A new species of Eogruidae (Aves: Gruiformes) from the Miocene of the Linxia Basin, Gansu, China: Evolutionary and climatic implications

ABSTRACT Despite having one of the most robust fossil records within core-gruiform birds (rails, cranes, and allies), the biogeographic history of Gruidae (cranes) and key drivers of diversification within this group remain largely unknown. The Eogruidae of Eurasia represent some of the earliest known crane-like fossils. Here, we present description of a new species represented by a well-preserved specimen of a foot from the late Miocene (7–6.5 mya) Liushu Formation of Linxia Basin, Gansu, China. It is the only eogruid fossil that has been found in this formation and is the first eogruid known from northwest China. Linxia Basin is located along the margin of the northeastern Tibetan Plateau, which allows for new insight into Miocene dispersal of the Eogruidae and potential climatological and geological connections. It is also the first specimen with an associated tarsometatarsus and nearly complete phalanges, including a claw, which provides further morphological information on this taxon. Referral of the new specimen to Eogruidae is based on extreme reduction of the trochlea of metatarsal II, which is most similar to the condition present in the eogruid subclade traditionally termed Ergilornithidae.


INTRODUCTION
The fossil record of Gruidae (cranes) is one of the most extensive within core-Gruiformes. Gruid fossils have largely been found in northern hemisphere localities (Mayr 2009(Mayr , 2016a. The biogeographic history, life history, and potential drivers of diversification within extinct gruids remains little understood, and many of these fossils require phylogenetic revision. This is especially true of the Eurasian Eogruidae, a group that contains the oldest crane-like remains after those of the Geranoididae from the early-middle Eocene of Wyoming (Wetmore 1933, Cracraft 1969, 1973Clarke et al. 2005, Mayr 2009). The only phylogenetic study of Eogruidae (Clarke et al. 2005) recovered Eogrus aeola (Wetmore 1934) within an unresolved group containing Psophiidae and Gruidae using a modified dataset (Mayr and Clarke 2003). Results also placed an eogruid-like specimen (IGM 100/1447) as the sister taxon of an Aramidae Volume 137, 2020, pp. 1-13 DOI: 10.1093 + Gruidae sister group. Traditionally, the morphologically similar Eogruidae and Ergilornithidae were divided into separate families; however, traditional Eogruidae is likely paraphyletic with respect to Ergilornithidae (Clarke et al. 2005). Here, we use the suggested terminology of Clarke et al. (2005), and consider Eogruidae to include taxa that were historically placed within Ergilornithidae.
Here, we describe a new eogruid taxon (Eogruidae sensu Clarke et al. 2005) from the late Miocene Liushu Formation of the Linxia Basin in Gansu, China. It is the only eogruid fossil that has been found within this formation, and the first to be located within northwest China. Avian fossils have only been recovered from the late Miocene Liushu formation and include ostriches, a pheasant, vultures, and falconids in addition to the species described here (Hou et al. 2005, Zhang et al. 2010. Baumel and Witmer (1993). The specimen was compared to osteological specimens of the Texas Memorial Museum at the University of Texas at Austin, and was scanned using x-ray microtomography (225 Micro CT) at the Key Laboratory of Vertebrate Evolution and Human Origins at the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP). The specimen is housed in the collections of IVPP, Beijing, China. CT data generated during the current study is available at Dryad: https://doi.org/10.5061/dryad.jh9w0vt6j.

Systematic Paleontology
AVES Linnaeus, 1758 GRUES Bonaparte, 1854 GRUOIDEA Vigors, 1825 EOGRUIDAE Wetmore, 1934(sensu Clarke et al. 2005 Sinoergilornis, gen. nov. (Figures 2-6) Type species. Sinoergilornis guangheensis, sp. nov. Diagnosis. The didactyl foot distinguishes Sinoergilornis guangheensis from all Gruidae, Eogrus, Ergilornis, and Sonogrus. Sinoergilornis guangheensis is differentiated from all other Eogruidae by a unique combination of features, including the following that are novel within the remaining TABLE 1. Summary of the species and recovered elements of all previously described didactyl Eogruidae. See Figure 1 for locality and age data of presented taxa. Boldfaced elements are those that overlap with the holotype specimen of the new species. Abbreviations: prox = proximal, dist = distal, R = right, L = left, tbt = tibiotarsus, tmt = tarsometatarsus.
Differential diagnosis. Although the tarsometatarus is distinct when compared with other Neogene didactyl Eogruidae, the general shape and size of the pedal phalanges of S. guangheensis are most similar to the condition in Urmiornis orientalis ( Figure 6). In addition to the diagnostic differentia of the new genus, S. guangheensis can be differentiated from the Miocene U. orientalis due to (1) the presence of further dorsally raised trochleae that grade proximally into the shaft of each phalanx (  Figure 6 for comparative drawings of differentia). Micro-CT data (see Figure 6, Supplementary Material Videos 1, 2, and 3, and data on Dryad: https://doi. org/10.5061/dryad.jh9w0vt6j) reveals further differentiation of III:1 in S. guangheensis. The phalanx possesses a proximodistally truncate, plantar eminence compared to those of other didactyl eogruids. The incisura along the dorsal margin of this eminence is relatively deep, like that of U. orientalis, although it appears to be dorsoplantarly wider ( Figure 5; inc). Characters 1-5 were only able to be assessed for U. brodkorbi and U. orientalis, and characters 6-8 were only assessable in U. orientalis.
Although reduction of trochlea II is similar to the condition in ostriches, complete eogruid tarsometatarsi reveal enclosed flexor canals within the hypotarsus that place this group within Neoaves, as the canals of Paleognathae are not closed (Clarke et al. 2005). Sinoergilornis guangheensis additionally exhibits many characters within the distal tarsometatarsus and pedal phalanges that place it firmly within Eogruidae. In the tarsometatarsus, trochlea II is more prominent than that of Struthio, the fovea for the collateral ligament in trochlea IV is shallow in S. guangheensis and is deep and circular in Struthio, the lateral margin of trochlea IV is much more plantarly projected in the new taxon, and the mediodistal margin of trochlea IV is markedly medially projected in S. guangheensis. Within the phalanges, the most notable differentia comprise a sickle-shaped flexor pit of III:1 in S. guangheensis, recurvature of the ventral margin of III:1 in the new taxon, and the more proximodistally shortened III:2 and IV:2-3 of TABLE 2. Measurements of digit III, phalanx 1 in select members of Eogruidae and several extant Gruidae. Measurements (mm): a = total length; b = distal depth; c = proximal depth; d = minimum diaphysis depth; e = distal width; f = proximal width; g = minimum width (see Boev et al. 2013 figure 3 for details). ?Amphipelargus measurements are from Zelenkov et al. (2016). All measurements other than those of Sinoergilornis guangheensis are from Boev et al. (2013). Extinct taxa are denoted by daggers. S. guangheensis (Figures 3-6). The latter phalanges are subequal in size, whereas those of Struthio are roughly twice as elongate as their distal counterparts. The single preserved pedal ungual IV:5 of S. guangheensis is additionally elongate and recurved, unlike the relatively small claw of an ostrich that is flattened along the plantar margin ( Figures 5-6). Sinoergilornis guangheensis can be distinguished from Miocene ostrich by the plantar extension of trochlea IV of the tarsometatarsus in S. guangheensis, which is limited in Struthio cf. karatheodoris (Miocene, southwestern Bulgaria; Boev and Spassov 2009). If another individual of this taxon is found that is represented by other elements not contained in the holotype specimen, it will not be assignable to this taxon until further associated elements are located. Type locality and horizon. Linxia Basin, northeastern Plateau, China, Liushu Formation. The exact locality of the specimen is unknown as it was collected by locals in 2018. The locality and horizon are similar to that of Li et al. (2016). The Linxia Basin is an intracontinental foreland basin located on the northeastern margin of the Tibetan Plateau (Wang et al. 2014). It is currently located in a transitional zone between the East Asian monsoon and the non-monsoon arid climate of the Asian inland (Fang et al. 2016). Long and continuous sedimentary succession was deposited in this basin from the Oligocene to the Pliocene and Pleistocene (Li 1995, Fang et al. 2003Qiu et al. 2004, 2013Garzione et al. 2005). The stratigraphy of Linxia Basin has previously been divided into 8 formations based on lithofacies, contacts, paleontology, and magnetostratigraphy (Li 1995, Li et al. 1997, Fang et al. 2003. While mammalian remains have been recovered in many of these deposits (Deng et al. , 2013, avian remains have only been recovered in the Liushu formation (Hou et al. 2005, Zhang et al. 2010. The most recent dates provided for the Liushu formation are late Miocene in age, from 7.78 to 6 million years ago [mya] (Fang et al. 2016). It is largely made up of mudstone and siltstone (Wu et al. 2017).
Description and comparison. The specimen is preserved three-dimensionally and comprises the distal portion and metatarsal trochleae of the left tarsometatarsus along with nearly complete sets of pedal phalanges for digits IV and III, including a decurved ungual (IV:5, Figure 5). The size of the specimen is similar to that of a large extant gruid, such as Grus grus. The tarsometatarsus is preserved in dorsal aspect with both lateral and medial aspects visible, as in digit III. A large area of breakage is evident along the proximal, dorsal region of III:2. Digit IV is preserved in laterodorsal aspect. The shaft of the tarsometatarsus is not preserved, and the specimen is broken along the proximal margin of the medial groove of the trochlea of metatarsal III and the foramen vasculare distale. The foramen vasculare distale is ovoid and the proximal margin is slightly angled medially. A shallow groove extends along the length of the intertrochlear area from the distal portion of the foramen. A small amount of breakage is located along the distal margin of trochlea II.
The trochlear area is wide and exhibits dorsoplantar flattening, as in extant Gruidae (Figures 2 and 5). A small portion of the distal margin of the trochlea of metatarsal II is slightly broken. This trochlea is reduced and located much more proximally as compared to those of trochleae III and IV. It extends little medially. The trochlea of metatarsal III is the most robust trochlea both lateromedially and proximodistally and extends approximately twice the distal length of trochlea IV. This is similar to the condition in both extant Gruidae and in IGM 100/1447, the Eogrus aeola holotype specimen (AMNH 2936), and 2 specimens referred to Eogrus aeola (AMNH 2937 and AMNH 2946; Clarke et al. 2005). The depth of the medial groove of trochlea III is shallow to moderate, is mediolaterally broad, and continues along the midline of trochlea III to the small distal portion of the plantar aspect of trochlea III that is visible. The terminus of this groove cannot be determined without further preparation. The proximal margin of the groove terminates just below the level of the distal margin of the foramen vasculare distale. This is like that of IGM 100/1447 and the abovementioned Eogrus specimens. The lateral and medial aspects of trochlea III are deeply excavated and exhibit circular pits. The pit of the lateral aspect is deeper than that of the medial aspect.
The intertrochlear incisura between trochleae III and IV is small, only about 2 mm between the lateral margin of trochlea III and the distomedial margin of trochlea IV. This is similar to the condition in Balearica pavonica (M-5323) and Grus canadensis (M-11728), although trochlea IV does not present as much lateral torsion as that of G. canadensis. The distal margin of trochlea IV angles medially, which is most like that of IGM 100/1447, the Eogrus aeola holotype specimen, and the 2 Eocene specimens referred to Eogrus aeola (Clarke et al. 2005). Trochlea IV is slightly plantarly deflected, more so than that of IGM 100/1447. The degree of deflection is most similar to that of the Eogrus aeola holotype specimen. The ala of trochlea IV is stout, rounded, and robust. Its distoplantar extent is greater than that of IGM 100/1447. A shallow depression is present on the lateroplantar margin of the ala.
Digit III comprises the most robust elements of the preserved digits. Phalanx 1 of digit III is recurved (see Supplementary data and videos) and is more mediolaterally broad and proximodistally elongate than phalanx 1 of digit IV (Figures 4 and 5). The proximal margin of III:1 is especially broad, with a robust and acuminate plantar eminence present (see Supplementary Material Videos 1, 2, and 3 and data on Dryad: https://doi.org/10.5061/dryad. jh9w0vt6j) that is accompanied by a deep incisura along its dorsal margin. The lateral flexor pits or collateral ligament pits of III:1 are deep and the lateral flexor pit is sickle shaped (Figure 5), with a narrow and elongate incisura extending proximally from the fovea. The trochlea of III:1 is proximodistally extensive and lateromedially wide. A triangular depression is present above the cartilaginous trochlea (Figures 3, 4, and 5). III:2 is approximately half the length of III:1 but exhibits approximately the same width as the distal portion of III:1. III:3 is similarly approximately half the length of III:1 and as lateromedially robust. The trochleae of both III:2 and III:3 are proximodistally shortened compared to that of III:1, and symmetrical, semicircular indentations are present along the lateral margins of the proximal eminence of III:3 (Figures 3, 4, and 5; scd). Deep lateral flexor pits are also present in these phalanges, although the sickle shape is less pronounced in these pits than those of III:1. "III:4" has been identified as a likely mammalian bone that was artificially attached to phalanx III:3 due to incongruous morphology and CT scanning of the specimen revealing that this bone was higher in density (i.e. more comparable to that of a mammal than of a bird; Supplementary Material Videos 1, 2, and 3 and data on Dryad: https://doi.org/10.5061/dryad.jh9w0vt6j) and set atop darker, broken matrix that was likely mixed with glue (shown in gray in Figures 3, 4, and 5).
IV:1 is relatively slender, approximately two-thirds the length of III:1 and half as wide. The lateral and medial flexor pits of this phalanx are shallow and circular. IV:2, IV:3, and IV:4 are markedly proximodistally shorter than IV:1, with IV:2 being only slightly more elongate than IV:3 and IV:4. The proximal eminences of each phalanx are distinctly projected proximally and are proximally acuminate. Shallow, circular lateral and medial flexor pits are similarly located on all 3 of these phalanges. IV:4 is exposed in lateral view, but appears to be broad at the base and robust. The claw tapers to what appears to be a rounded terminus, although this is somewhat obscured by matrix.

DISCUSSION
Compared to Urmiornis, Amphipelargus, and Ergilornis, Sinoergilornis guangheensis exhibits the largest III:1 measurements for distal depth, minimum diaphysis depth, and minimum width, and has one of the largest measurements for proximal width after that of Urmiornis orientalis (see Table 2). Zelenkov et al. (2016) suggested that flattening of III:1 was indicative of running adaptation, and that the more robust phalanx of the Greek Amphipelargus-like specimen KRY 1300 suggests that it was less adapted to running, perhaps indicating that it lived in a more humid and vegetated environment than its eastern counterparts. Sinoergilornis guangheensis shares similar depth measurements and overall shape with this specimen. Kurochkin (1982) hypothesized that Eogruidae grew larger in body mass over time as their cursorial adaptations became more apparent; however, it is unclear how depth and width of the phalanges are related to body mass in this group. The length of III:1 in Sinoergilornis guangheensis is within the range of those of the extant cranes Anthropoides virgo (Demoiselle Crane) and Grus grus (Common Crane), although its width and depth measurements are approximately twice as robust (see Table 2).
Several workers have suggested that the Eogruidae were flightless (Wetmore 1934, Kurochkin 1976, Feduccia 1999, although the morphological evidence known from recovered specimens needs confirmation (Clarke et al. 2005). A humerus (PIN 3110-60;Kurochkin 1976) exhibiting characteristics of flightlessness was attributed to Ergilornis sp. (Clarke et al. 2005); however, it is an isolated bone and it is unclear whether it was assigned correctly to Eogruidae rather than to an ostrich. In addition, a coracoid assigned to E. aeola does not exhibit flightless characteristics (Clarke et al. 2005, Mayr 2016b). The curved, elongate claw of digit IV in Sinoergilornis guangheensis is less suggestive of a cursorial, flightless locomotor strategy than the straightened and relatively truncate and dorsoplantarly flattened condition exhibited in claws of extant Struthio (Birn-Jeffery et al. 2012). Further fossil evidence, namely of elements more directly related to flight such as those of the pectoral girdle and forelimb, is needed to thoroughly assess the flight capabilities of the Eogruidae.
Sinoergilornis guangheensis provides additional insight into the diversification and differentiation of the Eogruidae due to its age and locality. Current fossil evidence suggests that the Eogruidae were largely present in southeastern Mongolia during the Eocene and that they largely diversified during the Miocene, during which time Eogrus and Sonogrus disappeared and the distribution of Eogruidae expanded westward to the Balkan peninsula, northward to northern Mongolia, and southward to the northeastern and southwestern Tibetan Plateau (Figure 1). This burst of diversity and range expansion corresponds approximately with the beginning of monsoon-dominated climate patterns around the Oligocene-Miocene boundary (Liu et al. 1998, Guo et al. 2002, 2008Wang et al. 2003aWang et al. , 2003bWang et al. , 2005Sun and Wang 2005, Qiao et al. 2006, Wang 2009, Qiang et al. 2011, the onset of the East Asian monsoon (Wu et al. 2017), and northwestern encroachment of the humid belt into the arid/semi-arid belts of China (Guo et al. 2008). The late Oligocene mammalian assemblage of giant rhino fauna in the Linxia Basin also support the onset of the East Asian monsoon around this time, as their presence indicates a warm and humid habitat , Deng et al. 2013.
The presence of Eogruidae in the late Miocene Liushu Formation additionally corresponds with the timing of northeastern Tibetan Plateau uplift and intensification of the East Asian monsoon around the pre-late Miocene (~8 mya; Wang et al. 2014, Wu et al. 2017, Xu et al. 2018. Tibetan Plateau uplift has been linked to East Asian monsoon intensification by several studies, although its exact relationship with this climatic phenomenon remains uncertain (Wang et al. 2014). Grain size evidence from Linxia has similarly shown that the Asian winter monsoon intensified ~7.4 mya (Fan et al. 2007). Range and diversity shifts of Eogruidae coupled with the timing of the onset and intensification of the East Asian monsoon, associated Tibetan Plateau uplift, and the northwestern expansion of the humid belt may indicate the Monsoon as a potential driver of eogruid diversification and dispersal to more open and arid environments in western Eurasia.
Mammalian diversity and faunal similarity of Hipparion fauna in the Liushu Formation along with evidence from lithology, carbon isotopes, and paleobotany suggest a subarid, open steppe environment during the late Miocene in the Linxia Basin that was dominated by C 3 plants. Xerophilous and subxerophilous grasses were additionally present, indicating a dry grassland environment (Deng 2006). Conversely, Hipparion fauna of Greece indicate the presence of a sclerophyllous, evergreen woodland environment during the late Miocene. This is likely the environment that western late Miocene eogruid genera such as the morphologically similar Amphipelargus experienced.
The appearance of Eogruidae in the Nagri and Chinji Formations of the Siwaliks in Pakistan (late middle and early late Miocene, ?Urmiornis cracrafti; Harrison andWalker 1982, Karhu 1997) corresponds roughly with the timing of the intensification of the Asian monsoon along the southern Tibetan Plateau during the mid-to late Miocene (as early as 11-7 mya; Quade et al. 1989, Sanyal et al. 2010 and the uplift of the Himalayas to their present elevation around 11-9 mya (Garzione et al. 2000, Rowley et al. 2001, Saylor et al. 2009, Quade et al. 2011. Intensification of the Asian monsoon in this area is indicated by a dramatic environmental shift from C 3 to C 4 plants in the Siwalik Basin, and Himalayan uplift has been linked to the onset and intensification of the Asian monsoon (Araguás-Araguás et al. 1998, Wang et al. 2014. Eolian sediments in China and the marine sediment record of the Indian and North Pacific oceans additionally support onset of the Indian and East Asian monsoon around 9-8 mya (An et al. 2001). As in Linxia, carbon (Barry et al. 2002) and oxygen (Behrensmeyer et al. 2007) isotope evidence indicates that the late Miocene environment of the Siwaliks shifted to a drier and more seasonal environment that contains fluvial sediments indicating the presence of floodplains (although these were surrounded by C 4 grasslands). Similar environmental shifts were associated with the first appearance of eogruids, as the Eocene and Oligocene sediments of southeastern Mongolia and the adjacent portion of China that have produced eogruid fossils contain lacustrine and lacustrine-alluvial facies that represent lacustrine-alluvial plains (Dashzeveg and Devyatkin 1986).
Additional climate phenomena highlight uncertainty surrounding possible drivers of the diversification and dispersal of both Eogruidae and gruid-like extinct taxa. Eocene-Oligocene global cooling may have had an effect on crane-like taxa globally, including the Eogruidae, although sampling and rock record biases cannot be ruled out to explain Oligocene sampling. Preservation bias and locality sampling bias generally must be considered when drawing conclusions from the fossil record. Crane-like taxa of uncertain phylogenetic placement (see Table 2) are abundant in Europe and North America during the Eocene, with only one Oligocene taxon (Parvigrus pohli) being known from Europe (Mayr 2005, Mayr 2013. Similarly, few eogruids have been found in Oligocene sediments, and those that are known are limited to southeastern Mongolia. Faunal shifts within Linxia since the late Miocene suggest that large environmental change occurred, and the presence of Eogruidae in this locality further emphasizes this (Li et al. , 2016. It is unclear why Eogruidae are only known until the early Pliocene while undoubted extinct crown gruids are not abundant in Asia until the Pliocene and Pleistocene (Zelenkov 2015). Only one eogruid, Urmiornis dzabghanensis, is known from the early Pliocene, and was recovered from western Mongolia (Zelenkov andKurochkin 2015, Zelenkov et al. 2016). Other than the east coast of China, the Tibetan Plateau currently holds the highest amount of extant crane diversity in the world, with 4 species having overlapping or nearly overlapping distributions within the margins of the Tibetan Plateau (del Hoyo et al. 2019). Phylogenetic reassessment of the Eogruidae within the context of extinct crown gruids and other stem gruidlike fossils is needed to better understand the biogeographic history of these taxa and better estimate the primary drivers of eogruid extinction and extant crane diversification.

ACKNOWLEDGMENTS
Gao W. is thanked for photography and Hou Y. for scanning of the specimen. C. Urban is thanked for aid in CT segmentation of the specimen. T. Stidham is thanked for valuable discussion. The nomenclature in this paper has been reviewed by the Working Group on Avian Nomenclature of the International Ornithologists' Union, and the new genus and species have been registered with ZooBank under LSID urn:lsid:zoobank. org:pub:EF3BA455-373C-4A0D-A1E1-BE85DEB502D0.