Limusaurus

To test the influence of the extreme anatomical changes with growth in Limusaurus, Wang and colleagues, in their 2017 study, performed separate analyses that were based on only the adult anatomy or on both the adult and juvenile anatomy. In another analysis, each Limusaurus individual was treated as an independent unit. All the juvenile Limusaurus specimens grouped together to the exclusion of adult specimens, showing that their anatomy changed significantly through growth. The inclusion or exclusion of juvenile features had little effect on the placement of Limusaurus in the phylogenetic tree.[15]

The cladogram below shows the position of Limusaurus within Noasauridae according to Baiano and colleagues, 2020:^[18]

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

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.^[2][20]

However, the hypothesis of LDR is in contradiction to some embryological studies on birds which show that, from five developmental sites, the digits that develop are the three middle digits (II, III, IV). This inconsistency has been a matter of debate for almost 200 years,^[21] 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.^[22] The mainstream view of bird origins among paleontologists is that birds are theropod dinosaurs.^[23] 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.^[2][24] 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).^[2][25]

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,^[26] 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.^{[9][20][27][28][29][30]} 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.^[31] 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.^[2][20][32]

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.

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.^[4]

The most obvious change that happened during the growth of Limusaurus was the complete loss of teeth from juveniles to adults. Juveniles began with one tooth in each premaxilla, eight in each maxilla, and at least twelve in each half of the lower jaw (at least 42 teeth in total). At the next stage, the first, sixth, and eighth teeth in each maxilla, as well as the sixth in each half of the lower jaw had all been lost, although the sockets were still present, and there was a small replacement tooth in the socket of the sixth lower tooth (leaving at least 34 teeth in total). During this stage, use of teeth and normal tooth replacement likely ceased or became reduced, since none of the still-erupted teeth bear any wear marks or resorption. As the specimens grew, the transformation became more radical. In subadult and adult specimens older than one year, all the teeth were missing. CT scanning shows that only five empty tooth sockets remained in the adult maxilla; all the sockets in the lower jaw were fused into a single, hollow canal, and the rest of the tooth sockets were obliterated.^[4]

The loss of teeth with age in Limusaurus is the most extreme case of tooth morphology changing with age recorded among dinosaurs. Limusaurus is one of the few known jawed vertebrates where teeth are completely lost during growth. The other known examples are the red mullet and striped red mullet, several armored catfish, and the platypus. Meanwhile, its complicated pattern of tooth loss, from both the front and the back, is most similar to that of the avialan Jeholornis.^[15][34] 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.^[15][35] 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.^[4][15][36]

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^[37]), indicating that Limusaurus grew quickly;^[4] by contrast, the noasaurines Masiakasaurus and Vespersaurus had parallel-fibred bone indicative of slower growth, possibly due to the drier and more resource-poor environments that they would have lived in.^[38] 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.^[4]

Feeding and diet

Anatomical features of Limusaurus such as the small head with toothless jaws and long neck were interpreted as indicating a herbivorous diet by Xu and colleagues in 2009.

The paleontologist David A. Eberth and colleagues suggested in 2010 that the large number of Limusaurus specimens in the Shishugou Formation mud pits indicates they were either abundant among the small vertebrate animals in the area, or that the trapped individuals had been drawn there. They found it unlikely that animals were trapped on any basis other than size, and pointed out that it was difficult to explain why herbivores like Limusaurus would be attracted to sites where other animals were mired, so they considered it most likely that the larger number of Limusaurus fossils was due to their abundance. These authors also suggested that the abundance of Limusaurus inferred for the area and the evidence for successive, rapid burials of each individual made it possible that Limusaurus was gregarious, living in groups. There is some evidence for gregariousness in many small theropods and that there may have been social behaviours related to age, but it remains unknown whether the bone beds containing Limusaurus specimens preserve evidence of sociality and segregation related to age.[1] Paleontologist Rafael Delcourt agreed in 2018 that since both Limusaurus and Masiakasaurus have been found in assemblages of multiple specimens each, this suggests these small ceratosaurs lived in groups.^[40]

Paleoenvironment

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 350–400 m (1,150–1,310 ft) 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.^[1][2][41] The climate was probably highly seasonal due to monsoonal influences, with warm, wet summers and dry winters.^[42] 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.^[43]

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.

• Timeline of ceratosaur research
• 2009 in paleontology

References