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

Pathological features and insect boring marks ina crocodyliform from the Bauru Basin,Cretaceous of Brazilzoj_715 140..151

UIARA G. CABRAL1*, DOUGLAS RIFF2, ALEXANDER W. A. KELLNER1 andDEISE D. R. HENRIQUES1

1Setor de Paleovertebrados, Departamento de Geologia e Paleontologia, Museu Nacional/Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, So Cristvo, RJ 20940-040, Brazil2Instituto de Biologia, Universidade Federal de Uberlndia, Campus Umuarama, Bloco 2D sala28, Rua Cear, s/n, 38400-902, Uberlndia, Minas Gerais, Brazil

Received 7 June 2009; revised 11 April 2010; accepted for publication 25 October 2010

The type specimen of Stratiotosuchus maxhechti (DGM 1477-R), a baurusuchid mesoeucrocodylian from the BauruBasin (Upper Cretaceous of Brazil) displays some abnormalities that are here described. The holotype wasexamined macroscopically and compared with other skeletal elements of S. maxhechti and Baurusuchus salga-doensis (UFRJ DG 288-R). After this analysis, the elements with signs of alterations were subjected to a computedtomography (CT) scan exam which gave more information about them. The medial and proximal thirds of the rightmetacarpal V show an extensive bone growth, which modified the normal form of this element. The left metatarsalsI and II exhibit an abnormal bone callus covering part of the medial third of the distal end. Based on theirmorphology these features are regarded as the result of two injuries of distinct natures. In the right metacarpalV, 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 marksin the left ulna and right and left tibia of the same specimen were observed, which could be confused withpathologies. These bone changes may provide additional clues about the palaeoenvironment, such as habitatconditions, in which the specimen studied here lived.

2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, S140S151.doi: 10.1111/j.1096-3642.2011.00715.x

ADDITIONAL KEYWORDS: Mesoeucrocodylian palaeopathology Presidente Prudente formation tapho-nomical discorders Stratiotosuchus maxhechti.

INTRODUCTION

Pathological changes in bone tissue are the result ofimbalances in the normal equilibrium of bone resorptionand formation or growth-related disorders, being thecausal agents related to mechanical stress, changes inblood supply, inflammation of soft tissues, infectiousdiseases, hormonal, nutritional and metabolic upsets,and tumours, amongst others (White & Folkens, 2005).Skeletal diseases may be expressed as abnormal boneformation, abnormal bone destruction, abnormal bone

density, abnormal bone size, and abnormal bone shape,and each of these bone expressions may occur as theonly manifestation of disease in a skeleton or as acombination of one or more of the other expressions(Ortner, 2003). Buikstra & Ubelaker (1994) recognizedthat one of the rules to assist the diagnosis of apathological condition is the evidence of an inflamma-tory reaction or process of healing, which indicatesthat the animal survived for some time after sufferingan injury. Together with the advent of new tools andtechniques, the ability to make accurate diagnoses ofdiseases in fossils has increased greatly, sometimeswith the same methods and the same degree of cer-tainty as in living patients (Martin & Rothschild,*Corresponding author. E-mail: [email protected]

Zoological Journal of the Linnean Society, 2011, 163, S140S151. With 8 figures

2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, S140S151S140

1989). Thus, the correct identification of a palaeopa-thology can be helpful to our understanding of theorigin, distribution, and evolution of a disease, and atthe same time, help to understand a number ofissues such as predator-prey relationships, intraspe-cific interactions, and disease or trauma experiencedby an animal (e.g. Rothschild & Martin, 1993; Roths-child 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 themajor problems that we find is distinguishing themfrom biostratinomic and diagenetic damage (post-mortem abnormal modifications resulting frommechanical, environmental, biological, and/or chemi-cal processes). Some post-mortem changes can mimicpathological lesions and lead to misinterpretation.Biogenic changes indicate post-mortem processesin burial sites, and provide evidence of trophic andbehavioural interactions within ancient communities(Rogers, 1992; Jacobsen, 1998; Roberts, Rogers &Foreman, 2007). Insect-generated bone modificationsare particularly useful in the understanding of trophicand behavioural interactions because of the extremesensitivity of insects to local conditions and to the useof 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 ofdiseases in Brazilian fossils are not very common.In the case of fossil reptiles, pathological featureswere mentioned only by Kellner & Tomida (2000),who observed broken ribs and a probable infectionin the skull of a pterosaur, and Azevedo, Henriques& Gomide (1995), who reported rehealed ribs in atitanosaurid dinosaur from the Bauru Group.Recently several new crocodyliforms have been col-lected from Brazilian deposits (e.g. Carvalho, Vas-concellos & Tavares, 2007; Barbosa, Kellner &Viana, 2008; Kellner et al., 2009; Campos et al.,2011) but in none were pathological featuresdescribed. Here we report some abnormal featuresobserved in the type specimen of Stratiotosuchusmaxhechti Campos et al. 2001 (DGM 1477-R), a bau-rusuchid mesoeucrocodylian from the Upper Creta-ceous, Bauru Basin, Brazil. They are of pathologicalnature, the first record of these features in a cro-codyliform from Brazil. Furthermore, burrows perfo-rating some elements were also observed and areregarded as insect borings. All these abnormalitiesare 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 deGeologia.

GEOLOGICAL SETTING

The fossil remains of S. maxhechti reported here werecollected in the Irapuru city outcrops (Campos et al.,2001), which are located in the west of So PauloState, near to the junction between the SP-501 andSP-294 roads, in the south-west part of Bauru Basin.This basin is a large cratonic depression that devel-oped during the Late Cretaceous in the centralsouth-eastern portion of the South American Platform(Fernandes & Coimbra, 1996). It represents theCretaceous coverage overlying the spills of the SerraGeral 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 So Paulo State(Soares et al., 1980; Fernandes & Coimbra, 1996;Fernandes & Coimbra, 2000) and even today there isno consensus on this subject. The classical divisionwas proposed by Soares et al. (1980) and includes theCaiu, Santo Anastcio, Adamantina, and MarliaFormations. Fernandes & Coimbra (2000) redefinedthe stratigraphical division of the Bauru Basin andrecognized the follow units in the west of So PauloState: Santo Anastcio and Rio Paran Formations(both included in the Caiu Group) and the BauruGroup, including the Marlia Formation and areinterpretation and subdivision of the formerAdamantina Formation in the Vale do Rio do Peixe,Araatuba, So Jos do Rio Preto, and PresidentePrudente Formations.Unfortunately, many fossils from the Bauru Basin

were found by chance, with no precise stratigraphicalcontrol, as it is the case for the type specimen of S.maxhechti. However, outcrops of the municipality ofIrapuru are considered to be present in the Presi-dente Prudente Formation, owing to their geographi-cal location in the deposits of the Bauru Basin. Thelithological characteristics of the matrix in which thespecimen was found concur with this stratigraphicalpositioning.The Presidente Prudente Formation occurs in por-

tions of the valleys of the Peixe and Paranapanemarivers, in the region between Presidente Prudenteand Adamantina cities, in the west of So Paulo State(Fernandes & Coimbra, 2000). Its thickness is about50 m and lays gradually in interdigital mode over theVale do Rio do Peixe Formation (Fernandes, 2004).The matrix where the fossil was included consistsof a massive, fine-grained, friable sandstone withbeige to light-brown coloration, bearing sparse and

PATHOLOGICAL FEATURES AND INSECT BORING MARKS IN A CROCODYLIFORM FROM BRAZIL S141

2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, S140S151

subrounded intraclasts of mudstone (pellets), whichhave a slightly darker brown coloration and millimet-ric diameters, with a maximum diameter of 2 cm,without carbonatic cementation. The depositionalenvironment of the Presidente Prudente Formation isinterpreted as fluvial meandering, of shallow chan-nels 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, includingthe skull, with no significant distortion or compres-sion (Campos et al., 2001; Riff, 2007). There is norecord of the relative position and attitude of theskeleton on the field, but a block containing theanterior dorsal vertebrae and the right scapulargirdle and member, articulated and complete (includ-ing the phalanges and carpal elements), was notprepared until the beginning of the detailed descrip-tion of the skeleton (Riff, 2007). Analysing this mate-rial, we inferred that no significant transportoccurred and that desiccation was taking place at thetime of fossilization, as the anterior member waspreserved with a strong flexion.

MATERIAL AND METHODS

By the time of the present study all elements of theholotype of S. maxhechti (DGM 1477-R) had alreadybeen prepared. They were analysed macroscopicallyand were compared with other skeletal elements of S.maxhechti and with two specimens of Baurusuchussalgadoensis (UFRJ DG 285-R and UFRJ DG 288-R).After this first analysis, bones with signs of alterationwere subjected to a computed tomography (CT) scanexam in a GE HiSpeed CT scanner, and images wereproduced with slices of 1.0 and 0.6 mm thickness.Each abnormal element was described considering itslocation, extent, texture, and measurements of theaffected area. Many of the terms and definitions hereused follow those applied to the description of dis-eases in human bones.

DESCRIPTION AND COMPARISONS

Riff (2007) pointed out some abnormalities present inbones of the anterior and posterior limbs of the DGM1477-R S. maxhechti specimen. The morphologicalcomparison with other skeletal elements of S. max-hechti and with B. salgadoensis (UFRJ DG 285-Rand UFRJ DG 288-R) was helpful in establishingthe normal pattern of the bones and in identifying theelements that should be subjected to the CT scantechnique. After a detailed analysis CT scan imagesof the abnormal bones, it was possible to depict,

according to the origin, two types of bone alterationshere classified as pathological and taphonomicaldisorders.

PATHOLOGICAL DISORDERS

Three elements of the holotype of S. maxhechti pre-sented pathologies: the right metacarpal V and leftmetatarsals I and II.

Right metacarpal VMacroscopic examination revealed a right metacarpalV (Fig. 1A) with an extensive bone deformity of thediaphysis to the proximal epiphysis, forming a bonestructure similar to a triangle. However, the proximalarticular surface is well defined and has not beenaffected (Fig. 1A). The distal epiphysis also maintainsits normal morphological pattern. The affected areasare mainly in the ventral edge, close to the proximaljoint, and can be described as a roughened surfacewith a process of abnormal bone growth and numer-ous lesions (Fig. 1A). The abnormal growth increasesthe width of the metacarpal to 13.3 18.1 mm at thecentral shaft (normal left is 8.1 9.6 mm) (Fig. 1A,B). Based on this evidence it is possible to infer thatthe pathological process was in progress by the timeof the animals death. A large hole was also observedthat crosses the metacarpal V dorsoventrally in themedial surface between the metaphysis and the proxi-mal epiphysis. The tilted condition of the bonebecause of the dorsoventral displacement of the dia-physis is evident when compared to the left metacar-pal V and other metacarpals of the DGM 1477-Rspecimen.In contrast to the linear orientation of normal tra-

beculae, microscopic examination of the affected areasshowed irregular trabeculae as are expected to occurin 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 anda consequent increase of the spaces amongst themwas also observed (Fig. 2). It was possible for all thesedata to be microscopically analysed, without bonedestruction, because of the exposition of the trabecu-lar bone caused by the partial loss of cortical bonelayer in the affected regions.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 inprogress (Fig. 3). The visualization of the bone conti-nuity is impaired in the region between the proximalmetaphysis and epiphysis, suggesting a break in thisbone, which is supported by the existence of a radi-olucent line crossing the region. On the CT scan thisarea is dark in aspect, as is typical of increased bone

S142 U. G. CABRAL ET AL.


density. Thus, the CT images support the idea thatthere was a displacement of the proximal end of theright metacarpal V.

Left metatarsals I and IIIn contrast to the other DGM 1477-R metatarsals,the left metatarsals I and II showed signs of alter-ation. In both elements a bone callus could beobserved in the lateral to medial surfaces, coveringpart of the medial third of the distal end. On meta-tarsal I the bone callus measures approximately40 mm (prox-dist) by 14 mm (med-lat) (Fig. 4A); thebone callus on metatarsal II is slightly larger at53 mm (prox-dist) by 15 mm (med-lat) (Fig. 4B). Itsedges are well defined in lateral surfaces. However,in medial surfaces the edges are not well defined,merging with the normal bone surfaces. The othermetatarsals of DGM 1477-R do not carry any sign ofabnormality (Fig. 4C).The CT scan exam confirmed that the bone pattern

is similar in both metatarsals I and II and in thecallus (Fig. 5AD). In some regions, the callus is fullymerged into the bone placed laterally, and in otherregions there is a very small space between them. Inaddition, breaks in some regions are regarded astaphonomic disorders in addition to the pathologicalfractures.

TAPHONOMICAL DISORDERS/INSECT BORING MARKS

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

Left ulnaThe left ulna presents two boring marks in its proxi-mal end (Fig. 6A). One, measuring 21 16 mm, ispresent in the lateral surface, being concave andsemicircular in shape. It penetrates the cortical andspongy bone layers and the bone wall is completederoded. It shows the same light brown colour as thesedimentary matrix where DGM 1477-R wasincluded. There are no signs of bone growth and/ordestruction caused by a pathological process in thisarea. The second boring mark (19 15 mm) is locatedmedially and shows the same morphological charac-teristics of that previously cited, although it issmaller. There is no ornamentation in the cavities.CT scan images demonstrated that the borings

extend into the interior of the bone in the medullarcavity, forming tunnel filled with sediments (Fig. 7).

Right tibiaThe right tibia has two boring marks in its proximalend (Fig. 6B). The anterior one (23.7 16.2 mm) ispositioned at the cranial-medial edge of the proximalarticular surface and has an irregular shape. The

Figure 1. Metacarpals V of Stratiotosuchus maxhechti (DGM 1477-R). The pathological right metacarpal V (A) andnormal left one (B). In dorsal, ventral, proximal, lateral, and medial view from left to right. The thick arrow indicates theproximal articular surface that has not been affected. The thin arrow indicates the roughened surface and the bone lesionsin ventral view. The black line indicates the orientation of the bones. Scale bars = 2.5 cm.



posterior one (17 16.2 mm) is located at thecaudal-lateral edge of the proximal articular surfaceand has a circular shape. Both the anterior andposterior borings have a concave surface and the bonewall is extremely eroded, showing a light browncolour, similar to that in the left ulna, and withno ornamentation. The cortical and spongy bonelayers are penetrated by both perforations and thereare no signs of growth and/or bone destruction owingto any pathological process. Through a break made inthe diaphysis it was possible to observe that theinterior of the bone is filled with sediment identicalto that of the borings and the host matrix. In

the other bones of the same specimen, which arecompletely preserved, the innermost layer has beenfilled by calcite permineralization. This fact allows usto infer that this bone had its cavities filled before theprocess of permineralization of the other bones hadbegun.The radiographic examination corroborated what

was seen in the macroscopic one: the images obtainedby the CT scan exam demonstrated that both theinnermost layer and the two borings have an identicalsedimentation pattern. These perforations, as well asthose in the left ulna, form an anteroposterior tunnelfilled with sediments (Fig. 8). The images also

Figure 2. Comparison between normal (left) and pathological (right) bone trabeculae of the metacarpals V of Stratioto-suchus maxhechti (DGM 1477-R). Increase of 1.2 (A), 2.5 (B), and 5.0 (C).



revealed that the external and interior bone layersshow no signs of abnormal growth and/or bonedestruction of pathological nature.

Left tibiaThe left tibia is incomplete as it lacks its distal third.A unique boring (18.3 16.7 mm) can be observed inthe caudal edge of the proximal articular surface(Fig. 6C). Irregular in shape, its surface is concavealthough shallower than those in the left ulna and theright tibia, reaching only the cortical bone layer. It isalso eroded and filled with sediments identical to thehost matrix. There are no signs of abnormal growthand/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 pos-terior limbs of the DGM 1477-R S. maxhechti speci-men deviate from the osteological pattern expectedfor this taxon and for that reason were analysed inorder to determine the cause of these changes.The roughened surfaces of right metacarpal V

suggest that the lesions were in the process of beingremodelled (with absorption of the bone callus). Like-wise, the bone callus in left metatarsals I and IIindicate that the lesions were in the process ofhealing. In addition, these features were not found inany other element of S. maxhechti. These reactionarybone growths allow us to refute the possibility thatthe damage resulted from scavenging or another post-mortem modification, being considered instead to be aresult of disease or trauma.According to the set of characteristics found in the

right metacarpal V of S. maxhechti (a radiolucent linecrossing the bone, formation of irregular trabeculae,an exuberant bone callus, and the displacement of the

proximal end of the bone), the differential diagnosisincludes fracture, post-traumatic infection, andtumour.Regarding bone healing in extant reptiles, little

information is available; however, it appears that itoccurs at a significantly slower rate when comparedwith birds and mammals (Mader, 1996). Bone healingin reptiles takes about 630 months but 48 weeksand 26 weeks in mammals and birds, respectively.There are several factors that can affect bone healing,including fracture type, patient age, environmentaltemperature, and nutritional status (Mitchell, 2002).Moreover, unlike mammals, which routinely producea significant periosteal reaction in response to a bonefracture, most reptiles produce only a subtle peri-osteal reaction (Mitchell, 2002). Nowadays it iscommon to find individuals with traumatic injuriesresulting from aggressive intraspecific behaviour indisputes for territory and mates. This kind of behav-iour in extant crocodilian populations has been docu-mented in the literature through direct observationsbased on captured animals. According to Webb &Messel (1977), several injuries observed in Crocodylusporosus originated when attacking prey, when beingattacked by predators, or when involved in conflictsrelated to social behaviour and territoriality. Like-wise, Webb & Manolis (1983) attributed the scars andinjuries found in Crocodylus johnstoni to the samecauses as for C. porosus. However, the right metac-arpal V of the S. maxhechti presents the opposite ofthe pattern expected for healing in reptiles: largeareas of bone destruction and new bone formation.For this reason, it is more likely that the extensivebone neoformation of the right metacarpal V wastriggered 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 acallus (Schulp et al., 2004). An infectious process canbe started after a bone fracture and consequently theoriginal shape of the bone can be strongly alteredunder the callus as seen in the right metacarpal V ofthe holotype of S. maxhechti. In addition, Schulp et al.(2004) also describe the development of pus drains,similar to the lesions observed in the metacarpalstudied here. Nevertheless, sequestrum, a diagnosticcharacteristic of infection, is absent.It is interesting to note that tumours (of lytic, mixed,

or even sclerotic origin) may result in pathologicalfractures and thus the great bone formation and thefracture in right metacarpal V of S. maxhechti could beexplained as the result of a cancer. Bone cancer canresult in the formation of irregular trabeculae (Roth-schild et al., 1999), a feature that is also found in thisbone. Moreover, cancer precludes bone healing in mostpathological fracture situations, which could explain

Figure 3. Computed tomography scan of the pathologicalright metacarpal V of Stratiotosuchus maxhechti (DGM1477-R) in ventral view. The arrows indicate the fractureline.



Figure 4. Metatarsals of Stratiotosuchus maxhechti (DGM 1477-R). Pathological left metatarsal I (A) and II (B) andnormal right metatarsal I (C). In dorsal, ventral, lateral, and medial view from left to right. Arrows indicate the bonecallus. Scale bars = 2.5 cm.



the unhealed status of the fracture. According tomacroscopic, microscopic, and radiological observa-tions, these two diseases could be interpreted as post-traumatic infection and tumour, reflecting the injuriesfound in the right metacarpal V of S. maxhechti.The set of bone modifications observed in both

metatarsals is consistent with stress fracture. Stressfractures are alterations in bone that take place inresponse to unusual, submaximal, repeated stressforces (Rothschild & Martin, 1993). Stress fractures ofthe lower extremities most commonly involve thetibia and metatarsal bones, and although severalfactors appear to contribute to the development ofstress fractures they generally occur as a result of arepetitive use injury that exceeds the intrinsic abilityof the bone to repair itself. (Sanderlin & Raspa, 2003).Prolonged, unconditioned, strenuous activity pro-duces progressive microfractures and promotesresorption (accelerated remodelling) of bone, whichprecipitates such stress fractures (Rothschild &Martin, 2006). Animal studies have demonstratedthat bone subjected to repetitive cyclical loading alsodevelops these microfractures (Reeser, 2009).Rothschild (1988) noticed stress fracture in ceratop-

sian phalanges and more recently in theropods

(Allosaurus and Ceratosaurus) and sauropods(Diplodocus, Apatosaurus, Camarasaurus, and Nuro-saurus) (Rothschild & Martin, 2006). This kind ofpathology 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, thebone callus does not involve the whole bone and thereis no angulation or displacement of it. Their aetiologyin man typically relates to marching, heavy lifting, orprolonged standing (Rothschild, 1988). Although theS. maxhechti lesion may be related to long periods ofstanding, a more likely scenario is sudden exertionsrelated to their aggressive behaviours.Although not directly related to the animals death,

the lesions found in right metacarpal V, and in bothmetatarsals I and II of S. maxhechti, may have con-tributed to it as the ability to obtain food tends to bereduced; the animal tends to be more susceptible toother diseases and complications, and also has anincreased risk of being predated.The other three elements in DGM 1477-R, the left

ulna and both tibiae, right and left, also present some

Figure 5. Computed tomography scan of the pathological left metatarsal I of Stratiotosuchus maxhechti (DGM 1477-R).



abnormalities. However, although some features inthese specimens suggest pathologies, such anomaliesmay have another origin. The differential diagnosis inthis 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 infectionsand tumours. They are characterized as a lyticlesion, usually elliptical, that is orientated along the

long axis of the bone and the cavity marginsare typically sclerotic and sharply defined, occasion-ally associated with widening of the bone itself(Rothschild & Martin, 1993). However, the elementsanalysed here do not present any evidence of reac-tive sclerosis, a typical condition of an abscess.Multiple myelomas are characterized by several

punched out holes in the bone, decreased bonedensity on X-rays, and by lesions with effaced/erased

Figure 6. Left ulna (A) and right (B) and left (C) tibiae of Stratiotosuchus maxhechti (DGM 1477-R) showing boringmarks. In proximal, cranial, lateral, caudal, and medial view from left to right. The arrows indicate the borings. Scalebars = 2.5 cm.



trabeculae (Rothschild & Martin, 2006). However,these last two characteristics cited are not observedin the specimens studied here.Gout may have a punched-out appearance that is

accentuated by a sclerotic margin and, in additionradiology is very helpful in the diagnosis of thiscondition because it may well demonstrate scleroticmargins, the presence of a Martel hook or, rarely,interosseous calcification (Waldron, 2009), but none ofthese features are observed in the specimen describedhere.The bone changes in erosive arthritis are mostly

confined to the hands and in radiography thesechanges appear as a mixture of proliferation(osteophytes) and bone erosions (Waldron, 2009), fea-tures which are not found in the left ulna or eithertibiae of S. maxhechti.

Based on the observations above, the differentialdiagnosis of the abnormalities in the left ulna andboth tibiae allowed us to discard the possibilityof abscesses, multiple myelomas, gout, and erosivearthritis. Thus, the most likely explanation, sup-ported by elimination of the others previously cited, isthat the borings were generated by some kind oftaphonomical disorder. The borings, however, cannotbe assigned either to tooth marks, as there are nosigns of crushing of bone near the perforation, or toplant roots, because they generally leave more irregu-lar borings and cause bone fragmentation as theygrow. The alterations found here can be regarded asboring marks, which are bioerosion structures pro-duced mainly by insects. Unfortunately, the boringswere not detected before the bones were extractedfrom the sediment, and thus the position of suchborings in the outcrop context remains uncertain.Bone modification provides a critical insight into

the post-mortem history of vertebrate fossil assem-blages (Roberts et al., 2007). These modifications canbe caused by mechanical, environmental, chemical,and biological factors and have been well documentedin bone fossils as trampling marks, tooth marks,scratch marks, weathering, breakage, and bioerosionstructures (Behrensmeyer, 1978; Rogers, 1992; Jacob-sen, 1998; Rogers, Krause & Curry Rogers, 2003;Fejfar & Kaiser, 2005). Bioerosion structures resultfrom biochemical or mechanical excavation producedby an organism in consolidated substrate (rocks,trunks, shells, or bones) (Fernandes et al., 2002). Theorganisms producing these structures in bones maybe other vertebrates or even invertebrates. Neverthe-less, the form and depth of the borings found in DGM1477-R indicate that the organisms responsible forthese modifications were invertebrates, the scaven-gers and butchers being excluded as possible produc-ers. Insect generators of bone modifications are usefulin providing evidence of behaviour and trophic inter-actions within ancient communities because they areextremely sensitive to local conditions and theyutilize 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 Prosau-rolophus (Hadrosauridae dinosaur) from the UpperCretaceous of Montana, USA, suggesting the activityof carrion beetles. The borings in these bones aresolitary, nontapering shafts, filled with sedimentidentical to the host matrix of the bone bed and withno indication of surface modification. Schwanke &Kellner (1999) registered the first occurrence of insectboring marks in Triassic bones from Brazil. Thesemarks were recognized in a left humerus of a dicyn-odont that shows several cylindrical perforationswith a diameter of about 6 mm. They present no

Figure 7. Computed tomography scan of the left ulna ofStratiotosuchus maxhechti. The arrows indicate theborings in the bones.

Figure 8. Computed tomography scan of the right tibia ofStratiotosuchus maxhechti. The arrows indicate theborings in the bones.



preferential orientation, but each one tends to beretilineous and does not change in diameter. Theborings were attributed to dermestid pupation cham-bers (Schwanke & Kellner, 1999). Roberts et al. (2007)reported some types of borings in dinosaur bones fromcontinental deposits of the Upper Cretaceous Mae-varano Formation of Madagascar and the Upper Cre-taceous Kaiparowits Formation of southern Utah,USA, and attributed these borings to necrophagous orosteophagous insects that were presumed to havebeen constructed for purposes of reproduction andfeeding. Dominato et al. (2009) recognized severalperforations, represented by hollow oval-shapedstructures (without filling), excavated in the spongypart of the bone, in vertebrae of Pleistocene mast-odons of Minas Gerais State, Brazil, that were iden-tified as being related to the ichnofossil Cubiculumornatus, a ichnospecies associated with a dermestid(Coleoptera).The characteristics of borings found in DGM 1477-R

are very similar to those reported previously andsuggest that the organism producers of the borings wasa carrion insect, most likely associated to dermestids.This is supported by the aspect of the borings and bythe sediment that filled the inner tunnel on the righttibia indicating that the borings were created beforethe fossilization of the bones. Both the borings and theinnermost part of the bone are filled by sediment andtherefore were not permineralized as were the otherbones that still had some organic matter. The occur-rence of dermestids indicates extended subaerial expo-sure under warm conditions and a palaeoclimatesusceptible to desiccation (Rogers, 1992; Martin &West, 1995). The presence of such borings in theholotype of S. maxhechti extends the still very scarcerecord of insect bone borings in Brazilian fossils, andrepresents the first record in vertebrate fossils of thePresidente Prudente Formation.

CONCLUSIONS

The skeletal abnormalities for S. maxhechti here pre-sented are restricted to the anterior and posteriorlimbs. Two diseases must be considered as possiblecauses of the injuries in right metacarpal V: post-traumatic infection or tumour. In left metatarsals Iand II the diagnosis is a stress fracture. This canbe considered the first record of this kind in croco-dyliform fossils from Brazil. The presence of insectboring marks was detected in the left ulna and bothtibiae, right and left. This suggests the activity ofcarrion insects in the Presidente Prudente Formationecosystem, the first record of this, and expands thefossiliferous record of insect bone borings in Brazilianfossils.

ACKNOWLEDGEMENTS

We would like to thank Ms Diogenes de AlmeidaCampos (Museu de Cincias da Terra/DNPM, Rio deJaneiro), Dr Ismar S. Carvalho, and Dr Felipe Vas-concellos (Insituto de Geocicias/UFRJ, Rio deJaneiro) for access to specimens, Dr Sheila M. F. M.de Souza (Instituto Oswaldo Cruz) for relevant sug-gestions and discussion on the early versions of themanuscript and Dr Bernardo Tessarollo (Univer-sidade do Estado do Rio de Janeiro) for access to CTequipment. This project was partially funded by theCoordenao de Aperfeioamento de Pessoal de NvelSuperior (CAPES) (fellowship to U. G. C.) with addi-tional support by the Fundao de Amparo Pesquisado Estado de Minas Gerais (FAPEMIG, grant numberAPQ-0058109 to D. R.), Conselho Nacional de Desen-volvimento Cientfico e Tecnolgico (CNPq, grantsnumbers 307276/20090 and 501267/20085 to A. W.A. K.) and Fundao Carlos Chagas Filho de Amparoa Pesquisa do Estado do Rio de Janeiro (FAPERJ,grant number E-26/102.779/2008 to A. W. A. K.).

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