaceous deposits in Japan, notably the Yezo Group of Hokkaido, the Kuwajima Formation of Ishikawa Prefecture, and the Ohyamashimo Formation in Hyōgo Prefecture. These include eggs which are thought to have come from Ornithopod and Theropod Dinosaurs (including Oviraptosaurs, Troodontids, and Birds). These findings add to the known palaeobiodiversity of these areas, by indicating the presence of groups not known from the skeltal fossil record. However, the majority are of Aptian or Albian age (121.4-100.5 million years old), with earlier examples being much rarer.

The Okurodani Formation outcrops in the Shokawa area of northwestern Gifu Prefecture, and is considered to be of Hauterivian age (i.e. between 132.9 and 129.4 million years old). This formation has produced a variety of Vertebrate remains, including Dinosaurs, aquatic Tetrapods and Fish, as well as a number of fragmentary egg pieces, which have been assumed to have been of Dinosaurian origin, but never formally investigated.

In a paper published in the journal Historical Biology on 24 November 2022, Rina Uematsu of the Graduate School of Science and Technology at the University of TsukubaKohei Tanaka of the Faculty of Life and Environmental Sciences at the University of Tsukuba, Shohei Kozu of the Gifu Prefectural Museum, Shinji Isaji of the Natural History Museum and Institute of Chiba, and Shizuo Shimojima of Takayama City, describe the known egg material from the Okurodani Formation, and discuss the implications this has for the known biodiversity of the environment which produced these strata.

All the fossils examined in the study were collected between 1988 and 2009 by Shizuo Shimojima, Masatoshi Okura and Satoru Sakamoto, from the Okurodani Formation, a 220 m thick sequence of shale, alternating sandstone and mudstone, and sandstone beds, which forms part of the Itoshiro Subgroup of the Middle Jurassic to Lower Cretaceous Tetori Group, which has been dated to between 133 and 129 million years old, based upon uranium-lead dates obtained from layers of volcanic tuff within the formation.

Map of the eggshell locality. (A) Distribution of the Tetori Group in Japan formed of three subgroups. (B) Stratigraphic position of the Okurodani Formation in the Shokawa area. (C) Detail of the boxed area in (A), showing the distribution and the stratigraphic sequence of the Okurodani Formation with the locations where eggshell materials were collected. GPM-Fo-1923, 09/Cr/89/01 and 09/Cr/88/07 were found in debris of fallen rocks and their location is not specified in the stratigraphy. Uematsu et al. (2022).

Sevem fragments of eggshell and two eggshell impressions were found within black mudstone layers within the Okurodani Formation. These mudstone layers are also rich in Plant fossils and freshwater Molluscs, and are interpretted as having been laid down in a network of stagnant pools or oxbow lakes within a floodplain environment. Vertebrate remains, predominantly Fish scales and Turtle shells, but also including Frogs, small Lizards, and Choristoderes (Crocodile-like Diapsids of uncertain affinities) are typically preserved in three dimensions (i.e. not compressed),  which implies rapid burial with minimal movement. Dinosaur fossils are rare in these layers, but the teeth of Ornithopods, Sauropods, and Verociraptorines have been found, as well as the tarsometatarsus of an Enantiornithine Bird.

The first two eggshell fragments discussed, GPM-Fo-1923 and 09/Cr/89/01, are assigned to the Oofamily Testudoolithidae (i.e. Turtle Eggs). These fragments are approximately 5 x 6 mm and 3 x 3 mm, respectively, and are assumed to have come from the same egg, based upon cross-sections of the joint and the overall  shape of the fragments when jointed. However their precise origin is unclear, because they were collected by Masatoshi Okura, who has since passed away, and are now housed in separate museums. The outer surfaces of both shells are strongly abraded and show nodular patterns composed of tightly packed shell units. Based upon the curvature of the eggshell, the original egg would have been about 22 mm in diameter.

Eggshell assigned to Testudoolithidae. (GPM-Fo-1923). (A) Nodular outer surface with exposed shell units. (B) Radial thin section under normal light, showing discrete shell units (bracket), tubular pore canals (white arrowheads) and cratered bases (black arrowhead). The shell appears two-layered with an undulating boundary (arrow). (C) The same view as (B) under polarised light, exhibiting irregular extinction patterns. (D) Radial view, scanning electron microscope, showing discrete shell units (bracket) with ill-preserved ultrastructure. Uematsu et al. (2022).

These shells show two separate layers, separated by an undulating horizontal boundary. In the upper layer, needle-like crystals radiate outward from the boundary. Although less prominent, such acicular crystals are also found in the lower layer; the crystals develop concentrically from the organic cores, making the basal parts of the shell units rounded in shape. Under polarised light, the eggshell exhibits irregular extinction patterns. 

Turtle eggs typically have only a single layer, so the structure of the these eggshells, with two distinct layers, each with a different type of crystals, is distinctly unTestudine. Apparently double-layered Turtle eggshells can be produced taphonomically, by when two shell fragments happen to come to rest with one sitting inside the other, or as a result of a pathology - gravid female Turtles, suffering from some king of environmental stress, can retain eggs instead of laying them, depositing additional layers of minerals on the surface of the egg during the process. Neither of these appears to be the case in this instance, rather the eggs appear to have been altered diagenetically, with the outer portion of the shell having been recrystalised as a result of contact with external chemistry.

Based upon the morphology of these eggshell fragments, it is estimated that they were laid by a small Cryptodiran Turtle, with a carapace length of less than 200 mm.

The next five specimens, GPM-Fo-1294, 1295, 1296, 1297, and 1298 are placed within the Oofamily Prismatoolithidae, which is typified by a two-layered structure and an ornamented shell surface. They are assigned to a new oospecies, with GPM-Fo-1925 as the holotype, and given the name Ramoprismatoolithus okurai, where 'Ramoprismatoolithus' derives from 'Ramo-' from the Latin 'ramus', meaning branch, plus '-prismatoolithus', from the oofamily name, in reference to the reticulate ridges on the other surface of the eggshell, and 'okurai', honours the late Masatoshi Okura who pioneered the discovery of fossil eggshells and other Vertebrate remains in Shokawa.

All of these specimens are fragmentary; no intact examples of this new oospecies are known. The outer surface of these shells is distinctly sculpted, with low ridges arranged in elaborate reticulated patterns. The shells range from 0.31 to 0.61 mm in thickness, with the average being 0.46 mm. Seen under a scanning electron microscope, a near-vertical, unbranching, pore canal could be observed, increasing slightly in width towards the surface of the egg.

Ramoprismatoolithus. (A), (B) Eggshell outer surfaces showing the well-sculpted reticulation: (A) holotype: GPM-Fo-1925 and (B) a cast of GPM-Fo-1924 made of  silicone rubber. (C) Radial thin section under normal light, showing a mammillary layer (ML) and a prismatic layer (PL) with a gradual boundary (horizontal bar on the left side) (holotype: GPM-Fo-1925). (D) the same view as (C) under PLM, showing columnar extinction patterns. (E)–(G) Radial view under Scanning Electron Microscope (holotype: GPM-Fo-1925), displaying (E) ML and PL, (F) numerous vesicles (arrowhead) over the eggshell and (G) acicular crystals at the base of mammillae. (H) Straight pore canal under Scanning Electron Microscope (GPM￾Fo-1928). Uematsu et al. (2022).

These eggshells show two layers, which appears to be an original feature rather than something produced by diagenetic alteration, with a lower mammillary layer (the inner layer of many eggs, which is made up of small calcium carbonate crystals, which are easily disolved and provide a source of calcium for the growing embryo) and the upper prismatic layer (made up of larger crystals, which provides structural strength to the egg) observable. These are separated by a gradual boundary. The mammillary layer makes up about one fifth to one sixth of the shell's thickness, and is comprised of  acicular crystals radiating from what were presumably organic cores. The base of this layer is abraded, probably due to absorption of calcium by the growing embryo. The prismatic layer is made up of narrow, columnular crystals, visible under polarised light. Vesicles can be seen in this layer under the scanning electron microscope.

Based upon the thickness of the shell fragments, the original Ramoprismatoolithus okurai eggs are calculated to have had an average mass of 99.39 g, which assuming an egg twice as long as it is wide, would give an original size of about 57 x 133 mm.

Prismatoolithid eggs are generally accepted to have been laid by Troodontid Dinosaurs, as intact eggs assigned to the oofamily have been found with Troodontid embryos inside. However, it has been suggested that some eggs assigned to this oofamily might have been laid by early Birds.

The small estimated size of the Ramoprismatoolithus okurai eggs leads Uematsu et al. to conclude the Animal which laid them weighed somewhere between twelve and seventeen kilograms, small for a Theropod Dinosaur, but not implausible for a non-Avian Maniraptoran.

The final two specimens described are GPM-Fo-1929, an impression of part of an outer eggshell surface measuring 6 × 7 mm, and 09/Cr/88/07, a possible impression of part of an inner eggshell surface, measuring 2 x 2 mm. Neither of these specimens preserves any of the original eggshell material. The outer surface impression GPM-Fo-1929 bears a strong resemblance to the outer surface of the Ramoprismatoolithus okurai egg fragments, with reticulate ornamentation and the remains of several pore openings. The inner shell fragment impression, 09/Cr/88/07, is smooth, with no discerning features which would allow it to be associated with any known egg fossil.

Indeterminate eggshell impressions. (A) Outer surface impression (GPM-Fo-1929). (B) Cast of (A) made of silicone rubber, showing reticulate ornamentation similar to Ramoprismatoolithus and remains of pore openings (arrowheads) between the ridges. (C) Inner? surface impression with a smooth appearance (09/Cr/88/07). Uematsu et al. (2022).

The specimens described by Uematsu et al. are the oldest known fossil eggshells from Japan, and provide additional information on biodiversity within the Early Cretaceous Tetori Group, within which skeletal material is scarce, demonstrating that Turtles and small Dinosaurs were nesting in the area. 

The eggs assigned to Ramoprismatoolithus okurai are likely to have been laid by a Troodontid, or closely related Maniraptoran Theropod. Okurodani Formation yields teeth of possible Velociraptorinae, and other strata within the Tetori Group (likely to be roughly co-eval, but laid down in different environments within the same landscape) have produced possible Oviraptorosauria and Dromaeosauridae, as well as the Therizinosaur-related Fukuivenator paradoxus. However, all of these groups are known to produce non-prismatic shells with microstructures unlike that of the Oofamily Prismatoolithidae. This strongly suggests that the Ramoprismatoolithus okurai eggs were produced by a small Maniraptoran Theropod not represented in the skeletal fossil record of the Tetori Group. 

Troodontids, and basal Paravians (the group that includes Troodontids, Birds, and Dromaeosaurs) in general are scarce in Early Cretaceous deposits, both as skeletal and egg remains. Examples are known from the US, Spain, and China, and all Early Cretaceous small non-Avian Theropods known from East Asia come from two formations in northeastern China, the Yixian and Huajiying. Thus the discovery of the Ramoprismatoolithus okurai eggs in Japan is a significant contribution to our understanding of the distribution of mall non-Avian Theropods from the early Early Cretaceous of East Asia.

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