The evolution of Nyctereutes (Carnivora: Canidae) in the Nihewan Basin, Hebei, northern China
Introduction
Nyctereutes first appeared during late Miocene in both China and Europe, it became one of the most common taxa and widely distributed in Eurasia and Northern Africa (Geraads, 2008). Although Nyctereutes species are not characterized as specialized carnivorous, their invasive traits and tolerance toward dietary changes are likely to affect the populations of other small mammals. During the Plio-Pleistocene transition the more advanced and larger forms such as Nyctereutes megamastoides and N. vulpinus appeared in Europe, N. abdesalami and N. lockwoodi in Africa and N. sinensis in East Asia (Tedford and Qiu, 1991; Geraads, 1997, 2008), showing a flourishing diversity. In the mid-Pleistocene, concurrent with rapid global climatic changes, Nyctereutes permanently retreated from Europe and North Africa, and are nowadays uniquely habituated in East Asia (natural distribution).
Nyctereutes is an opportunistic carnivore, mainly feeds on insects, small mammals, fish, birds, and plants, such as roots. Although it is well established that the geomorphological and environmental factors and seasonal changes widely influence the diet composition of this genus (Sutor et al., 2010), interactions between some small carnivorous and modern N. procyonoides consist of facilitative and competitive components, and their net effect varies seasonally (Kowalczyk et al., 2008). This reliance or coexistence with other Canidae is an essential parameter in studying the Nyctereutes extinct species, which may explain their extinction through the long glacial and interglacial periods. The omnivore or hypercarnivore diet of Nyctereutes, in comparison to other canids, is reflected in more generalized teeth and their habitats.
Biomorphologically, this genus is recognizable by a short snout, rounded cranium as well as their molar morphology. The length to width ratio of upper premolar and the size ratio between M1 and M2 of this species are notably higher and its molar is more rounded than that of other Canidae. The infraorbital foramen of Nyctereutes is closer to the orbit in comparison with other Canidae such as Vulpes vulpes. The unique presence of the subangular lobe in the mandible is much stronger than wild jackals or red fox beside the orientation of the ascending ramus, which is almost 90° among the fossil Nyctereutes (Reynolds, 2012).
Northern China has always been appreciated for its abundant depositions with fossils. The Nihewan Basin in Hebei province holds numerous important Plio-Pleistocene fossil sites (Fig. 1). The Nyctereutes fossils from the basin had been discovered in different localities of the Xiashagou and Dongyaozitou sections ranging from the late Pliocene to middle Pleistocene. In 1903, Schlosser studied some Chinese fossil raccoon dogs for the first time. Although, by describing fossil fragments obtained from pharmacies collected as ‘dragon bones’ for medicinal use, he recognized some materials as Vulpes sinensis (Schlooser, 1903). Later, Teilhard de Chardin and Piveteau demonstrated that V. sinensis should be referred to the genus Nyctereutes, based on fossil skulls from the Nihewan Basin collected by E. Licent (Teilhard de Chardin and Piveteau, 1930). Since then, Nyctereutes materials have been reported from many sites across China, such as the middle Pleistocene Zhoukoudian localities near Beijing, Pliocene localities from the Yushe Basin in Shanxi Province etc. (Pei, 1934; Tedford and Qiu, 1991). Till now, the earliest occurrences of Nyctereutes in northern China are the Pliocene form N. tingi from the Yushe Basin.
The abundance of the Plio-Pleistocene record of Chinese raccoon dogs and its diversity are comparable to the European counterparts, such as N. donnezani and N. megamastoides. Although, in contrast with European N. donnezani and its successor N. megamastoides, the Plio-Pleistocene coexistence of N. sinensis and N. tingi in the Nihewan Basin is widely accepted. Hence, the evolutionary history of Nyctereutes in eastern Asia, as revealed by the Chinese record shows the abrupt appearance of primitive (N. tingi) and derived taxa (N. sinensis) in the early Pliocene, the local extinction of the former by the late Pliocene and the loss of the latter either by extinction or evolution to N. procyonoides in middle Pleistocene (Tedford and Qiu, 1991).
The study of fossil records of the Nyctereutes in Asia is crucial due to the continuous occurrence of these species in the area. Unlike any other place in the world, the sequential presence of N. tingi, and N. sinensis leads to the appearance of modern N. procyonoides in the mid-Pleistocene. To understand the course of events that leads to the appearance of N. procyonoides, we investigated their ancestry throughout the Nihewan Basin. Hence, our study focused on three primary bases: 1. To determine the exact age of N. tingi and N. sinensis in the Nihewan Basin; 2. To investigate the paleo-biodiversity of Nyctereutes in the Nihewan Basin by exploring their molar morphometry; 3. To reconstruct their dietary changes throughout the Plio-Pleistocene based on their lower molar ratio.
The mammalian fossils from Nihewan were initially discovered by Licent and Teilhard de Chardin in 1925–1929. However, they failed to log the fossil localities in a stratigraphical scheme, and clumped all the fossils in the Nihewan (Nihowan) fauna, proposing that they are from the same horizon. During the summer fieldwork of 2017–2019, we managed to relocate most of the original sites found by E. Licent. We correlated our new lithostratigraphic profile with the latest magnetostratigraphic data of the Xiashagou section to estimate numerical age for different localities (Fig. 2). By recognizing five different horizons that produced N. sinensis, we estimate the first appearance of this species at around 2.3 Ma ago, while the youngest specimen recorded at ∼2.1 Ma ago (Appendix C).
Section snippets
Abbreviation:
Institute of Vertebrate Paleontology and Paleoanthropology of China (IVPP), Xiashagou (XSG), Danangou (DNG), Zhoukoudian (ZKD), Xujiayao (XJY), Dongyaozitou (DYZ), Shixiali (SXL). Canine length (CL), Canine width (CW), first upper premolar length (P1L), first upper premolar width (P1W), first upper molar length (M1L), first upper molar width (M1W), first lower premolar length (p1L), first lower premolar width (p1W), first lower molar length (m1L), first lower molar width (m1W).
Stratigraphy of the region
The thick exposure of sediments accumulated on the east bank of Huliuhe River, which is the eastern part of the Nihewan basin, was initially studied in 1924–1925 by Barbour (Barbour, 1924, 1925; Barbour et al., 1926). He divided the sediments in the into four groups and discussed on their properties and origin. During 1960s–1970s, studies resumed by Chinese pioneers, and resulted in more than 20 sites and subsequently the introduction of the following four formations: early Pliocene red bed
Magnetostratigraphy and age estimation
Based on the paleomagnetic analysis of the Nihewan basin in the XJY section, Matuyama reversed polarity were found at the middle to lower part of the sections (Su et al., 2000; Fan et al., 2002). While in the DNG section, the Normal polarities at the bottom and top of the section are referred to Guess and Brunhes normal polarities, respectively (Fan et al., 2002). Hence, regarding the excavation place of the new specimen in the lower part of the DNG section, we estimate an age of 2.58–2.7 Ma.
Materials and methods
When they described the fossils from Nihewan (Nihowan), Teilhard de Chardin and Piveteau (1930) did not list localities of the specimens. After exploring the collections in the Tianjin Natural History Museum, we extracted locality numbers marked on the specimens. The N. sinensis specimens used in this research, was excavated from locality 2, 3, 4, 11 and 15 of the XSG section. The majority of the studied specimens are housed in the Tianjin Natural History Museum (Hoangho Paiho) and IVPP. We
Results
The primary characteristics of the fossil raccoon dogs are the generalized characteristics of its lower and upper molar in comparison with other canids. Our study shows a gradual change in size and ratio of the lower and upper molars among the Nyctereutes species during their evolution in East Asia (Appendix A, Fig. 7). Primitive species N. tingi with a weak subangular lower mandibular lobe, more generalized teeth, and large body size in the late Pliocene was replaced or coexisted by larger
Concluding remarks
The study of new material from the DNG section and the previously materials from XSG, DNG, and ZKD reveals interesting facts about the evolution of raccoon dogs from Pliocene to Pleistocene. An increase in the body mass of Nyctereutes sinensis compared to early Pliocene N. tingi as well as changes in the molar teeth morphology, size, and its ratio may indicate a progressive evolution. Subsequently, changes in diet or environmental factors possibly cause the decrease of body mass in the
Acknowledgments
We are grateful to the IVPP collection staff, the Tianjin Natural History Museum staff, especially Ms. Min Zheng for her help in the study of fossils, and also to the kind local people of Xiashagou Village. Thanks are also due to Ms. Anja Rank for reviewing the text and providing productive suggestions. We appreciate the insightful and detailed comments from Dr. Masakazu Asahara and an anonymous reviewer that greatly improved our paper. This work has been supported by the Ministry of Science
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