Osteoderm histology of the Pampatheriidae (Cingulata,Xenarthra, Mammalia): Implications for systematics,osteoderm growth,and biomechanical adaptation

Pampatheres are extinct, large‐bodied cingulates, which share morphological characters with both armadillos and glyptodonts but are considered to be more closely related to the latter. The osteoderm histology of six pampathere taxa was examined and compared to the histology of other cingulate osteoderms. This study investigates the development and functional adaptation of pampathere osteoderms as well as the phylogenetic relationships of the Pampatheriidae within the Cingulata. We found that pampathere osteoderms share a uniform histological organization based on a basic diploe‐like structure. After initial stages of intramembranous growth, metaplastic ossification, that is, the direct incorporation and mineralization of pre‐existing protein fibers, plays an important role in osteoderm development and provides information on various kinds of soft tissue otherwise not preserved. The latest stages of osteoderm growth are dominated by periosteal bone formation especially in the superficial cortex. Movable band osteoderms show regular arrangements of incorporated fibers that may increase the resistance of particularly weak areas against strain. The histological composition of pampathere osteoderms is plesiomorphic in its basic structure but shows a number of derived features. A unique array of Sharpey's fibers that are incorporated into the bone matrix at sutured osteoderm margins is interpreted as a synapomorphy of pampatheres. The arrangement of dermal fibers in the deep and superficial cortexes supports the close relationship between pampatheres and glyptodonts. J. Morphol., 2012. © 2011 Wiley Periodicals, Inc.     

On the status of “Urotherium antiquum” (Ameghino) (Xenarthra,Glyptodontidae)

Within the Late Neogene Glyptodontidae of the Pampean region of Argentina, “Urotherium antiquum” was described on the basis of some associated osteoderms of the dorsal carapace, which in addition include a partial skull and left hemimandible. The diagnostic characters are located on the exposed surface of the osteoderms of the dorsal carapace which somewhat resembles those of the Pleistocene genus Neuryurus. Although the relationship of “U. antiquum” to the remaining Glyptodontidae has never been clarified, some cladistic analyses suggest a close phylogenetic affinity with the clade composed of Plohophorus + (Glyptodon + Doedicurus). A careful comparison of “U. antiquum” to well-characterized taxa with similar stratigraphic and geographic provenance reveals that no significant skull differences are observed from Plohophorus figuratus Ameghino. It seems likely that the alleged ornamentation pattern that characterizes this species was produced by a taphonomic alteration of the exposed surface of the osteoderms, a process broadly distributed in glyptodonts having a “rosette” ornamentation pattern. Finally, some characters present in the osteoderms of the type specimen of “U. antiquum” suggest that it may be a juvenile specimen. In summary, “U. antiquum” should be considered a junior synonym of P. figuratus.     

New material of Pachyarmatherium from the late Pleistocene of northeastern Brazil: insights into its morphology and systematics

A study of recently collected and other undescribed material of Pachyarmatherium brasiliense from the State of Pernambuco, Brazil, was performed, and its type material was revised, improving our understanding of this species and providing additional information on its affinities. Two fused osteoderms representing the posteriormost osteoderm row of the pectoral buckler are described for the first time in the Pachyarmatherium. Several additional specimens included buckler, border, and at least one caudal osteoderm. The relationships of Pachyarmatherium have been subject to different interpretations. We propose that the presence of some osteoderm features suggests a closer affinity with Dasypodinae/cf. Dasypodini armadillos. A key feature supporting this conclusion is the presence of complementary small figures in adjoining buckler osteoderms of Pachyarmatherium, indicating that a single scale covered portions of three contiguous osteoderms. Other features observed are related to the histological microstructure, which includes a central cortex characterized by a poorly developed cancellous bone and a deep cortex with mineralized collagen fiber bundles that are oriented roughly parallel to the deep osteoderm surface. Likewise, these histological features support its exclusion from glyptodonts and pampatheres, which show a different histological arrangement in their osteoderms.     

Osteoderm morphology and development in the nine-banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata)

Among modern mammals, armadillos (Xenarthra, Cingulata) are the only group that possesses osteoderms, bony inclusions within the integument. Along the body, osteoderms are organized into five discrete assemblages: the head, pectoral, banded, pelvic, and tail shields. The pectoral, banded, and pelvic shields articulate to form the carapace. We examined osteoderm skeletogenesis in the armadillo Dasypus novemcinctus using serial and whole-mount histochemistry. Compared with the rest of the skeleton, osteoderms have a delayed onset of development. Skeletogenesis begins as condensations of osteoblasts secreting osteoid, localized within the papillary layer of the dermis. Osteoderm formation is asynchronous both within each shield and across the body. The first osteoderms to mineralize are situated within the pectoral shield of the carapace, followed by elements within the banded, head, pelvic, and tail shields. In general, within each shield ossification begins craniomedially and proceeds caudally and laterally, except over the head, where the earliest elements form over the frontal and parietal bones. The absence of cartilage precursors indicates that osteoderms are dermal elements, possibly related to the all-encompassing vertebrate dermal skeleton (exoskeleton). The mode of development of D. novemcinctus osteoderms is unlike that described for squamate osteoderms, which arise via bone metaplasia, and instead is comparable with intramembranously derived elements of the skull.     

On the use of osteoderm features in a phylogenetic approach on the internal relationships of the Chroniosuchia (Tetrapoda: Reptiliomorpha)

Abstract: Chroniosuchians are an enigmatic Permian to Triassic group of crocodile‐like basal tetrapods. Their conspicuous dorsal osteoderm systems include most of the group’s yet documented postcranial morphological variability but have hardly been considered in cladistic approaches. Aiming at the clarification of the internal relationships of the Chroniosuchia, we have carried out a parsimony analysis including, among others, 23 morphological and osteohistological osteoderm characters and 12 chroniosuchian taxa. According to the most parsimonious trees, taxa usually referred to Chroniosuchidae form a paraphyletic succession with Madygenerpeton pustulatus and Chroniosaurus dongusensis as the basalmost chroniosuchians and Uralerpeton tverdochlebovae as the sister group of Bystrowianidae (hypothesis A). However, the concurrent hypothesis of a basal split into monophyletic subtaxa Chroniosuchidae and Bystrowianidae (hypothesis B) is only slightly less parsimonious and supported by an alternative analysis which includes embolomeres as the only reptiliomorph outgroup. Searching for the better hypothesis, we compare the respective order of branching to the order of first occurrences in the fossil record, demonstrating that hypothesis A provides a better stratigraphic fit than hypothesis B. Accordingly, the last common ancestor of the yet known chroniosuchians had a series of broad complexly interlocking ‘chroniosuchid’ osteoderms that served as a protection carapace apart from supporting the trunk during terrestrial locomotion. The later evolution of chroniosuchian carapaces was marked by a stepwise increase in flexibility and size reduction, which resulted in a loss of protective function and in a reduction in trunk support function. The flexibility increase is paralleled by the evolution of the Crocodylomorpha whose extant members do not possess as extensively interlocking osteoderm systems as some of their Mesozoic relatives.     

Biomechanics of the vertebrae and associated osteoderms of the Early Permian amphibian Cacops aspidephorus

Two series of osteoderms associated with the anterior three-quarters of the presacral vertebral column of the Early Permian temnospondylous amphibian Cacops aspidephorus have important implications for biomechanics of the axial skeleton. An internal series consists of an osteoderm fused to the distal tip of each neural spine. Lying dorsal to the internal series and overlapping each internal osteoderm is a second external series. The orientation of the zygapophyseal facets implies modest lateral flexion with limited coupled axial rotation of the column. However, the osteoderms restricted any possible lateral flexion through their inverted V-shape, strongly angled overlap between each external osteoderm and its neighbouring internal osteoderms, and the presence of a midsagittal flange on the ventral surface of each external osteoderm that fits into grooves on the anterior and posterior edges of the neighbouring internal osteoderms. This configuration allowed vertical flexion of the vertebral column with little lateral flexion. The rod-like nature of osteoderms with the anterior three-quarters of the presacral vertebrae suggests a restricted form of forward movement for Cacops unlike that of other early tetrapods.     

Palaeohistology and external microanatomy of rauisuchian osteoderms (Archosauria: Pseudosuchia)

Abstract: The presence of postcranial dermal armour is plesiomorphic for Archosauria. Here, we survey the external microanatomy and histology of postcranial osteoderms (i.e. dorsal paramedian and caudal osteoderms) of rauisuchians, a widely distributed assemblage of extinct predatory pseudosuchians from the Triassic. The osteoderms of eight rauisuchian taxa were found to be rather compact bones, which usually lack significant bone remodelling or large areas of cancellous bone. The presence of highly vascularized woven or fibrolamellar bone tissue deposited in the core areas indicates higher growth rates during earlier life stages, whereas a more compact parallel‐fibred bone matrix indicates reduced growth rates in later development. This pattern of change corroborates earlier studies on long bone histology. With the exception of a bone tissue found in the sample of Batrachotomus kupferzellensis, which might be the result of metaplastic ossification, the general mode of skeletogenesis is comparable with intramembraneous ossification. The lack of cancellous bone tissue and remodelling processes associated with bone ornamentation, as well as the predominantly intramembraneous mode of ossification, indicates that rauisuchian osteoderm formation differs profoundly from that of the osteoderms of the only extant pseudosuchian lineage, the crocodylians.     

Do the ornamented osteoderms influence the heat conduction through the skin? A finite element analysis in Crocodylomorpha

In order to assess the implication of the crocodylomorph ornamented osteoderms on the skin conduction during basking, we have performed three dimensional modeling and finite element analyses on a sample which includes both extant dry bones and well-preserved fossils tracing back to the Early Jurassic. In purpose to reveal the possible implication of the superficial ornamentation on the osteoderm heat conduction, we repeated the simulation on an equivalent set of smoothed 3D-modeled osteoderms. The comparison of the results evidenced that the presence of the apical sculpture has no significant impact on the osteoderm global conduction. Furthermore, as we also aimed to assess the influence of the inner bone porosity on the osteoderm conduction, we modified the heat equation parameters so that the 3D-modeled osteoderms successively score the compact and the cancellous bone properties (i.e. mass density, heat capacity, thermal conductivity and thermal diffusivity). Finally, we repeated the analyses using the soft-dermis properties which lead to outline that neither the degree of porosity nor the presence of the osteoderms (in itself) significantly modifies the heat conduction through the crocodylomorph skin. Consequently, as hypothesized by previous authors, if the dermal shield happens to be involved into heat capture during basking for crocodylians, this process must mainly rely on a convective effect based on the osteoderm relative degree of vascularization. This last assumption could thus explain why the crocodylians which produce little metabolic heat would carry an entire vascularized osteoderm shield.     

First Neogene skulls of Doedicurinae (Xenarthra,Glyptodontidae): morphology and phylogenetic implications

Among Glyptodontidae, Doedicurinae (late Miocene–early Holocene) includes the glyptodonts with the largest size and latest records. Doedicurinae is mainly characterised by a smooth surface of the osteoderms with large foramina, and a particular morphology of the caudal tube. All taxa except one (Doedicurus clavicaudatus) have been recognised and characterised on the basis of remains of caudal tubes and/or dorsal carapaces. This situation produced an evident overestimation of the real diversity of this group, and a taxonomic revision is needed. In fact, no Neogene skulls were known. We present and describe the first two Neogene skulls belonging to Doedicurinae (cf. Eleutherocercus antiquus). The materials come from the El Polvorín and Chapadmalal Formations, in the surroundings of Olavarría and Mar del Plata localities, respectively (Buenos Aires province, Argentina). A cladistic analysis was carried out in order to situate these materials among Glyptodontidae and inferring new synapomorphies at skull level in Doedicurinae. Cf. Eleutherocercus antiquus clusters with the Pleistocene species Doedicurus clavicaudatus showing three unambiguous synapomorphies, which in turn represents the first skull synapomorphies for Doedicurinae. Finally, the presence of cf. Eleutherocercus antiquus in the El Polvorín and Chapadmalal Formations suggests that the stratigraphic distribution of this species could include the Montehermosan–Chapadmalalan interval.     

Osteoderm histology of Proterochampsia and Doswelliidae (Reptilia: Archosauriformes) and their evolutionary and paleobiological implications

Postcranial osteoderms are commonly developed in the major lineages of Archosauriformes, including forms such as proterochampsids and doswelliids. Here, we survey the histology of osteoderms of the doswelliids Archeopelta arborensis and Tarjadia ruthae, and the proterochampsids Chanaresuchus bonapartei and Pseudochampsa ischigualastensis to understand better the morphogenesis of these skeletal elements. Whereas, the Doswelliid osteoderms possess a trilaminar organization, in which two cortices (external and basal) can be differentiated from an internal core of cancellous bone, these elements are compact structures in proterochampsids. The osteoderms of P. ischigualastensis are avascular and they consist entirely of parallel‐fibered bone. Conversely, the osteoderms of C. bonapartei are well vascularized structures composed of zones of woven‐fibered bone and annuli of parallel‐fibered bone. The rather simple microstructure observed in P. ischigualastensis osteoderms suggests that these elements grew at a constant, low rate. Compared with proterochampsids, doswelliid osteoderms possess a more complex histology, which appears to be linked to variations in the growth rate during the osteoderm formation and also to the development of the external ornamentation. A comparison of our findings with the results of earlier studies on other archosauriforms (phytosaurs and pseudosuchians) reveals that the general osteoderm histology of doswelliids bears a closer resemblance to that of phytosaurs and pseudosuchians than the proterochampsid osteoderm microstructure. If all archosauriform osteoderms are homologous structures, the closer resemblance of doswellid osteoderm microstructures to that of phytosaurs and pseudosuchians is in agreement with the hypothesis that doswellids are more closely related to archosaurs than proterochampsids. J. Morphol. 276:385–402, 2015. © 2015 Wiley Periodicals, Inc.     

A Peculiar New Pampatheriidae (Mammalia: Xenarthra: Cingulata) from the Pleistocene of Argentina and Comments on Pampatheriidae Diversity

Pampatheriidae are a group of cingulates native to South American that are known from the middle Miocene to the lower Holocene. Two genera have been recognized between the lower Pleistocene and the lower Holocene: Pampatherium Gervais and Ameghino (Ensenadan, Bonaerian and Lujanian, lower Pleistocene–lower Holocene) and Holmesina Simpson (Blancan, Irvingtonian, upper Pliocene–lower Holocene). They have been mainly differentiated by their osteoderm morphology and cranio-dental characters. These taxa had a wide latitudinal distribution, extending from the southern part of South America (Península Valdés, Argentina) to North America (Florida, USA). In this contribution, we describe a new genus and species of Pampatheriidae for the lower and middle Pleistocene of Buenos Aires Province and for the upper Pleistocene of Santa Fe Province (Argentina).The new taxon is represented by disarticulated osteoderms, one skull element, two thoracic vertebrae and a right femur and patella. It has extremely complex osteoderm ornamentations and particular morphological characters of the cranial element and femur that are not found in any other species of the family. This new taxon, recorded in the lower–middle Pleistocene (Ensenadan Stage/Age) and in the upper Pleistocene–early Holocene (Lujanian Stage/Age), is incorporated to the Pleistocene mammal assemblage of South America. Finally, the Pampatheriidae diversity is greater during the Lujanian Stage/Age than the Ensenadan Stage/Age.     

Bone microstructures and mode of skeletogenesis in osteoderms of three pareiasaur taxa from the Permian of South Africa

The extinct parareptilian clade of pareiasaurs was in the past often presented to constitute a morphocline from larger, less armoured forms to smaller, well armoured forms, indicating that the osteoderm cover became an increasingly prominent aspect in the post‐cranial skeleton of these animals. Here, we describe microanatomical and microstructural aspects of osteoderms of the three pareiasaur taxa Bradysaurus, Pareiasaurus and Anthodon from the Permian of South Africa. A generalized mode of osteoderm formation, consistent with intramembraneous skeletogenesis, is hypothesized to be present in all pareiasaurs. Few characters are shared between pareiasaur dermal armour and turtle shell bones and osteoderms. Otherwise, there is strong evidence from microanatomy and histology (i.e. absence of structures that formed via metaplasia of dermal tissue) that indicates nonhomology between pareiasaur dermal armour and the armour of living eureptiles. Analysis with bone profiler revealed no clear connection between bone compactness and lifestyle in the amniote osteoderm sample.     

Micromorphology of osteoderms in Dasypodidae (Cingulata,Mammalia): Characterization and 3D-reconstructions

Osteoderms are present in a variety of extinct and extant vertebrates, but among mammals, the presence of osteoderms is essentially restricted to armadillos (Cingulata, Dasypodidae). Osteoderms have been proposed to exhibit a variety of functionalities in Dasypodidae, mainly protection and thermoregulation, and they have been considered as one of the synapomorphies of this group. In this study, we use high-resolution microcomputed tomography to describe the osteoderm micromorphology of several extant species of Dasypodidae in a comparative context. This study allowed the identification, 3D-reconstruction and volume quantification of different internal structures of osteoderms as well as their interrelations. This detailed characterization of the internal osteoderm morphology was compared in a phylogenetic context to assess the evolutionary trends of the species involved. This enables the identification of distinctive patterns for the most widely recognized clades, the Dasypodinae and Euphractinae with a morphological homogeneity in the microstructure of their osteoderms, in comparison with Tolypeutinae where it has not been possible to establish a common morphological pattern. The most important features for linage differentiation is the degree of compaction of the osteoderms, the number of cavities and the development of hairs. It is likely that the differential development of the various structures occurred as adaptive response to climate changes.     

An Overview of the Presence of Osteoderms in Sloths: Implications for Osteoderms as a Plesiomorphic Character of the Xenarthra

The presence of osteoderms in the skin of some extinct sloths and in cingulates (armadillos, pampatheres, and glyptodonts) has often been considered a pleisomorphic character of the Xenarthra. While osteoderms are known from the earliest cingulates, they are absent in most sloths including the two extant taxa and only appear late in their fossil record. Osteoderms are currently only reported from five genera of mylodonts and two megatheres, out of the over 100 currently recognized genera of sloths. Consequently, rather than a plesiomorphic character of the Xenarthra, which has been secondarily lost in sloths, it is more likely that osteoderms in sloths are the result of parallel evolution to the cingulates that independently evolved in one, possibly two different sloth clades.     

Histological variability in fossil and recent alligatoroid osteoderms: Systematic and functional implications

Statements about morphological variation in extinct taxa often suffer from insufficient sampling that can be remedied by taking advantage of larger sample sizes provided by related, extant taxa. This analysis quantitatively and qualitatively examines histological and morphological variation of osteoderms from extant and extinct alligatoroid specimens. Statistically significant differences were correlated with changes in osteoderm size and shape. These differences are independent of position on the body, taxonomy, or evolution. Histological variation in alligatoroid osteoderms is due to morphological constraints on the elements themselves, and not taxonomic differences. This has implications for the recognition of histological characters in the osteoderms of extinct archosaur groups that lack extant representatives. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

A chroniosuchid from the Triassic of Kyrgyzstan and analysis of chroniosuchian relationships

A nearly complete skull and associated osteoderms from the Middle/Upper Triassic Madygen Formation of Kyrgyzstan are referred to a new chroniosuchid genus and species. The new taxon is characterized by a parabolic skull outline, pustular ornamentation, tabular‐squamosal contact, marked postparietal embayments, and the lack of an antorbital fontanelle. The palate is only preserved in part, showing broad palatines and ectopterygoids. Presence of a preorbital fenestra and characteristic osteoderm morphology are synapomorphies shared with all other chroniosuchids. According to the phylogenetic analysis performed, the new chroniosuchid nests with Chroniosaurus, with which it shares the wide, transversely extended osteoderms and pustular ornamentation. The chroniosuchians are robustly supported as a natural group, but their position within the reptiliomorph (stem‐amniote) clade is not adequately understood. Whereas the parasphenoid is similar to that of anthracosaurs, most other characters support a higher nesting of chroniosuchians within the stem‐amniotes. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 160 , 515–530.     

Phylogenetic relationships among families of the Scaphopoda (Mollusca)

Phylogenetic relationships among families in the molluscan class Scaphopoda were analysed using morphological characters and cladistic parsimony methods. A maximum parsimony analysis of 34 discrete characters, treated as unordered and equally weighted, from nine ingroup terminal taxa produced a single most parsimonious tree; supplementary analyses of tree length frequency distribution and Bremer support indices indicate a strong phylogenetic signal from the data and moderate to minimally supported clades. The traditional major division of the class, the orders Dentaliida and Gadilida, is supported as both taxa are confirmed as monophyletic clades. Within the Dentaliida, two clades are recognized, the first comprised of the families Dentaliidae and Fustiariidae, the second of the Rhabdidae and Calliodentaliidae; together, these groups comprise a third clade, which has the Gadilinidae as sister. Within the Gadilida, a nested series of relationships is found among [Entalinidae, [Pulsellidae, [Wemersoniellidae, Gadilidae]]]. These results lend cladistic support to earlier hypotheses of shared common ancestry for some families, but are at variance with other previous hypotheses of evolution in the Scaphopoda. Furthermore, analysis of constituent Gadilinidae representatives provide evidence for paraphyly of this family. The relationships supported here provide a working hypothesis that the development of new characters and greater breadth of taxonomic sampling can test, with a suggested primary goal of establishing monophyly at the family level.