A Giant Ostrich from the Lower Pleistocene Nihewan Formation of North China, with a Review of the Fossil Ostriches of China

Abstract
A large incomplete ostrich femur from the Lower Pleistocene of North China, kept at the Muséum National d’Histoire Naturelle (Paris), is described. It was found by Father Emile Licent in 1925 in the Nihewan Formation (dated at about 1.8 Ma) of Hebei Province. On the basis of the minimum circumference of the shaft, a mass of 300 kg, twice that of a modern ostrich, was obtained. The bone is remarkably robust, more so than the femur of the more recent, Late Pleistocene, Struthio anderssoni from China, and resembles in that regard Pachystruthio Kretzoi, 1954, a genus known from the Lower Pleistocene of Hungary, Georgia and the Crimea, to which the Nihewan specimen is referred, as Pachystruthio indet. This find testifies to the wide geographical distribution of very massive ostriches in the Early Pleistocene of Eurasia. The giant ostrich from Nihewan was contemporaneous with the early hominins who inhabited that region in the Early Pleistocene

Introduction
The Lower Pleistocene fossiliferous beds of the Nihewan Basin (Figure 1) in northern Hebei Province (North China) have been known for their vertebrate remains since the 1920s. More recently, abundant evidence of early human occupation has also come to light ([1], and references therein). The fossil mammals from the various formations of the Nihewan Basin have attracted considerable attention, starting with the pioneering paper by Teilhard de Chardin and Piveteau [2]. However, although bird bones have been mentioned, few of them have been described in detail, with the notable exception of a metatarsus belonging to a crow

Here we describe an ostrich femur, collected in the 1920s and kept in the paleontology collection of the Muséum National d’Histoire Naturelle (Paris, France). Although this bone is poorly preserved, a body mass estimate based on its circumference shows that it belonged to a giant ostrich, significantly larger than the living Struthio camelus. It provides new evidence of the wide geographical distribution of giant ostriches in the Early Pleistocene of Eurasia.
A note on spelling: in this paper we have used the modern pīnyīn spelling for place names. In the 1920s, a different transliteration was used by paleontologists working in China: “Nihowan” instead of Nihewan, “Sangkan Ho” instead of Sanggan He, etc.

Discovery and Geological Setting of the Specimen
Following discoveries of fossil bones by Father Vincent, a missionary based in Nihewan village (some 150 km NW of Beijing; Figure 1), in 1920 [4,5,6], the area was visited independently but almost simultaneously by the British geomorphologist George B. Barbour [7] and the French Jesuit and naturalist Emile Licent in 1924 [4]. Abundant vertebrate (mainly mammal) remains were subsequently collected from the Nihewan Basin in the course of field trips led by Licent in 1925 and Licent and Teilhard de Chardin in 1926 [6].
The first mention of an ostrich bone from the Nihewan Basin is in a section on the antiquity of the ostrich in eastern Asia in the monograph by Boule et al. [8] on the Paleolithic in China. The authors note (p. 92) that Licent has found in the “Sanmenian” [Lower Pleistocene] beds of the Sanggan He (the river which flows through the Nihewan Basin) an ostrich femur more than 340 mm in length, indicating a bird larger than the living ostrich. This brief mention seems to have attracted little attention, although it was noted by Lowe [9] and Lambrecht [10]. Later, in their study of the Nihewan mammals, Teilhard de Chardin and Piveteau [2] briefly mentioned in a footnote (p. 126) the few bird remains in their collection, viz. a humerus of a large vulture and an ostrich femur. These two bones are kept together at the MNHN, the ostrich bone bearing number NIH008. A second number, 1927–13, refers to a catalog entry briefly listing a collection of vertebrate fossils from Nihewan brought back from his second mission to China by Teilhard de Chardin on 20 November 1927. The words “Struthio” and “Femur” are written in pencil on the bone. There is therefore no doubt that the femur described below is that mentioned by Teilhard de Chardin and Piveteau in 1930. Whether it is the same bone as that mentioned by Boule et al. [8] is not so clear, because specimen MNHN–NIH008, in its present condition, is 247 mm in length, while the length provided by Boule et al. [8] is more than 340 mm. This may suggest that two distinct ostrich femora were found in the Nihewan beds in the 1920s and that one of them may have remained in China while the other was sent to Paris. However, no ostrich femur is currently kept at the Hoang Ho Pai Ho Museum in Tianjin, where Licent’s collections are kept, and there is no evidence that such a bone was part of the fossils that were transferred from the Hoang Ho Pai Ho Museum to Beijing in 1940 by Teilhard de Chardin and Leroy (see Leroy [11] about this transfer) and are now kept at the IVPP in Beijing. We therefore suppose that MNHN–NIH008 is indeed the bone mentioned by Boule et al. [8], which is no longer as complete as it was when Licent found it (probably during his 1925 collecting trip, when Teilhard de Chardin was not with him, since Licent alone is credited with the discovery), having lost a good part of the distal end.
Many vertebrate localities are currently known in the Nihewan Basin, in formations of different geological ages (see Cai et al. [12], for a recent review), and the exact place where the ostrich femur was found is unclear, all the more so given that Licent does not mention this find in his publications about his collecting trips in the Nihewan Basin ([4,13]). However, the early collections made by Licent and Teilhard de Chardin in the region were restricted to a relatively small area around the villages of Nihewan and Xiashagou (see map in Teilhard de Chardin and Piveteau

A Brief Review of the Fossil Record of Ostriches in China

The giant ostrich from the Nihewan Formation adds an Early Pleistocene link to a succession of large to very large ostriches known from Neogene and Quaternary formations in China. The earliest record of ostriches or ostrich-like birds from China seems to be eggshell fragments from two Lower Miocene localities in Inner Mongolia [27]. However, Mikhailov and Zelenkov [28] have suggested that the eggshell fragments may have been derived from more recent sediments. This suggestion is based on the fact that the eggshell fragments belong to a type which supposedly was not present in Asia at such an early date, and clearly this claim must be checked, possibly by further field observations, before the hypothesis of an erroneous dating is confirmed. The earliest skeletal remains have been referred to two more or less coeval Late Miocene species, Struthio wimani Lowe, 1931 [9] and S. linxiaensis Hou et al., 2005 [29]. The type specimen of Struthio wimani, a pelvis, was found in the so-called Hipparion red clay of the Baode area of NW Shanxi [9,30]. These highly fossiliferous deposits were traditionally referred to the Pontian, a stage once placed in the Pliocene, but are now referred to the Late Miocene [31]. Struthio linxiaensis was erected on the basis of a pelvis from the Liushu Formation (Late Miocene) of the Linxia Basin in Gansu Province [29]. Since both taxa appear to be of roughly the same geological age, it may be wondered whether they should really be considered as separate species, a point already made by Mikhailov and Zelenkov [28]. However that may be, both have been described as being larger than the living Struthio camelus. Ostrich eggshell remains from the Late Miocene (“Hipparion fauna”) of Shanxi and Gansu, many of them collected by Emile Licent, were reported by Andersson [30]. Lowe [9] referred these Miocene eggshell fragments to Struthio wimani.
Next in age is the Pachystruthio femur from the Lower Pleistocene Nihewan Formation described in the present paper. Eggshell remains have been reported from various anthropic sites in the Nihewan Basin (see below).
The Late Pleistocene species Struthio anderssoni was originally described by Lowe [9] on the basis of large eggs from many localities in the loess of northern China [30]. Many more eggs from the loess referrable to S. anderssoni have subsequently been reported (e.g., [32,33]). The name was later applied to skeletal remains (femora) from the Upper Cave at Zhoukoudian [17,18,34,35], for which dates ranging from 35.1 to 33.5 ky are available [36]. Eggshell fragments are known from several of the karstic localities at Zhoukoudian, of various geological ages, some being significantly older than the Upper Cave [32,35,37]. A discussion of the stratigraphic distribution of Struthiolithus eggshells in the loess of China and of the validity of applying the egg-based taxon Struthio anderssoni to skeletal remains is beyond the scope of this paper. It may be mentioned that mass estimates based on eggs referred to Struthio anderssoni and on a femur from the Upper Cave yield very similar results, viz. about 270 kg [16]. Both the eggs and the few skeletal remains thus indicate an ostrich significantly larger than the living one.
On the basis of C14 dates, Janz et al. [38] have suggested that ostriches survived in north-eastern Asia, including China, until the Holocene. This is in agreement with the suggestion by Kurochkin et al. [39], based on C14 dates from eggshell fragments, that they may have become extinct in the Holocene in Mongolia and Siberia. However, Khatsenovich et al. [40] have urged caution about dates obtained from ostrich eggshell, a material that poses special problems (including different ages for the outside and the inside of the shell) and which in some instances provides ages that are significantly younger than those obtained from bones from the same sites.
The available fossil record thus suggests that the ostrich has been present in China possibly from the Early Miocene to the Late Pleistocene, a time span covering some 20 My. Because of the scarcity of skeletal material (as opposed to the abundance of eggshell remains), it is difficult to reconstruct the evolution of ostriches in that part of the world and the relationships between the several species that have been described are unclear. The fact that these fossil ostriches were larger than the living species seems to be well established, and the form from the Nihewan Formation may have been the most massive of them all