Volume 299, Issue 7 p. 897-906
Evolutionary Biology
Free Access

An Injured Psittacosaurus (Dinosauria: Ceratopsia) From the Yixian Formation (Liaoning, China): Implications for Psittacosaurus Biology

B.P. Hedrick

Corresponding Author

B.P. Hedrick

Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, Pennsylvania, USA

Department of Biology, University of Massachusetts—Amherst, Amherst, Massachusetts, USA

Correspondence to: B.P. Hedrick, Department of Biology, University of Massachusetts—Amherst, Amherst, Massachusetts, USA. E-mail: [email protected]Search for more papers by this author
C. Gao

C. Gao

Dalian Natural History Museum, Dalian, China

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A.R. Tumarkin-Deratzian

A.R. Tumarkin-Deratzian

Department of Earth and Environmental Science, Temple University, Philadelphia, Pennsylvania, USA

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C. Shen

C. Shen

Dalian Natural History Museum, Dalian, China

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J.L. Holloway

J.L. Holloway

Department of Bioengineering, University of Pennsylvania, Philadelphia, Pennsylvania, USA

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F. Zhang

F. Zhang

Dalian Natural History Museum, Dalian, China

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K.D. Hankenson

K.D. Hankenson

Department of Small Animal Clinical Sciences, Michigan State University, East Lansing, Michigan, USA

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S. Liu

S. Liu

Dalian Natural History Museum, Dalian, China

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J. Anné

J. Anné

School of Earth, Atmospheric, and Environmental Sciences, University of Manchester, Manchester, UK

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P. Dodson

P. Dodson

Department of Earth and Environmental Science, University of Pennsylvania, Philadelphia, Pennsylvania, USA

School of Veterinary Medicine, Department of Animal Biology, University of Pennsylvania, Philadelphia, Pennsylvania, USA

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First published: 29 April 2016
Citations: 21

ABSTRACT

We describe a Psittacosaurus specimen from the Lujiatun beds of the Yixian Formation in Liaoning, China with an abnormality on its left fibula. Although a large number of Psittacosaurus specimens are known, only a single example of a pathologic Psittacosaurus has been previously noted. The specific pathology in the current specimen is believed to be a healed fibular fracture as assessed through a combination of gross morphology, microcomputed tomography (microCT), and histology data. The fracture can be identified using microCT, but the degree of remodeling and the stage of fracture repair are best determined histologically. The fracture callus is made up of radially oriented spokes of woven bone in a cartilage matrix and the original cortical bone prior to the fracture has been largely eroded. A transverse histologic section taken at the level of the fracture shows the displacement of the proximal and distal parts of the fibula. The Psittacosaurus appears to have survived the break considering the deposition of circumferential non-pathologic bone at the periosteal surface outside of the callus. The combination of gross morphological description, microCT data, and histologic data allowed for a full diagnosis of the abnormality. While some previous authors have preferred gross morphological description above other methods for assessing paleopathologies, it is evident based on this specimen that an amalgam of techniques provides greater clarity to paleopathology diagnoses. Although this Psittacosaurus lived in an environment with many predators, it was able to survive with a fracture on its hindlimb, which undoubtedly would have impacted its locomotion. Anat Rec, 299:897–906, 2016. © 2016 Wiley Periodicals, Inc.

Psittacosaurus is a small basal ceratopsian dinosaur from the Early Cretaceous of Asia (Sereno, 2010). It is one of the most speciose dinosaur genera known with eight named species and is known from hundreds of complete specimens (Sereno, 2010; Hedrick and Dodson, 2013). Given the large number of specimens across a range of body sizes and degrees of preservation, a substantial amount of work has been done concerning psittacosaur biology including ontogeny (Erickson and Tumanova, 2000; Erickson et al., 2009; Hedrick et al., 2014), integumentary structures (Lingham-Soliar, 2008; Lingham-Soliar and Plodowski, 2010), jaw mechanics (Tanoue et al., 2009), and also pathologies (Lü et al., 2007).

Despite the number of psittacosaur skeletons known, only one example of a pathology in a Psittacosaurus specimen (JZMP-V-11) has previously been described (Lü et al., 2007). The majority of examples of paleopathologies in dinosaurs have been found for theropods (Molnar et al., 2001; Rothschild et al., 2001; Rothschild and Tanke, 2005; Farke and O'Connor, 2007; Hone and Tanke, 2015). However, previous occurrences of pathologies in ceratopsians have been found including a pathologic ceratopsian phalanx (Rothschild, 1988) and several pathologies found in Albertan ceratopsids (Tanke and Rothschild, 2010). Vertebral pathologies such as hemivertebrae (Witzmann et al., 2008), numerous cases of diffuse idiopathic skeletal hyperostosis (Chinsamy-Turan, 2005), and healed neural spines (Tanke, 1989; Straight et al., 2009) have been described in ornithischians as a whole.

Studies of dinosaur paleopathologies have generally been confined to gross morphological description rather than description in concert with either microcomputed tomography (microCT) or bone histology data (Chinsamy-Turan, 2005). Waldron (2009) suggests that morphological description should be preferred over other methods and makes the claim that it is easier to diagnose pathologies on the basis of overall gross morphology. However, Anné et al. (2014) recently analyzed a fractured Allosaurus phalanx using both histology and synchrotron imaging revealing microstructural and geochemical changes central to the fracture repair process, which allowed for better diagnosis of the injury and a better understanding of fracture repair in general. Further, Witzmann et al. (2008) and Farke and O'Connor (2007) both used CT data to assess dinosaur pathologies and Straight et al. (2009) used a combination of CT data and bone histology to assess pathologic hadrosaur neural spines. Although paleopathology has traditionally been done primarily through morphological description, methods such as CT and bone histology can often help to identify abnormalities and pathologies, especially fractures. These techniques can further be used to assess the degree of remodeling and the stage of healing of the fracture, which are often not readily apparent through morphological description alone.

Studies of paleopathology are important for imparting a better understanding of how extinct animals lived and died. We describe a pathologic Psittacosaurus (DMNH D2596) that survived a fibular fracture using gross morphological description, microCT, and histologic analysis. Given the combination of methods used, this study has implications for dinosaur paleopathology as a whole; it also has implications for understanding the biology of Psittacosaurus. We discuss the injury in terms of its impact on the stance and gait of Psittacosaurus and we compare the injury to those of other dinosaurs that also suffered fibular fractures. This includes a reassessment of another Psittacosaurus specimen (JZMP-V-11) that has a fibular swelling similar to DMNH D2596 (Lü et al., 2007).

Institutional Abbreviations

DMNH—Dalian Natural History Museum, Dalian, Liaoning, China; FMNH—Field Museum of Natural History, Chicago, USA; JZMP—Jinzhou Museum of Paleontology, Liaoning, China; NMC—Canada Museum of Nature, Ottawa, Canada; USNM—National Museum of Natural History, Washington DC, USA.

MATERIALS AND METHODS

We examined the right and left fibulae of a psittacosaur (DMNH D2596). DMNH D2596 is stored at the Dalian Museum of Natural History in Dalian, Liaoning, China. The specimen is from the Lujiatun beds of the Yixian Formation (∼123 Ma, He et al., 2006) and is referable to P. lujiatunensis (Hedrick and Dodson, 2013). The lengths of the femora for DMNH D2596 are 125 mm (left) and 127 mm (right). This size corresponds to an age of ∼6 years based on growth curves derived from P. lujiatunensis histology (Erickson et al., 2009). The femoral circumference around the midshaft of the femur is ∼45 mm. The left and right fibulae both measure 132 mm in total length. During the casting process, both fibulae broke just distal to midshaft. Only the proximal half of the fibulae were used for the analysis as the pathology was confined to the proximal fourth of the left fibula.

Microcomputed CT scans of both the left (Fig. 1A, B) and right fibulae (Fig. 1C,D) were taken at Philadelphia's Veterans Affairs Medical Center using a Scanco Medical VivaCT 75 μCT scanner with X-ray acquisition settings at 70 kVp and 115 μA. Scans were performed using a 20.5 μm isotropic voxel size and an integration time of 381 ms. Scanco computer software was used to create three-dimensional reconstructions of the scanned tissue. MicroCT was used to access the internal architecture of the pathology and to determine the best possible locations for thin section sampling.

Details are in the caption following the image

MicroCT scans for the affected fibula (A) with longitudinal cross-section (B) and the normal fibula (C) with longitudinal cross-section (D) (Scale = 25 mm). Red arrows indicate the prefracture cortical bone in the affected fibula. (E) Close up of the cross-sectional view of the bony callus in (A). Blue lines show the original bone wall prior to the break. The red line shows the displacement as a result of the fracture (Scale = 5 mm).

Histologic sections were taken at Temple University. Four transverse sections and two longitudinal sections were taken on the proximal end of the pathologic fibula and one transverse section and two longitudinal sections were taken on the nonpathologic fibula (Fig. 2). We used the microCT scan as a guide for histologic sampling as was done by Straight et al. (2009). Transverse sections on the pathologic and normal fibula were labeled P1–4 and N1 proximal to distal respectively and longitudinal sections were labeled PL1–2 and NL1–2 proximal to distal respectively. A section was taken at the level of a displacement found on the microCT scan on the pathologic fibula (P2) and another section was taken at the same level on the nonpathologic fibula (N1) for comparison. Additional sections were taken proximal (P1) and distal (P3) to the displacement site on the pathologic section. Another section was taken midshaft on the pathologic fibula (P4) to see how the bone was affected far from the site of displacement. Additionally, proximal and distal longitudinal sections were taken on the proximal halves of the pathologic (PL1, PL2) and nonpathologic (NL1, NL2) fibulae. These sections together gave insight into how the microstructure of the pathologic fibula was affected at a distance from the displacement site. The nonpathologic fibula offered a control sample.

Details are in the caption following the image

The proximal halves of the left affected fibula (A, B) in lateral and caudal views and right normal fibula (C, D) in lateral and cranial views of DMNH D2596 showing the locations where histologic sections were taken. The affected fibula was sectioned transversely three times through the callus and once distal to the callus. The normal fibula was sectioned transversely once at the same level as the callus on the affected fibula. Both fibulae were sectioned longitudinally both proximal and distal to the middle sections (Scale = 25 mm).

The samples were cut using an Isomet 11-1180 low speed saw given the small size of the bones. Nine individual slices were mounted on 25 × 50 mm2 slides. Slides were viewed on a Nikon Eclipse 6600 Pol petrographic microscope fitted with a Nikon DXM1200F digital camera and were visualized under crosspolarized light with a lambda filter (Figs. 3, 4). Crosspolarized light gives an added advantage of showing the degree of bone development as higher birefringence patterns demonstrate more organized, mature lamellar bone. Methods for thin sectioning follow Chinsamy and Raath (1992) and bone microstructural terminology follows Francillon-Veilliot et al. (1990).

RESULTS

Based on gross morphology, there is a large swelling on the proximal left fibula near the insertion of the m. iliofibularis (Hedrick and Dodson, 2012; Maidment and Barrett, 2012). The size of the swelling dissipates quickly proximally and distally such that the proximal fibular head and the midshaft do not greatly differ from the normal right fibula. Based on the combination of techniques used, it is clear that the cause of the swelling on the pathologic fibula was due to a fracture. The microCT data reveal two dense longitudinal regions towards the center of the bone representing the original cortical bone wall prior to the fracture (Fig. 1B). A less dense callus surrounds this original cortical bone (Fig. 1B). To aid description, we term the original cortical bone wall the “prefracture cortical bone” to distinguish it from the callus. The normal fibula has much thicker cortical bone at the level of the fracture than the affected fibula suggesting that the pre-fracture cortical bone was partially eroded after the fracture (Fig. 1D). In the center of the callus on the affected fibula, there is displacement of one of the prefracture longitudinal cortical regions suggesting the location of fracture (Fig. 1E). Although the microCT data and overall morphology revealed a likely cause for the swelling (i.e., a fracture callus), it did not allow for a more thorough examination of the stage of fracture repair nor how the bone remodeled after the fracture.

Bone histology was used in order to understand the microstructural changes during fracture repair. The transverse section P2 was taken at the probable fracture site (Fig. 2A,B). This section revealed two small oval regions of cortical bone within the callus, which represent the remodeled prefracture remnants of both the proximal and distal shaft segments. Both the proximal pre-fracture fibula remnant and distal fibula remnant preserve portions of their cortical fibrolamellar bone, which strongly fluoresce under cross-polarized light and are easily distinguished from the callus tissue (Fig. 5A). The majority of the pre-fracture cortical bone and the entirety of the original medullary cavities have been heavily resorbed with large erosional cavities. These erosional cavities are evident in the callus region outside of the prefracture remnants as well. The callus region is primarily made up of radially oriented spokes of bone, some of which extend to the periosteal surface. These radial spokes are made up of woven bone and strongly fluoresce under crosspolarized light, likely demonstrating a higher level of organization than the surrounding callus (Fig. 6A). However, this could also be due to a higher degree of mineralization than the surrounding callus. The woven bone spokes also contain numerous randomly oriented osteocyte lacunae (Fig. 6B). The callus tissue itself has no evidence of chondrocytes, so it is not possible to positively demonstrate that it is a calcified cartilage matrix, but this is the most likely interpretation. Section P1 preserves only the proximal fibula remnant, as it is proximal to the fracture site (Fig. 3). However, it shows a similar organization with a thin cortical bone prefracture remnant, which is heavily eroded, surrounded by radially oriented bone that extends to the periosteal surface. Section P3 shows a similar organization to both sections P1 and P2, though it primarily preserves the distal pre-fracture remnant. However, there is a faint remnant of the proximal prefracture fibula suggesting a slight angle to the fracture rather than a perfect transverse break (Fig. 5B). There are clear radial outgrowths of bone in the callus, as in the other callus sections (Fig. 5C). At the midshaft, section P4 shows a more normal microstructure with radially reticular oriented primary osteons and lines of arrested growth (LAGs). However, towards the periosteal surface there is a sequence of radially oriented bone (Fig. 5D). Outside of that zone, radially reticular bone complete with LAGs continues to the periosteal surface. We consider the radial bone pathologic bone growth related to the callus formation rather than normal radial bone and a result of the injury, despite being such a far distance from the fracture site. Erickson and Tumanova (2000) note radial bone deposition in addition to reticular bone in the femora of P. mongoliensis at 7 years old. However, Erickson and Tumanova (2000) did not examine fibulae. Zhao et al. (2013) expanded Erickson and Tumanova's (2000) classification to include P. lujiatunensis and did consider fibulae in their study. However, at no point during the normal fibula growth cycle did they find radial bone. Six LAGs are evident in section P4 suggesting that the animal was 6 years old.

Details are in the caption following the image

Transverse sections of the proximal half of the affected fibula. The most proximal section (P1) shows the normal cortical bone of the fibula prior to the break. The original cortical bone is heavily eroded along the endosteal wall of the medullary cavity and is secondarily filled with erosional cavities. Outside of the original bone wall, radial bone extends to the edge of the callus. P2 shows two partially overlapping cortical bone walls of the fibula, one with the same location in P1 and one with the same location in P3. This section was taken at the level of the fracture seen in the microCT scan and confirms the displacement of proximal and distal bone segments demonstrated by the microCT scan. As in P1, the inside of the pre-fracture cortical bone wall is dominated by heavy erosion along the endosteal surface. P3 shows the distal pre-fracture cortical bone wall with a trace of the proximal original cortical wall showing that the fracture proliferated distally at a slight angle. Histologic bone tissues are similar to those in P1 and P2. All proximal sections have large radial spokes of woven bone perforating the callus tissue. P4 is much more distal than P1–P3 at the midshaft, but still shows some radial bone along nearly the entire outer edge demonstrating that the remodeling related to the fracture extended across the entire proximal half of the fibula. There are also six LAGs in section P4 (scale for the fibula = 50 mm; scale for the sections = 5 mm).

For comparison with the fracture site, the right normal fibula was sectioned at the level of the fracture (Figs. 2C,D, 4B). Similar to more proximal sections in other dinosaurs, including Psittacosaurus, the section was primarily composed of trabecular bone with only a small rim of cortical bone along the outer bone surface (Erickson et al., 2009; Zhao et al., 2013, 2016). The section has two clear circumferential LAGs in the cortical region and has circumferentially oriented primary osteons. It does not display any features that would be unexpected in a normal, healthy Psittacosaurus.

Details are in the caption following the image

Each histologic section laid out showing the locations of close-up figures seen in Fig. 5. The longitudinal sections also reveal the extent of the callus as it progresses proximally and distally (scale = 25 mm).

In addition to the transverse sections, two longitudinal sections were made of the proximal halves of the right and left fibulae, both proximal and distal to the transverse sections. The proximal end of the affected fibula appears normal and does not display any pathologic features (Fig. 4A). However, further distally on the proximal longitudinal section (PL1) at the level of the callus, there is a clear division and reorientation of bone relating to the fracture (Fig. 5F). The pre-fracture fibula is largely eroded, though there is a clear cortical bone remnant. Although section PL1 retains little prefracture cortical bone, the distal longitudinal section (PL2) has relatively thicker prefracture cortical bone that becomes more expansive distally. Near the fracture, there is clear radially oriented bone in the callus region. The thickness of the radially oriented bone diminishes distally with the reduction of the callus. Similar to what is visible in section P4, the distal end of section PL2 has a thin layer of circumferentially oriented bone along the outer cortical region outside of the pathologic bone demonstrating normal growth rather than pathologic growth at the time of death (Fig. 5E). The outer normal bone growth on the affected fibula is very similar to what is seen on the normal fibula (Fig. 4B), which is made up of longitudinal and circumferentially oriented canals.

Details are in the caption following the image

(A) The proximal and distal pre-fracture cortical bone walls from section P2 showing the displacement due to the fracture. (Scale = 1 mm). (B) The remnant of the proximal cortical bone fragment distal to the break from section P3. (Scale = 200 µm). (C) The pre-fracture cortical bone wall (upper left) with radial bone extending perpendicular to the prefracture cortical bone wall throughout the callus. (Scale = 200 µm). (D) The distal most transverse section (P4) with inner nonpathologic bone showing LAGs and a simple reticular osteonal arrangement with an abrupt change to radial bone marking the callus. There is also outer nonpathologic bone at the periosteal surface suggesting that the callus has completed healing and normal bone deposition has restarted (Scale = 200 µm). (E) The distal longitudinal section (PL2) showing inner circumferential bone, a change to radial bone, and then outer circumferential bone similar to what is seen in section P4. (Scale = 200 µm). (F) The proximal longitudinal section (PL1) showing inner circumferential bone and extensive outer radial canals at the level of the callus (scale = 200 µm).

Details are in the caption following the image

(A) The radial outgrowth of bone extending towards the periosteal surface in the callus. The blue represents the original prefracture fibula embedded in the callus with large, white erosional cavities within the original fibula. Scale = 1 mm. (B) A close-up of the radial spokes of bone showing that they are emerging directly from the prefracture cortical bone. Black osteocyte lacunae are present in the radial outgrowths (white arrow). No chondrocytes are evident in the callus matrix. Scale = 200 μm.

DISCUSSION

The process of fracture healing is well understood in terms of gross overall morphological changes, though the exact process of how fractures heal is still an open field of research (e.g., cell signaling during healing). After a fracture occurs, bone goes through a four-stage process similar to embryonic skeletogenesis (Ferguson et al., 1999; Waldron, 2008; Schenker et al., 2014; Stewart et al., in press). The inflammatory phase occurs for 3–4 days after the fracture and is marked by the formation of a fracture hematoma and the release of inflammatory mediators, which initiate the repair process. The second phase is the early callus phase, which can last up to several weeks after the fracture. There are a number of substages involved in the early callus phase relating to the release and condensation of chondrocytes from mesenchymal stem cells (Schenker et al., 2014). When there is excess motion at the site of the injury, a cartilage callus forms as the primary mode of regeneration (Ferguson et al., 1999). When the bone is stabilized, healing is done primarily through intramembranous ossification (Ferguson et al., 1999). The mature callus phase occurs when the cartilaginous early callus begins to mineralize and becomes vascularized. The final phase is the remodeling phase, which can last for several months to years. The bone remodels from woven bone to lamellar bone and the callus degrades eventually restoring the original cortical structure.

Although the general process of bone healing is relatively conservative within vertebrates, the timing of the fracture healing phases and architecture of the calluses can differ between groups (Pritchard and Ruzika, 1950). Birds and mammals form a much smaller and more ossified callus than reptiles, which results in quicker recovery, but a longer period of immobility (Pritchard and Ruzika, 1950; Redig, 1986; Cooper, 2002). Birds can take this condition to the extreme with some cases (stable fracture) showing minimal callus formation, suggesting primary rather than secondary callus formation (Redig, 1986). Alternatively, reptiles develop a large, mostly fibrous callus that enables union with less periosteal new bone growth than what is seen in mammals (Pritchard and Ruzika, 1950; Mader, 2006). This allows reptiles to move a short period of time after injury, but slows down the speed at which the bone reaches its initial strength (Bennett, 1989; Mader, 2006). These differences are important to consider in studies of dinosaur paleopathologies since the reptilian or avian condition could be present. In the case of DMNH D2596, the presence of a large cartilaginous callus may suggest a more reptilian mode of healing. However, fracture injuries in other dinosaurs including basal birds will need to be studied systematically using advanced imaging techniques such as microCT and bone histology in order to better evaluate whether dinosaurs exhibit the avian condition or if it evolved further down the avian lineage.

Another specimen of Psittacosaurus, JZMP-V-11 was described as having a similar pathology, a large swelling on the proximal fibula, but the pathology was instead diagnosed as necrotic bone caused by tuberculosis and the authors noted no sign of a fracture based on a morphological description (Lü et al., 2007). Although tuberculosis is common in both captive and wild avians, it is strictly degenerative, identified by small lesions or “pits” (Keymer, 1972; Cooper, 2002). The swelling on JZMP-V-11 is morphologically very similar to that on DMNH D2596 with the exception of a depression on one side of the swelling noted by Lü et al. (2007), which may be related to a fracture complication. It is possible that the swelling in JZMP-V-11 is related to a fracture rather than tuberculosis given the similar location, which could suggest that this was a point of weakness in the hindlimb of Psittacosaurus and was susceptible to fractures. Duff (1985) found the insertion of the m. iliofibularis to be a site of weakness in the broiler fowl.

Fibular fracture calluses have been reported in other dinosaurs including the distal end of the fibula of Allosaurus (USNM 4734; Gilmore, 1920), Tyrannosaurus (FMNH PR2081; Larson, 1991; Molnar et al., 2001), and Gorgosaurus specimens (NMC 2120; Lambe, 1917; Molnar et al., 2001) among others. Fibular fractures make up 10–15% of fractures in Albertan tyrannosaurs (Tanke and Currie, 1998). Rothschild (1988) notes that the majority of healed fractures are found on dinosaurian carnivores rather than herbivores, possibly due to increased predation on injured herbivores. Fractures that resulted in death prior to healing would likely not be identifiable and would appear indistinguishable from taphonomic breaks. Other than JZMP-V-11 and now DMNH D2596, no definitive pathologies have previously been reported in Psittacosaurus in spite of the large sample size for Psittacosaurus. DMNH D2596 was not only injured, but survived its injury as is apparent from the deposition of non-pathologic bone along the periosteal surface at midshaft (Fig. 5D).

The break in DMNH D2596 occurred proximally on the bone at the insertion site of the m. iliofibularis (Maidment and Barrett, 2011; Hedrick and Dodson, 2012). The m. iliofibularis is a hindlimb retractor and knee flexor muscle. Therefore an injury to this region of the fibula in DMNH D2596 would have potentially caused locomotion problems, especially considering the degree of displacement evident in DMNH D2596. There is some argument as to the bipedality of Psittacosaurus, though the majority of studies posit that it was primarily bipedal after reaching age three (Maidment and Barrett, 2012; Zhao et al., 2013; Hedrick et al., 2014). Thus, an injury to its hindlimb may have caused a postural shift from bipedality to facultative quadrupedality in DMNH D2596. Modern adult primates do not generally survive major fractures to limb bones in the wild and healed fractures tend to occur only in young animals (Bulstrode et al., 1986). Duff (1985) found that fibular fractures in the broiler fowl often healed though pseudarthrosis was also common following callus formation. However, numerous obligatory bipedal dinosaurs apparently survived injuries to their fibulae for at least some period of time (Molnar et al., 2001). Twenty-five percent of total pathologies in a study of theropods were found in the hindlimb with the fibula being much more commonly injured than the femur or tibia, but with pedal injuries dominating (Molnar et al., 2001). Therefore, some authors have suggested that the fibula is not a weight bearing bone in dinosaurs (Molnar et al., 2001; Lü et al., 2007). The tibia supports the fibula and the tibia may have acted as a natural splint. A shorter healing time was observed for fractured radii in extant pigeons when the ulna remained intact (Newton and Zeitlin, 1977). Clark et al. (1999) describe an oviraptorid with a large fracture callus on its ulna that showed no displacement and no break in the radius, which may suggest that the radius may have formed a natural splint. The tibia and fibula are weight bearing so the situation is not perfectly analogous, but this may explain the prevalence of healed fibular fractures in dinosaurs. Given that some large theropods evidently survived with fibular fractures including a Gorgosaurus that survived a fibular longitudinal fracture that extended at least 10 cm down the bone (Tanke and Rothschild, 2001), it is not necessary for Psittacosaurus to have adopted a facultative quadrupedal posture as a result of the injury.

DMNH D2596 survived a break to its hindlimb and healed to the point where it started to deposit nonpathologic bone (Fig. 5D), an event uncommon in some modern animals (Bulstrode et al., 1986) and evidently in herbivorous dinosaurs (Rothschild, 1988). It is not possible to know how DMNH D2596 was able to survive this injury in light of the large number of predators in its community, but it suggests that the fibula was not weight bearing and that the tibia may have acted as a natural splint allowing for a shorter healing period.

Although it is necessary to be cautious when diagnosing paleopathologies given the uncertainty even in modern clinical studies as well as the limitation of working only with osteological elements (Waldron, 2009), the use of multiple techniques can help to clarify the causes of pathologies as has been demonstrated in this study. Had we used morphological description alone, it would not have been possible to positively identify the abnormality on DMNH D2596 as a fracture. Therefore we urge the use of techniques such as microCT and histology in concert with morphologic description to better identify the causes of paleopathologies.

ACKNOWLEDGMENTS

The authors are thankful for helpful discussion from Sam Cordero (University of Pennsylvania) and Eric Morschhauser (Drexel University). They thank Dennis Terry (Temple University) for access to the microscope used for this study and Jim Ladd (Temple University) for help with thin sectioning equipment. They acknowledge the research division within Philadelphia Veterans Affairs Medical Center for use of their microCT.