Limusaurus

Between 2001 and 2006, a Chinese-American team of paleontologists examining the Wucaiwan locality in the Shishugou Formation, in the northeastern Junggar Basin of Xinjiang, China, discovered three bone beds (numbered TBB 2001, TBB 2002, and TBB 2005, found by T. Yu and J. Mo). The bone beds were dominated by the remains of small theropod dinosaurs, representing at least three genera, with most belonging to a small ceratosaur, the first member of this group found in Asia. Stacked skeletons from these bone beds were removed from the field in blocks, jacketed by plaster, and encased in crates. A resin cast of block TBB 2001 was made, making it available for study after the specimens had been extracted from the original matrix. Except one, all specimens from this block are mounted in a cast of the block in its semi-prepared state. The toothless adults and toothed juveniles were initially thought to be different kinds of dinosaurs, and were studied separately, until it was realized they represent the same species. ==Description==

Limusaurus was a small and slender animal. The holotype (which was originally considered an adult based on the level of fusion of its bones, but later as a subadult when analyzed along with other specimens) is estimated to have been about in length Skull The skull of Limusaurus was relatively tall and short, roughly half the length of the femur (upper thigh bone). The tip of its jaws was covered by a beak, a feature that was previously unknown in non-coelurosaurian theropods like Limusaurus (the coelurosaurs include the most bird-like dinosaurs). As in most dinosaurs, the skull featured five principal fenestrae (openings): the (bony nostril), orbit, antorbital fenestra (between the nostril and eye), as well as the and (on the top and on the side of the skull's rear, respectively). As in other ceratosaurians, parts of the bony nostril were formed by the maxilla (upper jaw bone); also, the antorbital fenestra was proportionally small, and the rear part of the nasal bone formed parts of the cavity which contained this opening. The external naris was large and located in a hindwards position, similar to tetanuran theropods. The orbit was large, while the lateral temporal fenestra was not as large as would be expected from more derived (or "advanced") members of the Ceratosauria. Uniquely to Limusaurus, the inner bottom edge of the premaxilla, the frontmost bone of the upper jaw, was convex. The nasal bone was distinct in having a "shelf" on its side, was short, wide, less than one-third of the length of the , and twice as long as it was wide. The lower part of the lacrimal, the bone that formed the front margin of the eye opening, was unique in being strongly inclined forwards. The jugal bone, which formed the floor of the eye opening, was slender, and its rami (or branches) were rod-like, which is also unique to this genus. The (claw bones) of the fingers were short, stout, and expanded at their base. They had two grooves on their sides, a feature also found in Masiakasaurus. Among the pelvic bones, the ilium was small and tilted towards the midline of the body, as was the case in Elaphrosaurus. As in other ceratosaurians, the lower end ("boot") of the pubis was large and expanded. Unique to the genus, it pointed backwards in a hook-like shape and had a ridge on each side. The elongated legs of Limusaurus had proportions that were well-adapted to running, with their lower segments much longer than the femur: the tibiotarsus, the fusion of the tibia (shin bone) and tarsal bones, was 1.2 times the length of the femur, and the foot was 1.3 times the length of the femur. The legs were 1.8 times the length of the torso. The upper half of the femur was triangular in cross section, a feature shared with Masiakasaurus. The metatarsals of the three weight-bearing toes were arranged in an arc, with the fourth metatarsal straight and adhering tightly to the third for its entire length; these features are unique to Limusaurus. The hallux (the first toe or dewclaw) was reduced, being only 17% the length of the third metatarsal, another unique feature. As in other ceratosaurians, the unguals of the foot had two grooves on their sides. ==Classification and evolution==

Limusaurus was classified as a basal member of Ceratosauria by Xu and colleagues in 2009 (who also considered the closely related Elaphrosaurus as such). It had several skull features in common with basal theropods such as other ceratosaurs and coelophysoids, but it also shared a number of traits, including the beak and the fused sternum, convergently with the later coelurosaurs. while a 2010 study by paleontologist Martin Ezcurra and colleagues placed them in the more derived group Abelisauroidea within Ceratosauria. A 2016 study by paleontologists Oliver Rauhut and Matthew Carrano found Limusaurus to be more derived, grouping together with Elaphrosaurus within the abelisauroid family Noasauridae. Together with an as-of-yet unnamed taxon represented by specimen CCG 20011, and not included in other analyses, the two taxa formed the clade Elaphrosaurinae; Elaphrosaurus and CCG 20011 were closer to each other than to Limusaurus within this group. Laevisuchus and Deltadromeus were placed basal to the group of Noasaurinae and Elaphrosaurinae within Noasauridae. The only known specimen of Elaphrosaurus is missing its skull and hands among other elements, and its affinities were long unclear (it was often considered an ornithomimosaur from 1928 well into the 1990s) until the more complete Limusaurus was found. The discovery of Limusaurus allowed the extrapolation of the complete length of Elaphrosaurus, . Wang and colleagues, in 2017, also found Limusaurus and Elaphrosaurus to group in the clade Elaphrosaurinae, within the family Noasauridae. Variants of their analysis also recovered Spinostropheus as a possible additional elaphrosaurine. The Noasauridae was placed in a position outside Neoceratosauria, the group containing Ceratosaurus and Abelisauridae. A 2019 study by paleontologist Max Langer and colleagues, which was based on the same data set used by the 2016 study, also grouped Limusaurus together with Elaphrosaurus and CCG 20011. Argentinian paleontologist Mattia Baiano and colleagues, in 2020, found Limusaurus to form a clade with Elaphrosaurus as well as with the new genus Huinculsaurus. , whose affinities and appearance were unclear until the discovery of Limusaurus|alt=Diagram showing a reconstructed skeleton of the related Elaphrosaurus'' In addition to being the first definite ceratosaur known from Asia to be discovered, Limusaurus is also one of the earliest known members of the group, living during the Oxfordian stage of the Jurassic period (approximately 161-157 million years ago). According to Xu and colleagues, its discovery shows that the Asian dinosaur fauna was less endemic during the Middle to Late Jurassic period than previously thought, and suggests a possible land connection between Asia and other continents during that period. Digit homology The most basal theropods had five digits in the hand. Along the lineage that led to birds the number of digits in the hand decreased; by the emergence of the group Tetanurae, which includes birds, two digits had disappeared from the hand, leaving three. Traditionally, it has been hypothesized that the digits lost were the two outermost digits, i.e. digits IV and V, in a process known as Lateral Digit Reduction (LDR). According to this scenario, the three fingers retained by tetanurans were therefore homologous (evolutionary corresponding to) with digit I, II, and III of basal theropods, which would have implications for the evolution of birds. and has been used by paleornithologist Alan Feduccia to support the hypothesis that birds are descended not from theropods but from some other group of archosaurs which had lost the first and fifth digits. The mainstream view of bird origins among paleontologists is that birds are theropod dinosaurs. To explain the discrepancy between morphological and embryological data in the context of bird origins, an alternative scenario to LDR was developed by paleontologists Tony Thulborn and Tim Hamley in 1982. In this scenario, the digits I and V of theropods were reduced in the process of Bilateral Digit Reduction (BDR), with the remaining digits developing to resemble the former digits I-III. Limusaurus was initially considered as evidence for the BDR hypothesis by Xu and colleagues in 2009 due to it—and other ceratosaurians—having a reduced first digit, with these researchers hypothesizing that a similar pattern of reduction occurred among the tetanurans (the sister group of the ceratosaurians). Several other hypotheses have been proposed to improve upon and reconcile the LDR and BDR hypotheses. One predominantly favored hypothesis, first developed by evolutionary biologist Günter P. Wagner and paleontologist Jacques Gauthier in 1999, involves a "frameshift" of the digits; the first digit fails to grow in the first developmental site due to not receiving the necessary signals, which has the effect of shifting digits I-III to the positions of II-IV. Thus, while digits I-III from the ancestral theropod are retained, they do not grow in the same location. A version of the frameshift hypothesis modified to incorporate both elements of BDR and fossil evidence from Limusaurus and other theropods, the "thumbs down" hypothesis of biologist Daniel Čapek and colleagues from 2014, suggests that this frameshift took place after the reduction of both the first and the fourth digits in the theropod lineage. The main alternative hypothesis, supported by Xu and colleagues, known as the "lateral shift hypothesis", considers a partial, step-wise frameshift in which, from a four-fingered hand with reduced digits I and IV, I fully disappears while IV develops into a fully-fledged finger, with II-IV taking on the morphologies of the former I-III. In a 2009 response to Xu and colleague's description of Limusaurus, biologist Alexander Vargas, Wagner and Gauthier stated in 2009 that it is plausible that ceratosaurians underwent BDR independent of the tetanurans, and therefore have no bearing on the issue of avian digit homology. Xu and biologist Susan Mackem stated in 2013 that the divergent developmental pathways of ceratosaurians and tetanurans are associated with a difference in forelimb function; tetanurans utilized their hands for grasping prey, while the hands of ceratosaurians almost certainly played no role in predation. An ancestral states analysis (estimation of the original anatomy of a group) by Dal Sasso and colleagues in 2018 also found that the digit reduction seen in Limusaurus occurred independently from that in tetanurans. According to this analysis, an axis shift from digit position IV to III took place at the basis of Tetanurae after the fourth finger was lost. ==Paleobiology==

Growth Specimens of Limusaurus show 78 different anatomical changes that occurred as the animals grew. In particular, their heads became proportionally shallower, their middle hand bones lengthened, and the "hook" of their pubis grew longer. The shaft of the quadrate bone in the skull also straightened in adults, and the tips of their lower jaws became more downturned. The early halt in tooth replacement possibly resulted from the regression of the replacement tooth buds during the first year, as in the veiled chameleon. The replacement of teeth by a beak through the growth of Limusaurus suggests that beaks in other lineages of theropods, and indeed beaked animals in general, may have evolved heterochronically, i.e. with beaks first occurring in adults and then gradually appearing in juveniles as these lineages evolved. This is in accordance with the presence of genetic signal pathways (molecular processes) which control the formation of teeth in birds. Wang and colleagues analyzed growth rings (visible in bone cross-sections and analogous to the growth rings of trees) of the tibiae from the various developmental stages of Limusaurus in 2017, and found that the animal was skeletally mature at six years of age. The bone tissue was primarily composed of fibrolamellar bone (where the internal fibres are disorganized), indicating that Limusaurus grew quickly; In older specimens, the outermost growth rings are very close together (forming what is known as the external fundamental system), indicating that rapid growth had ceased in these individuals. Wang and colleagues pointed out that adult specimens in particular are characterized by the presence of gastroliths (ingested stones retained in the stomach), with older adults having gastroliths that are larger and more numerous than those of younger adults. The size and quantity of these gastroliths are comparable to those of birds in young adults, and those of ornithomimosaurs and oviraptorosaurs in older adults. These groups of theropods all used gastroliths in processing plant matter, suggesting that Limusaurus did the same; the increased number of gastroliths in older adults may be indicative of the gut's ability to process plant matter more finely as they aged. An isotope analysis of the available specimens of Limusaurus likewise showed that adults consistently match the isotope signatures of other herbivorous dinosaurs. In the same analysis, juveniles and subadults were found to vary greatly in their isotopic signatures; this indicates that juveniles were likely omnivorous (feeding on both animals and plants), but switched to strict herbivory as they aged. This is comparable to the diet shift experienced by the aforementioned mullets and armored catfish. ==Paleoenvironment==

and a Yinlong, contemporaries of Limusaurus in the Shishugou Formation|alt=Artistic reconstruction of the habitat of Limusaurus'' All known Limusaurus fossils were recovered from the Shishugou Formation, a succession of sedimentary rocks that were deposited at the northeastern margin of the Junggar foreland basin and is about in thickness. The formation is dated to the Late Jurassic, around 161 to 157 million years ago. Limusaurus occurs in the upper part of the formation, which represents a variety of environments, including alluvial fans and alluvial plains, streams, wetlands, and shallow lakes. During the time when Limusaurus lived, the environment would have been relatively warm and dry, judging by the abundance of coal and carbon-rich deposits. The climate was probably highly seasonal due to monsoonal influences, with warm, wet summers and dry winters. The climate enabled the growth of a richly forested environment; the forest would have been dominated by Araucaria trees, with the undergrowth being occupied by Coniopteris, Anglopteris and Osmunda ferns, Equisetites horsetails, and Elatocladus shrubs. The environment of the Shishugou Formation hosted a diverse assemblage of animals. More than 35 species of vertebrates are known from fossils, including at least 14 dinosaur species. Small theropod dinosaurs are generally rare in the fossil record. According to Eberth and colleagues, the high incidence of Limusaurus indicates that the abundance of small theropods is underestimated elsewhere as these animals are generally less likely to fossilize. Two of the mud pits containing Limusaurus specimens were found at the same stratigraphic level, while a third was some higher in the stratigraphic column. The deformation structures and the consistent size of the pits suggest that they represent the footprints of giant sauropods such as Mamenchisaurus sinocanadorum, which was likewise found in the Shishugou Formation and would have had a mass of over and a limb length of over . Other possible explanations, including sand volcanoes or sinkholes, can be ruled out because characteristic sedimentological features are lacking. The possibility that the encased dinosaurs could have created the pits themselves can likewise be ruled out given their small size; the largest dinosaur found in the pits, Guanlong, would have been merely tall. When creating the pits, the footsteps of the sauropods could have led to soil liquefaction, resulting in smaller animals such as Limusaurus becoming stuck. In contrast to other incidences of miring in dinosaurs, where much larger individuals likely became stuck in a highly viscous sediment and got preserved in their original death positions, the mud pits containing Limusaurus were of a more liquid mud in which the carcasses floated before settling at the bottom. The size of these assemblages can be attributed to the tendency of smaller animals to become trapped in mud. of giant sauropods such as Mamenchisaurus|alt=Reconstructed skeleton of the giant sauropod Mamenchisaurus Limusaurus is the most abundant dinosaur found in the mud pits. One of the three pits, TBB2001, contained five Limusaurus individuals while other species are absent. TBB2002, on the other hand, contained five theropod dinosaur skeletons including two Limusaurus, two Guanlong and one individual of a not yet described species. The third pit, TBB2005, contained twelve Limusaurus individuals, including the holotype, but also the tail of a small ornithischian dinosaur as well as two crocodyliforms, two mammals, a turtle and three tritylodontid cynodonts. The completeness of the skeletons is variable; at least half of the theropod skeletons are complete, with missing parts due to recent erosion. Rear parts of the skeletons tend to be more common than front parts. Most individuals were embedded laying on their sides, though some lie on their backs or undersides. In pits TBB2001 and TBB2002 the skeletons lie one above the other. Bones pertaining to the same individual often lie upon each other in direct contact, while there is no direct contact between bones of separate individuals. This indicates that sediment settled within the mud pits between the burial events. These observations led Eberth and colleagues to conclude that the skeletons must have accumulated within the mud pits over an extended time span rather than during a short-term death event. The completeness and articulation (connectedness) of the skeletons suggest rapid burial, though the presence of isolated body parts also suggests that some carcasses were exposed to the air for days or months. Evidence for scavenging, such as isolated bones, tooth marks on bones, or of theropods, is lacking. However, it is possible that scavengers carried whole body parts away, as feeding at the pits might not have been possible. Eberth and colleagues speculated that the two Guanlong specimens preserved at the top of pit TBB2002 could have been scavenging on the mired carcasses before getting mired themselves. The horizontal orientation of the skeletons within the pits suggests that the mud was soft. The neck and tail of one specimen are bent upwards, suggesting that the carcass was pushed down towards the bottom of the pit by trampling of another animal that became trapped at a later time. Specimens typically show flexed hind limbs, indicating that the individuals died in a resting pose within the pits. The typical death poses seen in many other dinosaur skeletons, where the head and tail are drawn above the body, are absent. Eberth and colleagues found it likely that the burial of all individuals occurred in less than a year, based on the seasonality of the local climate and the similarity of the sediments of the three pits. ==See also==