Traumatic alterations in the exoskeleton of glyptodonts (Cingulata, Xenarthra) and associated to behavior

doi:10.21203/rs.3.rs-4980024/v1

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Traumatic alterations in the exoskeleton of glyptodonts (Cingulata, Xenarthra) and associated to behavior

https://doi.org/10.21203/rs.3.rs-4980024/v1

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Alterations in the exoskeleton of glyptodonts have provided valuable information about the behavior of these animals. Studying the exoskeleton of the most known genera of glyptodonts, we found traumatic alterations suggestive of impact provoked by armored parts of their bodies such as the tail. We linked our findings based on the anatomy and biomechanical traits and we used X-rays and digital microscopy to identify the lesions as complementary examination to the macroscopic analysis. Here we present the first records of traumatic alterations in Hoplophorus euphractus and Propalaeohoplophorus australis and we identified more cases of alterations in Panochthus and Glyptodon. The observed alterations were fractures, deformations and perforations with some of them associated with infections. These marks on the carapaces can be associated with caudal tube impacts, and the observed damages in the tails were made by the same nature of impact. The anatomy of the striking tail and the fighting behavior was probably guided by sexual selection, where males in intraspecific combats fought for territory or mates.

Glyptodont. Exoskeleton. Traumatic alterations. Intraspecific fighting

The clade Cingulata (armadillos, pampatheres, and glyptodonts) is renowned for its distinctive bony exoskeleton, evident even in the earliest fossils of this group (Fariña 1995; Oliveira et al. 1997; Oliveira and Bergqvist 1998). Among these taxa, glyptodonts stand out for their extensive diversity, substantial body size (particularly in later evolutionary branches), and unique morphology (Zurita et al. 2016). Throughout their evolutionary history, glyptodonts displayed an increase in exoskeletal thickness related to their enlarged body sizes. Their exoskeleton is a compact structure comprising subunits of osteoderms and covers the head, back, and tail (Carlini and Zurita 2010). The articulated osteoderms make up the cephalic shield and the dorsal carapace. In the tail, they form caudal rings (as in armadillos and pampatheres) or mobile rings plus a distal caudal tube (as in glyptodonts); the caudal tube results from the complete merge of the osteoderms as observed in the carapace in adulthood (Paula-Couto 1979; Fernicola and Porpino 2012).

The idea of glyptodont tails serving as a striking weapon akin to ankylosaurid dinosaurs has been suggested particularly for species armed with caudal tubes (Arbour and Zanno 2020). Previously, Ferigolo (1992) and Fariña (1995) proposed that some glyptodont species may have used their tails for intraspecific combat; on the other hand, an alternative hypothesis suggests that the tail also could have served as a defense against predators (Alexander et al. 1999). Although lacking direct fossil evidence, Alexander et al. (1999) provided initial support for those hypotheses, documenting alterations in the carapaces of Doedicurus and Glyptodon. Nonetheless, they did not describe them. Using biomechanical calculations, Alexander (2001) and Blanco et al. (2009) demonstrated that tails of glyptodonts could be used in intraspecific fights due to their strength and mobility. More recently, Zamorano and Fariña (2021), studying caudal tubes of the genus Panochthus, concluded that the caudal tube would be more efficient in these intraspecific combats than defending against predators.

Currently, the evolutionary purpose of carapaces and caudal tubes of glyptodonts—whether for predator evasion, intraspecific combat, or both—remains unclear. There are few records of ante mortem alterations that could be of use in settling the case, but the biomechanical evidence, the increase in their body size, and the acquisition of structures such as horny spines (Zamorano and Fariña 2021 and references therein) suggest that the primary use of the exoskeleton was to attack and/or defend themselves (Arbour and Zanno 2020).

In this paper, we analyzed the exoskeleton of the most known genera of glyptodonts looking for additional evidence to reinforce the tail-club hypothesis. We identified and described traumatic alterations in carapaces and tails such as those recently proposed for ankylosaurid dinosaurs by Arbour et al. (2022), suggesting a similar behavior related to a similar anatomy. We also intend to understand the effects of these blows on the bodies of these animals, proposing a brief explanation of how glyptodonts used their tails to strike and how these armored accessories may have evolved by sexual evolution.

Institutional abbreviations: MACN-Pv, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Buenos Aires, Argentina; MCN-PV, Museu de Ciências Naturais, Secretaria do Meio Ambiente e Infraestrutura, Porto Alegre, Brasil; UFMGMJ, Museu de História Natural e Jardim Botânico, Belo Horizonte, Brasil; MLP-PV, Museo de La Plata, La Plata, Argentina.

The fossils analyzed are housed in the collections of the Museo de La Plata, La Plata city/ Argentina, Museo de Nacional de Ciencias Naturales Bernardino Rivadavia (MACN) Buenos Aires city/Argentina; and in the collection of Museu de História Natural e Jardim Botânico (MHNJB) in Belo Horizonte city, Minas Gerais state, Brazil. The materials analyzed were well-preserved components of the exoskeleton of glyptodonts with a reasonable degree of preservation. We disregarded fossils with a low degree of conservation because they provide poor information in many cases, but we included one fossil fragment previously published (Ferigolo 2007). The material consists of cephalic shields, carapaces, and tails (caudal rings and caudal tubes) deposited in the mentioned collections which met the above inclusion criteria, ranging from basal genera to representative of late diverging lineages: Propaleohophophorus, Stromaphorus, Hoplophractus, Urotherium, Eosclerocalyptus, Pseudoplophorus, Neosclerocalyptus, Panochthus, Hoplophorus, Doedicurus and Glyptodon.

We adopted the anatomical terminology for the glyptodont exoskeleton proposed by Porpino et al. (2010) and Porpino et al. (2014). To describe ante mortem alterations and analytical methods adopted, we followed the classic works on paleopathology by Baker and Brothwell (1980), Ortner (2003), Rothschild and Martin (2006), Ferigolo (2007) and Waldron (2009) as well as works on ankylosaurs, which we are comparing with glyptodonts (Arbour et al. 2022 and references therein). We also resorted to current veterinary literature when necessary to describe injuries and assist in radiological interpretations of the trauma (Piermattei et al. 2006; Thrall 2013) and detailing histopathological processes on bone recovery (Kierszerbaum and Tres 2019).

The macroscopic inspection was the initial method for detecting alterations (Ferigolo 2007). In addition to this, we radiographed the material from MLP using a portable x-ray unit Fujifilm FDR Xair (ray emitter)/ Fujifilm FDR D-EVO II (receiver panel), and a portable x-ray unit AJEX Meditech AJEX9020H (ray emitter)/ Careray CareView 750 Cw (receiver panel) for material from MHNJB. We used a digital microscope, Dino-Lite Basic, with DinoCapture 2.0 Software to observe some microanatomical features. A digital caliper with an accuracy of 0.01 mm was used to scale out the lesions.

Traumas in carapaces are primarily diagnosed by identifying fractures or partial or total loss of osteoderms, which can affect from one to several. Despite their similarities, fully applying the classification of skull fractures to carapaces is impractical due to differences in anatomical terminology. Suture is a terminology for fibrous connective tissue of the skull; for other bones, the correct term is syndesmosis (Dyce et al. 2010). Therefore, we apply syndesmosis for the articulation made by connective tissue among the osteoderms. Zurita et al. (2010) used the term synostosis to refer to the joints among the osteoderms of the dorsal region of the carapace; however, strictly speaking, that terminology is applicable only for joints that were totally merged by ossification, which, in glyptodonts, occurs in carapace of older individuals (Cuadrelli et al. 2020). Therefore, it is essential to consider that the carapace may have regions with syndesmoses and synostosis.

In addition to fractures, the syndesmoses between osteoderms can also become separated, akin to what occurs in the skull. We used the syndesmosis distance among the osteoderms as a valid metric parameter for identifying and magnifying traumatic alteration in carapaces. We omitted osteoderms clearly separated by the taphonomic process, which is common in fragmented carapaces. In most species of glyptodonts, the osteoderms show considerable morphologic variability along and across the carapace, requiring attention. Therefore, we only measured osteoderms with the same morphology to ensure no significant variation.

In certain instances, the available material was exceedingly limited or fragmented, diminishing the sample size and reducing the likelihood of discovery. The genera that showed alterations were: Panochthus, Hoplophorus, Glyptodon, and Propaleohoplophorus.

Panochthus tuberculatus

Material

MLP-PV 98-XII-1-1; MLP-PV 98-XII-1-2; MLP-PV 16–36.

We analyzed a carapace of Panochthus tuberculatus MLP-PV 98-XII-1-1) divided into five fragments. All five fragments show loss of ornamentation at some points and smooth bone response in common. Nonetheless, we found two pieces with distinct lesions. The largest is on the laterodorsal region of the carapace; its external surface shows multilocalized loss of ornamentation with evident bone response in microscopical view analyses (Fig. 1a-c) and shows a circular depression that is associated with two fracture lines starting from the lesion (Fig. 1d). Immediately on the inner side of the depressed area, there is a bone callus on the internal surface with the same circular shape as the external lesion but larger (Fig. 1e). An x-ray analysis confirmed that it was a bone callus as it shows greater radiopacity, indicating in vivo enhanced deposition of mineral material in this region (Fig. 1f), which was not observed in other unaltered areas of the carapace.

On another fragment of MLP-PV 98-XII-1-1, we found an irregular and depressed lesion featuring a circular perforation inside, accompanied by lines of fracture (Fig. 2a). The affected osteoderms within this lesion exhibit severely eroded external surfaces, resulting in a spiculated aspect, due the exposure of trabecular bone, while neighboring osteoderms show moderated erosion. Additionally, we also observed fracture lines originating from the injured area. Microscopic examination revealed bone response at the edges of the lesion and around the perforation inside this lesion (Fig. 2c). The depression disrupted the syndesmoses, leaving impressions on the internal surface (Fig. 2b), with a whitish outline, likely indicating a minor bone reaction, which is absent in unaffected areas.

This same individual has a caudal tube (MLP-PV 98-XII-1-2) where we found several alterations (Fig. 3a). MLP-PV 98-XII-1-2 has a subelliptical hole between the left lateral Figs. 1 and 2 on the dorsal side of the mid-distal region. The orifice is 5,1 mm x 6,1 mm in diameter and passes through the bone into the internal cavity (Fig. 3b). At the edge of the orifice, there is a loss of ornamentation and irregular bone tissue with signs of a bone response, which increases towards the innermost portions (3c-d). Additionally, we observed a considerable bone fragmentation obliterating part of the lateral, central, and marginal figures, but with no sign of impact since we did not observe any sinking or fractures on the surface (Fig. 3e). In the right lateral region, bone tissue loss at l1 and l3 is seen. Ventrally, in the proximal region, the ornamentation is covered by sediment, but there are at least five small pittings.

We found more alterations in another almost complete carapace of Panochthus tuberculatus (MLP-PV 16–36). There are two conical-circular perforations separated by 18 cm in the right posterolateral region perfectly lined up and surrounded by loss of bone tissue (Fig. 4a). The cranial perforation is 4 cm wide and crosses completely the carapace, generating a conical hole due to the breakage of four osteoderms; the remaining osteoderms around the hole are inclined pointing out to the interior of the carapace. The caudal perforation damages two osteoderms and is 3 cm wide and considerably deep, although it does not reach the internal region of the carapace. We also observed bone response associated with loss of ornamentation in the osteoderm in contact with these perforations.

Finally, we have identified a second alteration in MLP-PV 16–36 in the left posterolateral region, damaging six to seven osteoderms. This area was depressed, with affected osteoderms displaying complete loss of ornamentation (Fig. 4b). The lesion is slightly elliptical, resembling a shallow funnel with a central aperture and two fractures running laterally in opposite directions. Notably, the carapace shows multilocalized loss of ornamentation, varying in size and lacking a defined shape similar to MLP-PV 98-XII-1-1.

Glyptodon

Material

MACN-Pv 12718; MACN-Pv 13776; MACN-Pv 200; MCN-PV 1920

The osteoderms of the carapace of Glyptodon exhibit considerable thickness akin to Panochthus and other larger glyptodonts. However, unlike Panochthus, Glyptodon lacks a fully-developed caudal tube; instead, the tail was covered solely by caudal rings of osteoderms, with a small cluster of fused osteoderms distally, forming a sort of rudimentary caudal tube (see Zurita et al. 2018). We observed alterations in two specimens from different individuals belonging to this genus: a carapace of Glyptodon munizi (MACN-Pv 13776) and a complete tail of Glyptodon sp. (MACN-Pv 12718), with all the caudal rings well preserved. Furthermore, we re-analyzed the specimens of Glyptodon reticulatus (MACN-Pv 200) and of Glyptodon sp. (MCN-PV 1920) respectively described by Alexander et al (1999) and Ferigolo (2007), which consist in the two previously documented cases of carapace alterations attributed to intraspecific combat in the genus Glyptodon.

In the carapace MACN-Pv 13776, we observed an extensive loss of ornamentation in the left posterolateral region, resulting in a rough appearance. Additionally, perforations and parallel grooves in this area contributed to a spiculated surface (Fig. 5a). No fractures, sutural disruptions, or depressions were evident.

Upon examination of MACN-Pv 12718, we noted alterations in the caudal rings, with varying degrees of osteoderm involvement. Notably, there were more affected osteoderms on the left side than on the right, suggesting a likely pathological condition as the alterations asymmetrically affect the tail (Fig. 5b). The conical shape of the osteoderms is more pronounced from the third caudal ring to the end of the tail, some of the proximal damaged osteoderms had fragmentation of the edges (Fig. 5c-e) while the most conical osteoderms had totally or partially lost the pointed end, conferring an excavated aspect to the affected surface in the distal portion of the tail. (Fig. 5f).

Regarding the Glyptodon reticulatus specimen MACN-Pv 200 described by Alexander et al. (1999), our findings confirm the presence of a lesion in the right anterolateral region that resulted in loss of ornamentation, without accompanying depressions or fractures. In addition to these observations, we observed numerous small, irregularly shaped, and perforating lesions dispersed across the carapace. Some of these lesions exhibit a twisted appearance of the ornamentation, indicative of a bone response, while others reveal the exposure of spongy tissue without any apparent reaction.

Another specimen revisited was a 15 cm fragment from the dorsal or dorsolateral region of a carapace of Glyptodon sp. (MCN-PV 1920), originally mentioned by Ferigolo (2007). Upon examination, we identified a fracture running through the fragment accompanied by the formation of a bone callus on the internal surface (Fig. 6). Due to the small size of the fragment, the extent of the lesion is not fully discernible. However, the preserved alteration on the external surface presents as a lip-like structure at the edges of the osteoderms with bone reaction positioned above the callus on the internal surface.

Hoplophorus euphractus

Material

UFMGMJ.07.1003; UFMGMJ.07.1005

Here, we studied an almost complete carapace (UFMGMJ.07.1003) and well-preserved caudal tube (UFMGMJ.07.1005) of Hoplophorus euphractus collected in a carbonate cave at Lapa do Borges, Pedro Leopoldo city, Minas Gerais state/Brazil, and initially described by Paula-Couto (1957). This species is a mid-sized glyptodont (Porpino et al. 2010), likely endemic to the Brazilian Intertropical Region (sensu Cartelle 1999). It contrasts with larger Quaternary genera such as Panochthus, Glyptodon, or Doedicurus.

We observed a circular orifice, approximately 5 cm in diameter, in the right lateromedial region of UFMGMJ.07.1003 characterized by loss of two osteoderms (Fig. 7a). The osteoderms adjacent to the edge of the orifice have suffered almost complete loss of ornamentation, with at least three osteoderms on the caudal edge of the orifice being fractured. In contrast, those on the cranial edge remain intact but inclined inwards (Fig. 7b). As in MLP-PV 98-XII-1-1, MLP-PV 16–36 (Panochthus) and MACN-Pv-13776 (G. munizi) specimens, UFMGMJ.07.1003 shows some multifocal lesions but smaller in number and sizes; in some, as such on the left lateral region, it looks like a perforation (Fig. 7c); in others, such as on the left lateral region, these lesions resemble perforations (see Fig. 7c). Some of the fractured osteoderms display whitish edges. Microscopic analysis reveals a subtle bone response in these osteoderms, which is practically invisible to the naked eye (see Fig. 7d). X-rays indicate that the greater radiopacity of osteoderms occurs precisely at the edges delineating the orifice (see Fig. 7e), consistent with a mild bone response.

Additionally, we discovered that the syndesmoses rupture between osteoderms in UFMGMJ.07.1003 resulted in notably different distances when comparing osteoderms near and far from the lesion. The distance between unaltered osteoderms ranges between 1.98 mm and 2.2 mm, whereas upon measuring four syndesmoses close to the lesion, we found significantly larger and smaller values (see Fig. 7a; Table 1). In MLP-PV 98-XII-1-1, no significant changes were observed in the distance between syndesmoses, except for the fracture lines. Unfortunately, we could not conduct this analysis on MLP-PV 16–36 because the specimen was on public exhibition.

Table 1

measurements of the distance between the affected osteoderms of UFMGMJ.07.1003.
Distance between disrupted osteoderms
Point 1 Point 2 Point 3 Point 4	4,69 mm 3,55 mm 0,5 mm 3,28 mm
In p1 is notable that the distance was increased twice times, while the osteoderms were not entirely disconnected. The lateral region of the carapace may have some minor tension resistance for impacts where the osteoderms were not merged.

Concerning the caudal tube UFMGMJ.07.1005, we observed a circular hole approximately 1 cm in diameter in the left lateral figure with a slight irregular growth on its edges, extending into the internal space of the tube (Fig. 8a), possibly representing a cloaca. On the right side, the terminal figure has lost the bone basis for the horny spine; compared to the other three figures, this one appears lowered. X-ray examination reveals higher radiopacity at the edge and on the walls of the inside of the cloaca, which is absent in the tissue of the unaltered left terminal figure, indicating bone growth (Fig. 8b). Interestingly, we noticed that the bone tissue in the insertion regions of the tubercles (lateral and terminal figures) is denser than the tissue of the osteoderms situated between them.

Propalaeohoplophorus australis

Material

MLP-PV 91-II-25-6

Propalaehoplophorus australis is an early Miocene glyptodont without a tail tube, and its body mass is much smaller than that of Plio-Pleistocene glyptodonts (Fariña 1995). In addition, its osteoderms vary in size and thickness, being smaller and thicker in the anterior region and larger and slightly less thick in the posterior region but much smaller and thinner than those of Quaternary large-sized glyptodonts (Scott 1903).

We analyzed a partially complete carapace (MLP-PV 91-II-25-6) and found two circular alterations in the left and right anterolateral regions (Fig. 9a). On the left side, the alteration is circular, with a smooth depression damaging at least three to four osteoderms, resulting in the loss of their ornamentation (Fig. 9b). Conversely, on the right side, a circular lesion has affected at least five osteoderms, leading to complete loss of ornamentation; its edges are irregular, and the depression is broader and more marked than that on the left (Fig. 9c). Shallow grooves occur in both alterations, like those on MACN-Pv 13776, but smaller and shallower. The radiographic examinations of these alterations in MLP-PV 91-II-25-6 revealed enhanced radiopacity at the two affected points, similar to what we observed in some alterations on carapaces of Panochthus and Hoplophorus (see above) (Fig. 9d). However, unlike these latter, there were no associated perforations or grooves.

We did not find traumatic alteration in the studied material of the following taxa: Stromaphorus, Hoplophractus, Urotherium, Eosclerocalyptus, Pseudoplophorus and Neosclerocalyptus. This may be explained assuming that these animals did not have the fight behavior, or, if they had, the impacts could not provoke serious damages in the opponent. Secondly, the glyptodonts of these genera were medium sized. According to the hypothesis of the sexual selection, an increase of the body size and accessories like horns or spines are typically results of male-male fighting behavior for mates. Blanco et al. (2009) estimate that the masses of the tail of a Pseudoplophorus and Neosclerocalyptus were, respectively, about 15x and 6x less heavy than Panochthus, and although they bear caudal tube, their lateral and terminal figures are smoot, without the marked tubercles and/or striated surfaces, as in Panochthus and Hoplophorus, and probably did not support developed horny spines.

Although these groups were fully armored with compact carapace and caudal tube, there are few samples or, some cases, they were not well preserved. For Doedicurus, we also did not find new cases of alterations, however, we discuss the specimen studied by Lyddeker (1894) which presents an alteration in the dorsal region of the carapace.

Ante mortem alterations and traumas in carapaces

Alterations observed in fossils may have originated either when the animal was alive (ante mortem) or through taphonomic processes (post mortem). We have ruled out the possibility of post-mortem alterations due to the presence of bone response in all analyzed carapaces. Furthermore, we emphasize that the unequal or localized erosions of the ornamentation provide additional evidence of a non-taphonomic process. For instance, erosion caused by transport, a bioestrinomic process, may produce marks quite similar to those produced by ante mortem events. However, transport would result in some level of disarticulation of the carapace, generating small fragments and the abrasion on the osteoderms would be uniform, likely affecting all sides and both external and internal surfaces (Lima and Porpino 2018).

Circular marks on bones can also be produced by taphonomic processes such as necrophagy by insect larvae, which has been previously described in fossil bones (Dominato et al. 2009; Paes-Neto et al. 2016), or tooth marks made by scavengers. However, necrophagic agents prefer nutritious parts like long bones for their bone marrow or soft tissues instead of osteoderms. Additionally, the holes produced by arthropods are usually too small, ranging in the scale of millimeters, unlike the perforations observed in carapaces here, which vary in centimeters.

Predation behavior could leave marks on the exoskeleton, such as holes, perforations, and depressions, but we dismiss this possibility. The Quaternary glyptodonts for which we described such marks here (e.g., Glyptodon, Panochthus, Doedicurus) were massive animals, characterized by an imposing tail and weighing between 750 to 1,4000 kg (Fariña, et al 1998; Barbosa et al. 2023). Their bony armor likely represented an insurmountable barrier even for large contemporaneous predators, such as saber-toothed cats (Smilodon populator), wolves (Canis nehringi), or bears (Arctotherium angustidens) (see Alexander 2001). In MLP-PV 16–36, the two perforations we observed may suggest a bite from a saber-tooth-car, but the distance between the orifices is approximately 18 cm. In contrast, the distance between the canines of such felid is roughly 10 cm. Some authors suggest that young or small glyptodonts could be prayed by felids (Prevosti and Vizcaíno 2006), but others reject this idea (Bocherens et al. 2016; Lima et al. 2022). In any case, our study focuses on adult glyptodonts, so we will not discuss these hypotheses.

Human predation is another possibility since humans coexisted and interacted with the megafauna. Carlini et al. (2022) recorded six cases of predation on glyptodont by humans, noting that in all cases, they were struck on the skull, specifically on unprotected points uncovered by the cephalic shield. In contrast, direct blows to the carapace were likely avoided due to their ineffectiveness.

The signals observed in the first analyzed fragment belonging to the carapace MLP-PV 98-XII-1-1 indicate a deformation associated with a diastatic fracture (Fig. 1d). Fractures are complete or incomplete bone ruptures (Piermattei et al. 2006). However, in the case of MLP-PV 98-XII-1-1, there are no broken osteoderms; they are disconnected due to the massive impact that separated the syndesmoses and caused the deformation. The perforating aspect and the circular depression suggest that this trauma was caused by a spiky structure striking with high energy in a localized area of the carapace, reminiscent of the armored caudal tube with horny spines, like those in Panochthus.

Although the impact was external in the above fragment, its internal surface suffered more damage. If we assume a blow from a caudal tube is a possible cause of these lesions, we can explain this difference through histology, material strength, and energy dissipation on osteoderms/carapaces. The external surface of an osteoderm consists of a superficial zone composed of compact bone, while the middle zone is formed by trabecular bone, which has a lower mineral density (Hill 2006; Pereira et al. 2014; Araújo and Porpino 2018). The caudal tube transferred its kinetic energy to the carapace, and the direct impact on the solid superficial zone destroyed ornamentation and the syndesmoses. In contrast, the middle zone dissipated energy over a larger area in the deep zone, also causing syndesmoses disruption, resulting in more extensive damage to the internal surface. The disruption of the syndesmoses was more pronounced in H. euphrctus (Fig. 7; Table 1), while the two alterations in Panochthus (MLP-PV 98-XII-1-1) are more subtle. The size of the osteoderms may explain this difference. Panochthus osteoderms are larger in area and thickness than those of Hoplophorus, consequently, there are more connective fibers making the syndesmoses firmer and more resistant to impacts. However, we cannot conclusively determine whether this denser bone structure is an adaptation to endure impacts or if it was formed during the animal's life, potentially indicating a physiological or pathological condition.

The injuries in Glyptodon possibly share the same traumatic cause as those in Panochthus. Although individuals of Glyptodon did not possess a caudal tube, the tail tip bore a massive bunch of osteoderms forming a mini club or short tube (Zurita et al. 2010). Some authors suggest they could have used their tail to strike; however, the tail design is less efficient than the caudal tubes of Doedicurus and Panochthus, resulting in weaker blows (Fariña 1995). We noted many small and medium lesions in the carapaces of Glyptodon, while Panochthus and Hoplophorus presented fewer but broader and more severe lesions. Perhaps individuals of the Glyptodon genus increased the number of blows to compensate for the weakness of the impacts. Except for the fracture in MCN-PV 1920, this could explain the scarcity of fractures or depressions in carapaces of Glyptodon, despite the high quantity of lesions observed here in a single individual, because the carapace retained thickness and resistance to endure weak strikes.

The carapaces MACN-Pv 200 and MACN-Pv 13776 exhibited more extensive ornamentation loss than Panochthus and Hoplophorus, likely indicating another evidence of tail blows. Despite its weakness, the Glyptodon tail surface that impacts the carapace is larger than that of caudal tubes with spines, which concentrated the energy of the blow in reduced points. In MCN-PV 1920, the ornamentation of healed osteoderms with bone callus was preserved, suggesting that the impact on the carapace may have struck a nearby region. Like MLP-PV 98-XII-1-1, unaltered osteoderms next to the bone callus retained their ornamentation.

We observed that trauma recovery differs between the internal and external regions of the carapace. Slight to moderate bone response areas were observed on the external surface of the carapaces in all genera in which we identified lesions. In MCN-PV 1920 (Glyptodon) and mainly in MLP-PV 98-XII-1-1 (Panochthus), there are bone calluses on the internal surface of the affected areas of the carapaces, indicative of more extensive healing processes (Waldron 2009). A bone callus is a normal healing reaction that reconnects bones separated by trauma (Waldron 2009). Bone repair typically begins with the deposition of material to form new collagen fibers and cartilaginous tissue, forming a soft callus (Mescher 2021). Full recovery generally takes approximately 16 weeks (Rothschild and Martin 2006). Radiographs confirmed osteogenesis, as evidenced by the higher bone density, a characteristic of calcified bone callus signaling the end of recovery.

The discrepancy between the bone reactions on the external versus the internal surfaces of the osteoderms may stems from the differential vascularization between them, which seems reduced in the external surface. In addition, we suggest that the erosive lesions on the external surface of MLP-PV 98-XII-1-1 and MLP-PV 98-XII-1-2 were much more difficult or impossible to fully recover due to direct and uninterrupted contact with infectious microorganisms that slow down the healing process.

The perforations observed in the carapaces of Panochthus sp. (MLP-PV 16–36) and Hoplophorus euphractus (UFMGMJ.07.1003) represent two potential events of intraspecific fights between glyptodonts. This is the first time the MLP-PV 16–36 specimen has been paleopathologically analyzed, and regarding the perforation in UFMGMJ.07.1003, Paula-Couto proposed a taphonomic explanation for the alteration in this specimen. According to him, the carapace rested on the spine of the caudal tube in the cave environment in which they were found, and this condition caused the perforation on the former (Paula Couto 1957: Fig. 29). However, this explanation does not seem reasonable due to the great resistance of the carapaces to impacts. In addition, the x-ray of UFMGMJ.07.1003 revealed bone response in the edges of the hole, evidencing the ante mortem nature of the lesion (Fig. 7E).

We argue that the alterations in MLP-PV 16–36 and UFMGMJ.07.1003 are related to intraspecific fighting, primarily based on the presence of the lateral figures for the insertion of the horny spines in the genera Hoplophorus and Panochthus and, secondly, on the symmetry between the size of the spines and the morphology of the lesions. Furthermore, in the caudal tube, the distal tubercle on which the spine is inserted has a larger base than the proximal one (Blanco 2009: Fig. 2; Porpino et al. 2010: Fig. 2-g). If the spines were conical, as commonly suggested (Paula Couto 1979; Zurita et al. 2010), and if we maintain the proportions in the size of the tubercles based on the area of insertion, this implies that the distal spine was taller than the proximal one, which would explain why the cranial lesion was larger than the caudal one in MLP-PV 16–36, assuming that they hit each other in inverted positions (Fig. 10) Blanco et al. (2009) pointed out that the region close to the distal tubercle has higher bone density, giving it greater resistance. Furthermore, as it is situated more caudally, the torque of the clubbing movement allows the distal extremities to hit the target more powerfully. In UFMGMJ.07.1003, as there was only one perforation, only the distal spiny seems to have hit the carapace.

Finally, the distance between the two perforations in MLP-PV 16–36 is 18 cm, which is compatible with the distance between the center of the lateral figure (lf1) and the lateral figure (lf2) (= 18–19 cm) of the caudal tube belonging to the same specimen of Panochthus in the exhibition. Assuming that there is body size variation among the individuals of the same species, the difference of 1 cm is negligible in a structure that reaches 80–100 cm or even more, suggesting that the blow was delivered by a glyptodont of similar size.

We can categorize the alterations in MLP-PV 16–36 and UFMGMJ.07.1003 as a comminuted and depressed fracture. Despite observing minor bone response signs close to the lesion through microscopy and x-rays, the osteoderms that formed the perforating site must have been destroyed with the impact, generating a large space among the remaining osteoderms. This prevented the formation of bone callus, in contrast with MLP-PV 98-XII-1-1.

The alteration in the left laterodorsal region of MLP-PV 16–36 resembles two previous records attributed to traumatic injuries in carapaces of glyptodonts. The first, described by Lydekker (1894) in a specimen of Doedicurus clavicaudatus (MLP-PV 16–23), was later attributed to fighting by Alexander et al. (1999) and Fariña (2009). The second is an alteration in Glyptodon reticulatus (MACN-Pv 200) described by Alexander et al. (1999), which we review in this paper (see Glyptodon section). Unfortunately, the MLP-PV 16–23 has undergone some restorations, obscuring the alteration. Still, it was described as a circular-elliptical depressed and fractured area with loss of ornamentation in the right laterodorsal region (Lydekker 1894: plate XXVII; Fariña 2009: Fig. 1), resembling the traumatic injuries we describe here. In MLP-PV 16–36, no fractures were observed, as in the two carapaces of Glyptodon MACN-Pv 200 and MACN-Pv 13776. However, these losses of ornamentation in other points on these carapaces lead us to infer that perhaps combats between glyptodonts did not necessarily result in traumas such as fractures or depressions, but rather wounds on the carapace from blows. We reinforce this by noting that these small lesions without fractures are also very similar to those observed on the left anterolateral region of UFMGMJ.07.1003 (Fig. 7e), which has a fracture but, at the same time, exhibits small lesions not directly associated with the perforation on the right side.

Primitive glyptodonts, such as Propalaeohoplophorus australis, were medium-sized, and their tails were neither armored with spines nor completely ossified like those of Plio-Pleistocene glyptodonts. However, in the diagnosis of P. australis, the author stated: “the tail-sheat in Propalaeohoplophorus is heavy and club-like, tapering but little and ending abruptly, the tube closed by a small irregular plate” (Scott 1903: p. 108). Anatomically, the tail of P. australis would resemble that of Glyptodon clavipes, which also lacked a terminal fully developed caudal tube formed by fused osteoderms typical of the genera such as Panochthus or Hoplophorus. It is accepted that G. clavipes could strike another animal (Fariña 1995), and we provided additional evidence for this in G. munizi, a very similar glyptodont. Therefore, based on Scott´s diagnosis, we hypothesize that even though it did not have a caudal tube, apparently, the tail of P. australis, like that of Glyptodon, would have the attributes to strike another individual in the context of intraspecific fights. In addition, Scott (1903) mentioned a certain uniformity in the morphology of the tail, such as a less mobile end and spiky osteoderms also in other genera within Propalaehoplophorinae (e.g., Asterostemma, Cochlops, and others). Thus, alternatively, the damaged osteoderms observed in MLP-PV 91-II-25-6 may have been generated by disharmonious interaction with other Miocene glyptodonts. In any case, this primitive tail design and the lesions in MLP-PV 91-II-25-6, like those of Plio-Pleistocene glyptodonts, suggest that the fighting behavior was already present in basal glyptodonts during the Miocene.

Alterations in caudal tubes

Osteomyelitis

Some alterations observed in caudal tubes have an infectious cause and are possibly related to the traumatic alterations identified in carapaces or the tube itself. This is supported by the fact that the injured caudal tubes belong to the same individuals with injured carapaces, as in MLP-PV 98-XII-1-1 and UFMGMJ.07.1003. We point out that the caudal tube MACN-Pv 12718 and the carapace MACN-Pv 13776 do not belong to the same individual, but the alterations observed in the caudal rings are also consistent with traumas.

Paula-Couto (1957), when describing the material of Hoplophorus euphractus, suggested that the right terminal figure in UFMGMJ.07.1005 has been pathologically altered; unfortunately, he did not advance this interpretation. In a taxonomic review by Porpino et al. (2010), the authors identified the presence of an orifice in the left lateral figure as an abnormal structure, also possibly pathological, such as a cloaca. In MLP-PV 98-XII-1-2, the orifice is practically identical to the one observed in UFMGMJ.07.1005, and considering other cases recorded in fossils, these may represent two cases of osteomyelitis.

Osteomyelitis is an infectious disease of the medullary canal and compact bone caused by bacteria, fungi, or viruses that preferentially affect long bones (Ortner 2003). Three causes are attributed to the development of osteomyelitis: direct inoculation, hematogenous dissemination, and/or injuries in soft tissues (Lew and Waldwogel 2004; Thrall 2013).

Determining the cause of osteomyelitis in MLP-PV 98-XII-1-2 and UFMGMJ.07.1005 remains challenging, but the evidence suggests multifactorial origins. With the description of the lesions in carapaces of Panochthus e Hoplophorus, we demonstrate that glyptodonts used the caudal tube as a weapon to strike. Although we did not observe fracture lines in the caudal tubes, as observed in carapaces, likely due to their high bone density, the direct inoculation seems plausible, supported by erosions in ornamentation potentially caused by opportunistic fungal or bacterial infections. Recently, Luna et al. (2024) described lesions in a caudal vertebra of Panochthus likely related to fighting behavior. The trauma in a vertebra of the caudal tube can trigger an internal infection, commonly caused by bacteria, that has the potential to spread to soft tissues attached to the internal surface of the caudal tube. Furthermore, breaks in lateral figures of MLP-PV 98-XII-1-2 and UFMGMJ.07.1005 (as observed by Paula-Couto) possibly correlate with striking behavior.

According to Lew and Waldwogel (2004), the hematogenous form of osteomyelitis is more prevalent in infants, with adults commonly experiencing its effects primarily in the vertebrae. Glyptodonts boasted well-developed caudal vertebrae capable of resisting infection. Using an X-ray, we compared the internal areas of the proximal and distal regions in UFMGMJ.07.1005, noting a reduction in vertebral elements in the distal region, particularly where the injured lateral and terminal figures exhibit pathology (Fig. 8). Concerning the third type of osteomyelitis, we believe that struck with the caudal tube could lead to hematomas in soft tissues beneath the bone layer, triggering an intense inflammatory response. However, the rigidity and integrity of the caudal tube offer protection, rendering this hypothesis less likely.

Osteomyelitis typically affects long bones possessing a medullary canal. Its potential presence in caudal tubes of glyptodonts can be attributed to the unique anatomy of such a structure, which shares a similarity with that of long bones. In adult glyptodonts, the osteoderms in the caudal tube are wholly fused, forming a continuous bone wall where syndesmoses are imperceptible. Additionally, the space between the internal wall of the caudal tube and the vertebrae it houses was filled, in life, by soft tissues such as muscles, tendons, and fat (Alexander et al. 1999). This space filled primarily with soft tissues could function similarly to an actual medullary canal, serving as a food source for microorganisms that cause osteomyelitis.

Pitting

The loss of ornamentation in carapace MACN-Pv 13776 and the breaking of the conical osteoderms on MACN-Pv 12778 must have been caused by the same type of impact, and additionally, we identified two pathological pitting marks on the edge of a single osteoderm which could mimic the marks produced by fracturing. The pitting process creates circumvallate cavities generated horizontally by erosions in the external cortical surface that could reach the trabecular bone (Mathias et al. 2016). Previously, we mentioned that the exposure of osteoderm trabecular bone creates the risk of infection that can trigger the pitting process. In Glyptodon, this mark is similar to the marks observed by Lima and Porpino (2018), suggesting that it is infectious.

Paleopathologies and their relationship with the evolution of armored accessories.

The evolution of a robust carapace and the large size of later glyptodonts suggest a primary defense strategy against predators, owing to their intimidating appearance. This is reinforced by the presence of a carapace with a structure that seems adapted to prevent traumas (Du Plessis et al. 2018) coupled with the possession of well-developed caudal tubes that may have served as potent weapons. However, according to some studies, the caudal tube was not an efficient weapon against fast predators, such as saber-tooth cats (Blanco et al. 2009). On the other hand, due to its weight, it would have been more effective against slower animals, including other glyptodonts. The traumatic alterations we described (see above) support this hypothesis of intraspecific combat. If this latter suggestion holds, we can ask an additional question: what were they fighting for?

Besides the increased size, robust carapace, and well-developed caudal tube, other remarkable characteristics emerged in the more recent lineages of glyptodonts. These include gigantic body sizes, the presence of spines at the end of the caudal tube in certain species, and the development of a carapace composed of even thicker osteoderms capable of withstanding stronger physical impacts (Fariña 1995; Fernicola 2008; Zurita et al. 2010; Zamorano and Fariña 2021). Collectively, these features strongly suggest a combative relationship among glyptodonts, likely evolving through sexual selection.

Although not the primary focus of this study, we put forward two hypotheses about the mechanism that guided the body modifications, assuming they occurred via sexual selection. Firstly, male-male combat for territory and/or partners may have favored an increased body size and the development of attack structures (such as the caudal tube) (Freeman and Herron 2007; Elmen 2008). One strategy adopted by males is to provoke health disorders in their opponents as a consequence of wounds, mutilations, or fractures produced during fights. These injuries are more easily made when pointed structures are present, as in the armors of ankylosaurs (Arbour 2022) or late diverging glyptodonts. Secondly, the complexification of the caudal tube and the appearance of horny spines may have been driven by female preference for attractive-looking males, with features associated with vigor and grandeur that would offer protection to females and their offspring. Nonetheless, to evaluate these hypotheses, further data on tail modifications across various glyptodont species under a phylogenetically informed framework is required, a task beyond the scope of this paper.

For the first time we identified traumatic alterations associated to behavior for three new genera, being three cases for Panochthus, one case for Hoplophorus and one case for Propalaeohoplophorus australis. For Glyptodon, we have recorded the second case in the literature, however, we provided more detailed description of the lesion. As for the type of lesions, we described the first cases of perforations in two carapaces provoked by horny spines of the caudal tube of glyptodonts, the first case of a large bone callus in a traumatic event in the exoskeleton and the first cases of alterations in the tail of three species of glyptodont possibly associated with combats. Finally, the alterations in P. australis infer that, although caudal tubes have appeared in more recent glyptodonts, it is not an indispensable structure for fighting between the glyptodonts. We brought new evidence of an evolutionary convergence between ankylosaurids and glyptodonts corroborating to the hypothesis that glyptodonts were analogously capable of striking other individual using their tail, but is not determinable if the development was by the mechanism male-male interaction or female preference.

Competing interests

The authors declare no competing interests.

Funding

No funding was received to assist with the preparation of this manuscript.

Author Contribution

"All authors made significant contributions to the conception of the work, as well as to the analysis and interpretation of the data. All authors reviewed the manuscript and approved the version to be published. F.L. examined the materials deposited in the museums and prepared Figures 1 through 9".

Acknowledgement

We thank Martín L. de los Reyes, Marcelo Reguero and Susana Bargo (Museo de La Plata, La Plata, Argentina), María Belén von Baczko, Martín D. Ezcurra Agustín G. Martinelli, Laura Cruz and Juan Carlos Fernicola (Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, MACN, Buenos Aires, Argentina) and André Leandro Silva (Museu de História Natural e Jardim Botânico, MHNJB) for granting us access to the collections under their care. We additionally thank Susana Bargo for her valuable help during radiographies of the material housed in MLP with Martin E. Gaggiotti. Alexandre Liparini and Rafael Felipe da Silva for helping us with X-rays images of the material housed in MHNJB

Data availability

All data generated and analyzed during this study are included in the present article and its supplementary files.

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Traumatic alterations in the exoskeleton of glyptodonts (Cingulata, Xenarthra) and associated to behavior

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Abstract

Figures

Introduction

Materials and Methods

Results

Panochthus tuberculatus

Glyptodon

Hoplophorus euphractus

Propalaeohoplophorus australis

Discussion

Ante mortem alterations and traumas in carapaces

Alterations in caudal tubes

Osteomyelitis

Pitting

Conclusions

Declarations

Competing interests

Funding

Author Contribution

Acknowledgement

Data availability

References

Additional Declarations

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