Pathological features and insect boring marks in a crocodyliform from the Bauru Basin, Cretaceous of Brazil

Authors

  • UIARA G. CABRAL,

    Corresponding author
    1. Setor de Paleovertebrados, Departamento de Geologia e Paleontologia, Museu Nacional/Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, RJ 20940-040, Brazil
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  • DOUGLAS RIFF,

    1. Instituto de Biologia, Universidade Federal de Uberlândia, Campus Umuarama, Bloco 2D – sala 28, Rua Ceará, s/n, 38400-902, Uberlândia, Minas Gerais, Brazil
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  • ALEXANDER W. A. KELLNER,

    1. Setor de Paleovertebrados, Departamento de Geologia e Paleontologia, Museu Nacional/Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, RJ 20940-040, Brazil
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  • DEISE D. R. HENRIQUES

    1. Setor de Paleovertebrados, Departamento de Geologia e Paleontologia, Museu Nacional/Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, São Cristóvão, RJ 20940-040, Brazil
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E-mail: uiara.gomes@gmail.com

Abstract

The type specimen of Stratiotosuchus maxhechti (DGM 1477-R), a baurusuchid mesoeucrocodylian from the Bauru Basin (Upper Cretaceous of Brazil) displays some abnormalities that are here described. The holotype was examined macroscopically and compared with other skeletal elements of S. maxhechti and Baurusuchus salgadoensis (UFRJ DG 288-R). After this analysis, the elements with signs of alterations were subjected to a computed tomography (CT) scan exam which gave more information about them. The medial and proximal thirds of the right metacarpal V show an extensive bone growth, which modified the normal form of this element. The left metatarsals I and II exhibit an abnormal bone callus covering part of the medial third of the distal end. Based on their morphology these features are regarded as the result of two injuries of distinct natures. In the right metacarpal V, the presence of a large bone callus and a fracture, with two possible causes: post-traumatic infection or tumour. In the metatarsal I and II a case of stress fracture with a marked bone callus. Additionally, insect boring marks in the left ulna and right and left tibia of the same specimen were observed, which could be confused with pathologies. These bone changes may provide additional clues about the palaeoenvironment, such as habitat conditions, in which the specimen studied here lived.

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, S140–S151.

INTRODUCTION

Pathological changes in bone tissue are the result of imbalances in the normal equilibrium of bone resorption and formation or growth-related disorders, being the causal agents related to mechanical stress, changes in blood supply, inflammation of soft tissues, infectious diseases, hormonal, nutritional and metabolic upsets, and tumours, amongst others (White & Folkens, 2005). Skeletal diseases may be expressed as abnormal bone formation, abnormal bone destruction, abnormal bone density, abnormal bone size, and abnormal bone shape, and each of these bone expressions may occur as the only manifestation of disease in a skeleton or as a combination of one or more of the other expressions (Ortner, 2003). Buikstra & Ubelaker (1994) recognized that one of the rules to assist the diagnosis of a pathological condition is the evidence of an inflammatory reaction or process of healing, which indicates that the animal survived for some time after suffering an injury. Together with the advent of new tools and techniques, the ability to make accurate diagnoses of diseases in fossils has increased greatly, sometimes with the same methods and the same degree of certainty as in living patients (Martin & Rothschild, 1989). Thus, the correct identification of a palaeopathology can be helpful to our understanding of the origin, distribution, and evolution of a disease, and at the same time, help to understand a number of issues such as predator−prey relationships, intraspecific interactions, and disease or trauma experienced by an animal (e.g. Rothschild & Martin, 1993; Rothschild et al., 1998; Sawyer & Erickson, 1998; Tanke & Currie, 1998; Rothschild, Witzke & Hershkovitz, 1999; Hanna, 2002; Wolff, Fowler & Bonde, 2007). However, when studying diseases in fossil remains one of the major problems that we find is distinguishing them from biostratinomic and diagenetic damage (post-mortem abnormal modifications resulting from mechanical, environmental, biological, and/or chemical processes). Some post-mortem changes can mimic pathological lesions and lead to misinterpretation. Biogenic changes indicate post-mortem processes in burial sites, and provide evidence of trophic and behavioural interactions within ancient communities (Rogers, 1992; Jacobsen, 1998; Roberts, Rogers & Foreman, 2007). Insect-generated bone modifications are particularly useful in the understanding of trophic and behavioural interactions because of the extreme sensitivity of insects to local conditions and to the use of a wide array of biological materials for feeding, reproduction, and shelter (Roberts et al., 2007).

Despite an increase in studies regarding fossil vertebrates (Kellner & Campos, 1999), studies of diseases in Brazilian fossils are not very common. In the case of fossil reptiles, pathological features were mentioned only by Kellner & Tomida (2000), who observed broken ribs and a probable infection in the skull of a pterosaur, and Azevedo, Henriques & Gomide (1995), who reported rehealed ribs in a titanosaurid dinosaur from the Bauru Group. Recently several new crocodyliforms have been collected from Brazilian deposits (e.g. Carvalho, Vasconcellos & Tavares, 2007; Barbosa, Kellner & Viana, 2008; Kellner et al., 2009; Campos et al., 2011) but in none were pathological features described. Here we report some abnormal features observed in the type specimen of Stratiotosuchus maxhechtiCampos et al. 2001 (DGM 1477-R), a baurusuchid mesoeucrocodylian from the Upper Cretaceous, Bauru Basin, Brazil. They are of pathological nature, the first record of these features in a crocodyliform from Brazil. Furthermore, burrows perforating some elements were also observed and are regarded as insect borings. All these abnormalities are here described and discussed.

Institutional abbreviations

DGM, Departamento de Geologia e Mineralogia, Rio de Janeiro, Brazil; UFRJ DG, Universidade Federal do Rio de Janeiro, Departamento de Geologia.

GEOLOGICAL SETTING

The fossil remains of S. maxhechti reported here were collected in the Irapuru city outcrops (Campos et al., 2001), which are located in the west of São Paulo State, near to the junction between the SP-501 and SP-294 roads, in the south-west part of Bauru Basin. This basin is a large cratonic depression that developed during the Late Cretaceous in the central south-eastern portion of the South American Platform (Fernandes & Coimbra, 1996). It represents the Cretaceous coverage overlying the spills of the Serra Geral Formation with an area of about 370 000 km2 and a maximum preserved thickness of 300 m (Riccomini, 1997; Fernandes & Coimbra, 2000; Fernandes, 2004).

Several stratigraphical divisions of the Bauru Basin have been proposed for the São Paulo State (Soares et al., 1980; Fernandes & Coimbra, 1996; Fernandes & Coimbra, 2000) and even today there is no consensus on this subject. The classical division was proposed by Soares et al. (1980) and includes the Caiuá, Santo Anastácio, Adamantina, and Marília Formations. Fernandes & Coimbra (2000) redefined the stratigraphical division of the Bauru Basin and recognized the follow units in the west of São Paulo State: Santo Anastácio and Rio Paraná Formations (both included in the Caiuá Group) and the Bauru Group, including the Marília Formation and a reinterpretation and subdivision of the former Adamantina Formation in the Vale do Rio do Peixe, Araçatuba, São José do Rio Preto, and Presidente Prudente Formations.

Unfortunately, many fossils from the Bauru Basin were found by chance, with no precise stratigraphical control, as it is the case for the type specimen of S. maxhechti. However, outcrops of the municipality of Irapuru are considered to be present in the Presidente Prudente Formation, owing to their geographical location in the deposits of the Bauru Basin. The lithological characteristics of the matrix in which the specimen was found concur with this stratigraphical positioning.

The Presidente Prudente Formation occurs in portions of the valleys of the Peixe and Paranapanema rivers, in the region between Presidente Prudente and Adamantina cities, in the west of São Paulo State (Fernandes & Coimbra, 2000). Its thickness is about 50 m and lays gradually in interdigital mode over the Vale do Rio do Peixe Formation (Fernandes, 2004). The matrix where the fossil was included consists of a massive, fine-grained, friable sandstone with beige to light-brown coloration, bearing sparse and subrounded intraclasts of mudstone (pellets), which have a slightly darker brown coloration and millimetric diameters, with a maximum diameter of 2 cm, without carbonatic cementation. The depositional environment of the Presidente Prudente Formation is interpreted as fluvial meandering, of shallow channels and low sinuosity, with facies of alluvial plains (Fernandes & Coimbra, 2000; Fernandes, 2004).

The holotype of S. maxhechti (DGM 1477-R) is an articulated and almost complete skeleton, including the skull, with no significant distortion or compression (Campos et al., 2001; Riff, 2007). There is no record of the relative position and attitude of the skeleton on the field, but a block containing the anterior dorsal vertebrae and the right scapular girdle and member, articulated and complete (including the phalanges and carpal elements), was not prepared until the beginning of the detailed description of the skeleton (Riff, 2007). Analysing this material, we inferred that no significant transport occurred and that desiccation was taking place at the time of fossilization, as the anterior member was preserved with a strong flexion.

MATERIAL AND METHODS

By the time of the present study all elements of the holotype of S. maxhechti (DGM 1477-R) had already been prepared. They were analysed macroscopically and were compared with other skeletal elements of S. maxhechti and with two specimens of Baurusuchus salgadoensis (UFRJ DG 285-R and UFRJ DG 288-R). After this first analysis, bones with signs of alteration were subjected to a computed tomography (CT) scan exam in a GE HiSpeed CT scanner, and images were produced with slices of 1.0 and 0.6 mm thickness. Each abnormal element was described considering its location, extent, texture, and measurements of the affected area. Many of the terms and definitions here used follow those applied to the description of diseases in human bones.

DESCRIPTION AND COMPARISONS

Riff (2007) pointed out some abnormalities present in bones of the anterior and posterior limbs of the DGM 1477-R S. maxhechti specimen. The morphological comparison with other skeletal elements of S. maxhechti and with B. salgadoensis (UFRJ DG 285-R and UFRJ DG 288-R) was helpful in establishing the normal pattern of the bones and in identifying the elements that should be subjected to the CT scan technique. After a detailed analysis CT scan images of the abnormal bones, it was possible to depict, according to the origin, two types of bone alterations here classified as pathological and taphonomical disorders.

Pathological disorders

Three elements of the holotype of S. maxhechti presented pathologies: the right metacarpal V and left metatarsals I and II.

Right metacarpal V

Macroscopic examination revealed a right metacarpal V (Fig. 1A) with an extensive bone deformity of the diaphysis to the proximal epiphysis, forming a bone structure similar to a triangle. However, the proximal articular surface is well defined and has not been affected (Fig. 1A). The distal epiphysis also maintains its normal morphological pattern. The affected areas are mainly in the ventral edge, close to the proximal joint, and can be described as a roughened surface with a process of abnormal bone growth and numerous lesions (Fig. 1A). The abnormal growth increases the width of the metacarpal to 13.3 × 18.1 mm at the central shaft (normal left is 8.1 × 9.6 mm) (Fig. 1A, B). Based on this evidence it is possible to infer that the pathological process was in progress by the time of the animal's death. A large hole was also observed that crosses the metacarpal V dorsoventrally in the medial surface between the metaphysis and the proximal epiphysis. The tilted condition of the bone because of the dorsoventral displacement of the diaphysis is evident when compared to the left metacarpal V and other metacarpals of the DGM 1477-R specimen.

Figure 1.

Metacarpals V of Stratiotosuchus maxhechti (DGM 1477-R). The pathological right metacarpal V (A) and normal left one (B). In dorsal, ventral, proximal, lateral, and medial view from left to right. The thick arrow indicates the proximal articular surface that has not been affected. The thin arrow indicates the roughened surface and the bone lesions in ventral view. The black line indicates the orientation of the bones. Scale bars = 2.5 cm.

In contrast to the linear orientation of normal trabeculae, microscopic examination of the affected areas showed irregular trabeculae as are expected to occur in areas where the process of bone healing takes place (disordered trabeculae) (S. M. F. Souza, pers. comm., 2009) (Fig. 2). A slight thinning of the trabeculae and a consequent increase of the spaces amongst them was also observed (Fig. 2). It was possible for all these data to be microscopically analysed, without bone destruction, because of the exposition of the trabecular bone caused by the partial loss of cortical bone layer in the affected regions.

Figure 2.

Comparison between normal (left) and pathological (right) bone trabeculae of the metacarpals V of Stratiotosuchus maxhechti (DGM 1477-R). Increase of 1.2 × (A), 2.5 × (B), and 5.0 × (C).

The CT scan exam revealed that the cortical bone layer remained preserved for almost its entire length, even in areas where abnormal bone growth was in progress (Fig. 3). The visualization of the bone continuity is impaired in the region between the proximal metaphysis and epiphysis, suggesting a break in this bone, which is supported by the existence of a radiolucent line crossing the region. On the CT scan this area is dark in aspect, as is typical of increased bone density. Thus, the CT images support the idea that there was a displacement of the proximal end of the right metacarpal V.

Figure 3.

Computed tomography scan of the pathological right metacarpal V of Stratiotosuchus maxhechti (DGM 1477-R) in ventral view. The arrows indicate the fracture line.

Left metatarsals I and II

In contrast to the other DGM 1477-R metatarsals, the left metatarsals I and II showed signs of alteration. In both elements a bone callus could be observed in the lateral to medial surfaces, covering part of the medial third of the distal end. On metatarsal I the bone callus measures approximately 40 mm (prox-dist) by 14 mm (med-lat) (Fig. 4A); the bone callus on metatarsal II is slightly larger at 53 mm (prox-dist) by 15 mm (med-lat) (Fig. 4B). Its edges are well defined in lateral surfaces. However, in medial surfaces the edges are not well defined, merging with the normal bone surfaces. The other metatarsals of DGM 1477-R do not carry any sign of abnormality (Fig. 4C).

Figure 4.

Metatarsals of Stratiotosuchus maxhechti (DGM 1477-R). Pathological left metatarsal I (A) and II (B) and normal right metatarsal I (C). In dorsal, ventral, lateral, and medial view from left to right. Arrows indicate the bone callus. Scale bars = 2.5 cm.

The CT scan exam confirmed that the bone pattern is similar in both metatarsals I and II and in the callus (Fig. 5A–D). In some regions, the callus is fully merged into the bone placed laterally, and in other regions there is a very small space between them. In addition, breaks in some regions are regarded as taphonomic disorders in addition to the pathological fractures.

Figure 5.

Computed tomography scan of the pathological left metatarsal I of Stratiotosuchus maxhechti (DGM 1477-R).

Taphonomical disorders/insect boring marks

Taphonomical disorders were identified in the left ulna and both tibiae of the holotype of S. maxhechti.

Left ulna

The left ulna presents two boring marks in its proximal end (Fig. 6A). One, measuring 21 × 16 mm, is present in the lateral surface, being concave and semicircular in shape. It penetrates the cortical and spongy bone layers and the bone wall is completed eroded. It shows the same light brown colour as the sedimentary matrix where DGM 1477-R was included. There are no signs of bone growth and/or destruction caused by a pathological process in this area. The second boring mark (19 × 15 mm) is located medially and shows the same morphological characteristics of that previously cited, although it is smaller. There is no ornamentation in the cavities.

Figure 6.

Left ulna (A) and right (B) and left (C) tibiae of Stratiotosuchus maxhechti (DGM 1477-R) showing boring marks. In proximal, cranial, lateral, caudal, and medial view from left to right. The arrows indicate the borings. Scale bars = 2.5 cm.

CT scan images demonstrated that the borings extend into the interior of the bone in the medullar cavity, forming tunnel filled with sediments (Fig. 7).

Figure 7.

Computed tomography scan of the left ulna of Stratiotosuchus maxhechti. The arrows indicate the borings in the bones.

Right tibia

The right tibia has two boring marks in its proximal end (Fig. 6B). The anterior one (23.7 × 16.2 mm) is positioned at the cranial−medial edge of the proximal articular surface and has an irregular shape. The posterior one (17 × 16.2 mm) is located at the caudal−lateral edge of the proximal articular surface and has a circular shape. Both the anterior and posterior borings have a concave surface and the bone wall is extremely eroded, showing a light brown colour, similar to that in the left ulna, and with no ornamentation. The cortical and spongy bone layers are penetrated by both perforations and there are no signs of growth and/or bone destruction owing to any pathological process. Through a break made in the diaphysis it was possible to observe that the interior of the bone is filled with sediment identical to that of the borings and the host matrix. In the other bones of the same specimen, which are completely preserved, the innermost layer has been filled by calcite permineralization. This fact allows us to infer that this bone had its cavities filled before the process of permineralization of the other bones had begun.

The radiographic examination corroborated what was seen in the macroscopic one: the images obtained by the CT scan exam demonstrated that both the innermost layer and the two borings have an identical sedimentation pattern. These perforations, as well as those in the left ulna, form an anteroposterior tunnel filled with sediments (Fig. 8). The images also revealed that the external and interior bone layers show no signs of abnormal growth and/or bone destruction of pathological nature.

Figure 8.

Computed tomography scan of the right tibia of Stratiotosuchus maxhechti. The arrows indicate the borings in the bones.

Left tibia

The left tibia is incomplete as it lacks its distal third. A unique boring (18.3 × 16.7 mm) can be observed in the caudal edge of the proximal articular surface (Fig. 6C). Irregular in shape, its surface is concave although shallower than those in the left ulna and the right tibia, reaching only the cortical bone layer. It is also eroded and filled with sediments identical to the host matrix. There are no signs of abnormal growth and/or bone destruction of a pathological nature.

CT scan analysis showed that the cavity does not extend to the inner of the bone, being only superficial.

DISCUSSION

The observed abnormalities on the anterior and posterior limbs of the DGM 1477-R S. maxhechti specimen deviate from the osteological pattern expected for this taxon and for that reason were analysed in order to determine the cause of these changes.

The roughened surfaces of right metacarpal V suggest that the lesions were in the process of being remodelled (with absorption of the bone callus). Likewise, the bone callus in left metatarsals I and II indicate that the lesions were in the process of healing. In addition, these features were not found in any other element of S. maxhechti. These reactionary bone growths allow us to refute the possibility that the damage resulted from scavenging or another post-mortem modification, being considered instead to be a result of disease or trauma.

According to the set of characteristics found in the right metacarpal V of S. maxhechti (a radiolucent line crossing the bone, formation of irregular trabeculae, an exuberant bone callus, and the displacement of the proximal end of the bone), the differential diagnosis includes fracture, post-traumatic infection, and tumour.

Regarding bone healing in extant reptiles, little information is available; however, it appears that it occurs at a significantly slower rate when compared with birds and mammals (Mader, 1996). Bone healing in reptiles takes about 6–30 months but 4–8 weeks and 2–6 weeks in mammals and birds, respectively. There are several factors that can affect bone healing, including fracture type, patient age, environmental temperature, and nutritional status (Mitchell, 2002). Moreover, unlike mammals, which routinely produce a significant periosteal reaction in response to a bone fracture, most reptiles produce only a subtle periosteal reaction (Mitchell, 2002). Nowadays it is common to find individuals with traumatic injuries resulting from aggressive intraspecific behaviour in disputes for territory and mates. This kind of behaviour in extant crocodilian populations has been documented in the literature through direct observations based on captured animals. According to Webb & Messel (1977), several injuries observed in Crocodylus porosus originated when attacking prey, when being attacked by predators, or when involved in conflicts related to social behaviour and territoriality. Likewise, Webb & Manolis (1983) attributed the scars and injuries found in Crocodylus johnstoni to the same causes as for C. porosus. However, the right metacarpal V of the S. maxhechti presents the opposite of the pattern expected for healing in reptiles: large areas of bone destruction and new bone formation. For this reason, it is more likely that the extensive bone neoformation of the right metacarpal V was triggered from another pathological condition, causing an intense lytic and sclerotic process.

Some forms of infection and tumour affect the underlying bone structure in addition to forming a callus (Schulp et al., 2004). An infectious process can be started after a bone fracture and consequently the original shape of the bone can be strongly altered under the callus as seen in the right metacarpal V of the holotype of S. maxhechti. In addition, Schulp et al. (2004) also describe the development of pus drains, similar to the lesions observed in the metacarpal studied here. Nevertheless, sequestrum, a diagnostic characteristic of infection, is absent.

It is interesting to note that tumours (of lytic, mixed, or even sclerotic origin) may result in pathological fractures and thus the great bone formation and the fracture in right metacarpal V of S. maxhechti could be explained as the result of a cancer. Bone cancer can result in the formation of irregular trabeculae (Rothschild et al., 1999), a feature that is also found in this bone. Moreover, cancer precludes bone healing in most pathological fracture situations, which could explain the unhealed status of the fracture. According to macroscopic, microscopic, and radiological observations, these two diseases could be interpreted as post-traumatic infection and tumour, reflecting the injuries found in the right metacarpal V of S. maxhechti.

The set of bone modifications observed in both metatarsals is consistent with stress fracture. Stress fractures are alterations in bone that take place in response to unusual, submaximal, repeated stress forces (Rothschild & Martin, 1993). Stress fractures of the lower extremities most commonly involve the tibia and metatarsal bones, and although several factors appear to contribute to the development of stress fractures they generally occur as a result of a repetitive use injury that exceeds the intrinsic ability of the bone to repair itself. (Sanderlin & Raspa, 2003). Prolonged, unconditioned, strenuous activity produces progressive microfractures and promotes resorption (accelerated remodelling) of bone, which precipitates such stress fractures (Rothschild & Martin, 2006). Animal studies have demonstrated that bone subjected to repetitive cyclical loading also develops these microfractures (Reeser, 2009).

Rothschild (1988) noticed stress fracture in ceratopsian phalanges and more recently in theropods (Allosaurus and Ceratosaurus) and sauropods (Diplodocus, Apatosaurus, Camarasaurus, and Nurosaurus) (Rothschild & Martin, 2006). This kind of pathology has also been found in tyrannosaurids (Rothschild, Tanke & Ford, 2001).

The CT scan images also suggest the diagnosis of stress fracture because there is no line of fracture (which would be expected for a complete fracture), even in the inner bone layer. In the same way, the bone callus does not involve the whole bone and there is no angulation or displacement of it. Their aetiology in man typically relates to marching, heavy lifting, or prolonged standing (Rothschild, 1988). Although the S. maxhechti lesion may be related to long periods of standing, a more likely scenario is sudden exertions related to their aggressive behaviours.

Although not directly related to the animal's death, the lesions found in right metacarpal V, and in both metatarsals I and II of S. maxhechti, may have contributed to it as the ability to obtain food tends to be reduced; the animal tends to be more susceptible to other diseases and complications, and also has an increased risk of being predated.

The other three elements in DGM 1477-R, the left ulna and both tibiae, right and left, also present some abnormalities. However, although some features in these specimens suggest pathologies, such anomalies may have another origin. The differential diagnosis in this case includes abscesses, multiple myelomas, gout, erosive arthritis, and taphonomical disorders.

The presence of abscesses is a condition that is related to some types of disease such as infections and tumours. They are characterized as a lytic lesion, usually elliptical, that is orientated along the long axis of the bone and the cavity margins are typically sclerotic and sharply defined, occasionally associated with widening of the bone itself (Rothschild & Martin, 1993). However, the elements analysed here do not present any evidence of reactive sclerosis, a typical condition of an abscess.

Multiple myelomas are characterized by several ‘punched out’ holes in the bone, decreased bone density on X-rays, and by lesions with effaced/erased trabeculae (Rothschild & Martin, 2006). However, these last two characteristics cited are not observed in the specimens studied here.

Gout may have a punched-out appearance that is accentuated by a sclerotic margin and, in addition radiology is very helpful in the diagnosis of this condition because it may well demonstrate sclerotic margins, the presence of a Martel hook or, rarely, interosseous calcification (Waldron, 2009), but none of these features are observed in the specimen described here.

The bone changes in erosive arthritis are mostly confined to the hands and in radiography these changes appear as a mixture of proliferation (osteophytes) and bone erosions (Waldron, 2009), features which are not found in the left ulna or either tibiae of S. maxhechti.

Based on the observations above, the differential diagnosis of the abnormalities in the left ulna and both tibiae allowed us to discard the possibility of abscesses, multiple myelomas, gout, and erosive arthritis. Thus, the most likely explanation, supported by elimination of the others previously cited, is that the borings were generated by some kind of taphonomical disorder. The borings, however, cannot be assigned either to tooth marks, as there are no signs of crushing of bone near the perforation, or to plant roots, because they generally leave more irregular borings and cause bone fragmentation as they grow. The alterations found here can be regarded as boring marks, which are bioerosion structures produced mainly by insects. Unfortunately, the borings were not detected before the bones were extracted from the sediment, and thus the position of such borings in the outcrop context remains uncertain.

Bone modification provides a critical insight into the post-mortem history of vertebrate fossil assemblages (Roberts et al., 2007). These modifications can be caused by mechanical, environmental, chemical, and biological factors and have been well documented in bone fossils as trampling marks, tooth marks, scratch marks, weathering, breakage, and bioerosion structures (Behrensmeyer, 1978; Rogers, 1992; Jacobsen, 1998; Rogers, Krause & Curry Rogers, 2003; Fejfar & Kaiser, 2005). Bioerosion structures result from biochemical or mechanical excavation produced by an organism in consolidated substrate (rocks, trunks, shells, or bones) (Fernandes et al., 2002). The organisms producing these structures in bones may be other vertebrates or even invertebrates. Nevertheless, the form and depth of the borings found in DGM 1477-R indicate that the organisms responsible for these modifications were invertebrates, the scavengers and butchers being excluded as possible producers. Insect generators of bone modifications are useful in providing evidence of behaviour and trophic interactions within ancient communities because they are extremely sensitive to local conditions and they utilize a wide array of biological materials for feeding, reproduction, and shelter (Roberts et al., 2007).

Rogers (1992) identified the occurrence of macro-borings in bones of an undescribed species of Prosaurolophus (Hadrosauridae dinosaur) from the Upper Cretaceous of Montana, USA, suggesting the activity of carrion beetles. The borings in these bones are solitary, nontapering shafts, filled with sediment identical to the host matrix of the bone bed and with no indication of surface modification. Schwanke & Kellner (1999) registered the first occurrence of insect boring marks in Triassic bones from Brazil. These marks were recognized in a left humerus of a dicynodont that shows several cylindrical perforations with a diameter of about 6 mm. They present no preferential orientation, but each one tends to be retilineous and does not change in diameter. The borings were attributed to dermestid pupation chambers (Schwanke & Kellner, 1999). Roberts et al. (2007) reported some types of borings in dinosaur bones from continental deposits of the Upper Cretaceous Maevarano Formation of Madagascar and the Upper Cretaceous Kaiparowits Formation of southern Utah, USA, and attributed these borings to necrophagous or osteophagous insects that were presumed to have been constructed for purposes of reproduction and feeding. Dominato et al. (2009) recognized several perforations, represented by hollow oval-shaped structures (without filling), excavated in the spongy part of the bone, in vertebrae of Pleistocene mastodons of Minas Gerais State, Brazil, that were identified as being related to the ichnofossil Cubiculum ornatus, a ichnospecies associated with a dermestid (Coleoptera).

The characteristics of borings found in DGM 1477-R are very similar to those reported previously and suggest that the organism producers of the borings was a carrion insect, most likely associated to dermestids. This is supported by the aspect of the borings and by the sediment that filled the inner tunnel on the right tibia indicating that the borings were created before the fossilization of the bones. Both the borings and the innermost part of the bone are filled by sediment and therefore were not permineralized as were the other bones that still had some organic matter. The occurrence of dermestids indicates extended subaerial exposure under warm conditions and a palaeoclimate susceptible to desiccation (Rogers, 1992; Martin & West, 1995). The presence of such borings in the holotype of S. maxhechti extends the still very scarce record of insect bone borings in Brazilian fossils, and represents the first record in vertebrate fossils of the Presidente Prudente Formation.

CONCLUSIONS

The skeletal abnormalities for S. maxhechti here presented are restricted to the anterior and posterior limbs. Two diseases must be considered as possible causes of the injuries in right metacarpal V: post-traumatic infection or tumour. In left metatarsals I and II the diagnosis is a stress fracture. This can be considered the first record of this kind in crocodyliform fossils from Brazil. The presence of insect boring marks was detected in the left ulna and both tibiae, right and left. This suggests the activity of carrion insects in the Presidente Prudente Formation ecosystem, the first record of this, and expands the fossiliferous record of insect bone borings in Brazilian fossils.

ACKNOWLEDGEMENTS

We would like to thank Ms Diogenes de Almeida Campos (Museu de Ciências da Terra/DNPM, Rio de Janeiro), Dr Ismar S. Carvalho, and Dr Felipe Vasconcellos (Insituto de Geociêcias/UFRJ, Rio de Janeiro) for access to specimens, Dr Sheila M. F. M. de Souza (Instituto Oswaldo Cruz) for relevant suggestions and discussion on the early versions of the manuscript and Dr Bernardo Tessarollo (Universidade do Estado do Rio de Janeiro) for access to CT equipment. This project was partially funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (fellowship to U. G. C.) with additional support by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG, grant number APQ-00581–09 to D. R.), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grants numbers 307276/2009–0 and 501267/2008–5 to A. W. A. K.) and Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ, grant number E-26/102.779/2008 to A. W. A. K.).

Ancillary