Tiny steps towards greater knowledge: An osteological review with novel data on the Atlantic Forest toadlets of the Brachycephalus ephippium species group

Brachycephalus is a small, endemic genus of anurans that occur throughout the Brazilian Atlantic Forest. Recent analyses corroborated the monophyly of two species groups within this genus (B. ephippium and B. pernix), whereas the B. didactylus group appears to be polyphyletic. Herein, we compare and describe the skeletal system of all species from the Brachycephalus ephippium species group. We investigated diagnostic characters that are potentially useful to delimit similar species, confirmed the previously proposed genus definition and added six extra characters. We propose an osteological diagnosis for each species of the B. ephippium group, evaluating and describing intraspecific variations. Our results suggest that adults of B. ephippium group have ornamented parotic plates, ornamented post-orbital crests, absence of quadratojugal and neopalatines, distal end of the otic ramus of squamosal expanded towards the parotic plate, reduced zygomatic ramus of the squamosals, posterolateral projection of the crista parotica, presence of ornamented spinal plates (except B. alipioi) and ornamented paravertebral plates. We highlighted the importance of including more than one specimen per species when dealing with miniaturized taxa. A comparison with other Brachycephalus species groups and with Ischnocnema was also provided. Lastly, we suggest some characters to be included in future phylogenetic analysis.     

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.     

The development of cephalic armor in the tokay gecko (Squamata: Gekkonidae: Gekko gecko)

Armored skin resulting from the presence of bony dermal structures, osteoderms, is an exceptional phenotype in gekkotans (geckos and flap-footed lizards) only known to occur in three genera: Geckolepis, Gekko, and Tarentola. The Tokay gecko (Gekko gecko LINNAEUS 1758) is among the best-studied geckos due to its large size and wide range of occurrence, and although cranial dermal bone development has previously been investigated, details of osteoderm development along a size gradient remain less well-known. Likewise, a comparative survey of additional species within the broader Gekko clade to determine the uniqueness of this trait has not yet been completed. Here, we studied a large sample of gekkotans (38 spp.), including 18 specimens of G. gecko, using X-rays and high-resolution computed tomography for visualizing and quantifying the dermal armor in situ. Results from this survey confirm the presence of osteoderms in a second species within this genus, Gekko reevesii GRAY 1831, which exhibits discordance in timing and pattern of osteoderm development when compared with its sister taxon, G. gecko. We discuss the developmental sequence of osteoderms in these two species and explore in detail the formation and functionality of these enigmatic dermal ossifications. Finally, we conducted a comparative analysis of endolymphatic sacs in a wide array of gekkotans to explore previous ideas regarding the role of osteoderms as calcium reservoirs. We found that G. gecko and other gecko species with osteoderms have highly enlarged endolymphatic sacs relative to their body size, when compared to species without osteoderms, which implies that these membranous structures might fulfill a major role of calcium storage even in species with osteoderms.     

Novel data on aetosaur (Archosauria,Pseudosuchia) osteoderm microanatomy and histology: palaeobiological implications

One of the most striking features of aetosaurs is the possession of an extensive bony armour composed of dorsal, ventral and appendicular osteoderms. With the purpose of establishing the main histological changes during ontogeny and the degree of histological variation within the armour, we analysed the bone histology of dorsal (paramedian and lateral), ventral and appendicular osteoderms from different taxa from the Late Triassic of South America, including Aetosauroides scagliai, Aetobarbakinoides brasiliensis and Neoaetosauroides engaeus. Histological data support an intramembranous origin for osteoderms. Nevertheless, evidence for metaplastic ossification (i.e. structural fibres) at advanced ontogenetic stages, in at least some elements, is also present. A variant type of parallel fibred bone, which we have named ‘crossed parallel fibred bone’, is characterized for aetosaurs. In this pseudosuchian group, osteoderms exhibit very important microstructural changes during ontogeny, which can be useful for determining ontogenetic stages from isolated elements. Histological data suggest a relatively early onset of sexual maturity among aetosaurs. Microanatomical analysis from different taxa reveal that having high values of compactness is the plesiomorphic condition for Aetosauria. The notably increased compactness of the osteoderms does not appear to be related to size, ontogeny, sex or reproductive status of the individuals. Although a high degree of compactness of osteoderms and other bones has been considered as evidence for an aquatic lifestyle in vertebrates, such an inference contradicts the current concept of a fully terrestrial lifestyle in aetosaurs.     

A new metriorhynchid crocodylomorph from the Lower Kimmeridge Clay Formation (Late Jurassic) of England,with implications for the evolution of dermatocranium ornamentation in Geosaurini

A new metriorhynchid crocodylomorph from the Lower Kimmeridge Clay Formation (Kimmeridgian, Upper Jurassic) of England is described. This specimen, a three‐dimensionally preserved skull and left mandibular ramus, is referred to a new species: T orvoneustes coryphaeus sp. nov. Within the genus Torvoneustes, T . coryphaeus sp. nov. is unique as it has a long anteromedial process of the frontal, ornamented dermatocranium, and the supraorbital notch forms a strongly acute angle. Our phylogenetic analysis confirms the placement of this specimen in Torvoneustes. The dentition of T . coryphaeus sp. nov. , like that of the type species, has a blunt apex, crown basal–mid regions with numerous tightly packed apicobasally aligned ridges, and apical region with an anastomosed pattern of ridges that interact with the carinae. Within Thalattosuchia these dental characteristics are only found in Torvoneustes and the teleosaurid Machimosaurus. The heavily ornamented dermatocranium of T . coryphaeus sp. nov. is in contrast to the unornamented (nasals and frontal)–lightly ornamented (maxillae and premaxillae) pattern seen in Torvoneustes carpenteri. Curiously, this pattern of reduction and loss of dermatocranium ornamentation is also observed in Metriorhynchus, Dakosaurus, and the subclade Rhacheosaurini. We hypothesize that the ‘smooth’ dermatocranium of Late Jurassic metriorhynchids evolved independently in each subclade (parallel evolution), and would have reduced drag, thereby making locomotion through water more energy efficient. © 2013 The Linnean Society of London     

A new species of Acynodon (Crocodylia) from the upper cretaceous (Santonian–Campanian) of Villaggio del Pescatore,Italy

Abstract: The new species Acynodon  adriaticus is described on the basis of remains from the Santonian–Campanian of Villaggio del Pescatore (Trieste, NE Italy). This species differs in several cranial features from Acynodon  iberoccitanus, the only other Acynodon species whose cranial osteology is known in detail. The absence of maxillary and dentary caniniform teeth coupled with the presence of enlarged molariform teeth suggests that Acynodon probably fed on slowly moving hard‐shelled prey. Moreover, the new materials reveal for the first time the morphology of some postcranial elements of Acynodon: in particular, medial‐most paravertebral osteoderms that are characterized by two keels. A new cladistic phylogenetic analysis resolves the previously reported polytomy among the basal Globidonta: Acynodon is recognized as the most primitive globidontan. This genus may represent the geologically oldest known globidontan. The fact that Acynodon has been found only in Europe and that the outgroup of Globidonta, the Diplocynodontinae, is mainly known from Europe, suggests that globidontans may have originated in Europe and not in North America as previously supposed.     

Systematic and ecological wood anatomy of Neotropical Schefflera (Araliaceae), with an emphasis on the Didymopanax group

Wood anatomy has been investigated from 35 species belonging to the Neotropical clade of the polyphyletic genus Schefflera (Araliaceae), representing three of the five subgroups (Didymopanax, Crepinella and Sciodaphyllum). The species examined are rather uniform in their wood structure, sharing the presence of scalariform and simple perforation plates, septate fibres and scanty paratracheal axial parenchyma. The observed variation in many wood characters showed statistically significant differences relative to latitude, climate and, especially, vegetation types. In particular, the intervessel pits are larger in species from higher latitudes and in seasonally dry habitats than those from lower latitudes and rainforests. Latitudinal and ecological trends in the variation of vessel element lengths, bar numbers on perforation plates, intervessel pit sizes and ray widths may be at least partially explained as effects of adaptation to drier environments in the course of dispersal outside the Amazonian region and diversification in the Atlantic Forest subclade and the Savannic subclade within the Didymopanax group. The occurrence of a granular annulus on the intervessel pit membranes in S. chimantensis and S. sprucei (both of the Crepinella group) is the first record of this feature in Araliaceae. In comparisons of Neotropical Schefflera with the other major clades of Schefflera sensu lato, wood anatomical diversity is consistent with the polyphyly of this genus based on molecular phylogenetic analyses. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 452–475.     

Evolution of skull and body shape in Triturus newts reconstructed from three‐dimensional morphometric data and phylogeny

To explore the relationship between morphological change and species diversification, we reconstructed the evolutionary changes in skull size, skull shape, and body elongation in a monophyletic group of eight species that make up salamander genus Triturus. Their well‐studied phylogenetic relationships and the marked difference in ecological preferences among five species groups makes this genus an excellent model system for the study of morphological evolution. The study involved three‐dimensional imagery of the skull and the number of trunk vertebrae, in material that represents the morphological, spatial, and molecular diversity of the genus. Morphological change largely followed the pattern of descent. The reconstruction of ancestral skull shape indicated that morphological change was mostly confined to two episodes, corresponding to the ancestral lineage that all crested newts have in common and the Triturus dobrogicus lineage. When corrected for common descent, evolution of skull shape was correlated to change in skull size. Also, skull size and shape, as well as body shape, as inferred from the number of trunk vertebrae, were correlated, indicating a marked impact of species' ecological preferences on morphological evolution, accompanied by a series of niche shifts, with the most pronounced one in the T. dobrogicus lineage. The presence of phylogenetic signal and correlated evolutionary changes in skull and body shape suggested complex interplay of niche shifts, natural selection, and constraints by a common developmental system. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 243–255.     

Sunosuchus (Archosauria, Crocodyliformes) from the Toutunhe Formation (Middle Jurassic) of the Southern Junggar Basin (Xinjiang, NW-China)

A new specimen of the widespread Middle Jurassic to Lower Cretaceous Asian gonipholidid crocodilian genus Sunosuchus is described on the basis of a partial skeleton from the Upper Toutunhe Formation (Middle Jurassic, ?Bathonian-Callovian) of Liuhonggou, SW of Urumqi, Xinjiang Uygur Autonomous Region, People’s Republic of China. The specimen is represented by a partial mandible, teeth, vertebrae, limb and girdle bones and osteoderms. It can be distinguished from other nominal species of the genus by a unique combination of characters: slightly heterodontous dentition, strongly sculptured posteroventral part of the mandible, short fenestra mandibularis, convex dorsal surface of the retroarticular process, keeled cervical vertebral centra and ventral osteoderms with a distinctive sculpture of wide pits and narrow ridges. The heterodontous dentition is a potential autapomorphy of this form. The new specimen is closest in morphology to material described recently from the Callovian of Kirghisia as Sunosuchus sp. It represents the second Middle Jurassic record of the genus, the first crocodile from the Toutunhe Formation, the first substantial crocodile find from the Mesozoic of the Southern Junggar Basin, and the first Middle Jurassic record of Sunosuchus from China. This extends both the paleobiogeographical distribution of the genus in Asia and its stratigraphic distribution in China considerably.     

Osteoderm morphology in recent and fossil euphractine xenarthrans

The presence of osteoderms within the integument, forming a carapace, is one of the most distinctive features of armadillos with the external morphology of these elements forming the basis of most systematic schemes. This is especially true for fossil taxa, where these elements are most frequent in the palaeontological record. A detailed study of osteoderms from the cephalic shield and different regions of the dorsal armour of Chaetophractus villosus (Euphractinae, Xenarthra) was made and compared to those of the extant genus Dasypus (Dasypodinae, Xenarthra), and the extinct genus ?Eutatus. Three distinct histological zones were recognized: outer and inner zones are thin, formed by regular compact bone, the middle zone is thicker, with large cavities that contain mainly adipose tissue, hair follicles, and sweat and sebaceous glands. The internal structure of ?Eutatus (also a member of Euphractinae) osteoderms is close to that of C. villosus, consistent with the notion that these taxa are phylogenetically closely related. In contrast, Dasypus shows marked differences. Dasypus shows hair follicles associated with both gland types (sweat and sebaceous) and connected to foramina on the external surface. Although not observed in adult C. villosus, it has been documented during embryonic development, only to atrophy later in ontogeny. Furthermore, the presence of red bone marrow is rare in C. villosus, but widespread in Dasypus novemcinctus osteoderms. These results suggest an early split of both subfamilies and support the hypothesis that the Euphractinae are more derived than the Dasypodinae.     

RESTUDY OF SHANTUNGOSUCHUS BRACHYCEPHALUS YOUNG, 1982

ThreespecieshavebeenreferredtoShantungosuchustodate.ThetypespeciesS.chuhsienensis(Young,1961)isrepresentedbyanarticulatedskeletonpreservedasanimpressionofitsventralsurface.S.hangjinensiswasrecentlydescribedbyWuetal.(1994)onthebasisofanincompleteskull(withthemandible)andthepartofthepostcranialskeleton.ThethirdspeciesisS.brachycephalus,whichwillberestudiedinthepresentpaper'sbrachycephaluswaserectedbyYoungforaspecimen,consistingofpartialskullandsomepostcranialelements(V4020).Itwaspublishedinon…     

Osteoderm microstructure indicates the presence of a crocodylian‐like trunk bracing system in a group of armoured basal tetrapods

Buchwitz, M., Witzmann, F., Voigt, S. and Golubev, V. 2012. Osteoderm microstructure indicates the presence of a crocodylian‐like trunk bracing system in a group of armoured basal tetrapods. —Acta Zoologica (Stockholm) 93 : 260–280. The microstructure of dorsal osteoderms referred to the chroniosuchid taxa Chroniosuchus, Chroniosaurus, Madygenerpeton and cf. Uralerpeton is compared to existing data on the bystrowianid chroniosuchian Bystrowiella and further tetrapods. Chroniosuchid osteoderms are marked by thin internal and relatively thick external cortices that consist of lowly vascularised parallel‐fibred bone. They are structured by growth marks and, in case of Madygenerpeton, by lines of arrested growth. The cancellous middle region is marked by a high degree of remodelling and a primary bone matrix of parallel‐fibred bone that may include domains of interwoven structural fibres. Whereas the convergence of Bystrowiella and chroniosuchid osteoderms is not confirmed by our observations, the internal cortex of the latter displays a significant peculiarity: It contains distinct bundles of shallowly dipping Sharpey’s fibres with a cranio‐ or caudoventral orientation. We interpret this feature as indicative for the attachment of epaxial muscles which spanned several vertebral segments between the medioventral surface of the osteoderms and the transversal processes of the thoracic vertebrae. This finding endorses the hypothesis that the chroniosuchid osteoderm series was part of a crocodylian‐like trunk bracing system that supported terrestrial locomotion. According to the measured range of osteoderm bone compactness, some chroniosuchian species may have had a more aquatic lifestyle than others.     

A comparison of the structure,composition and mechanical properties of anosteocytic vertebrae of medaka (O. latipes) and osteocytic vertebrae of zebrafish (D. rerio)

Medaka (O. latipes) and zebrafish (D. rerio) are two teleost fish increasingly used as models to study human skeletal diseases. Although they are similar in size, swimming pattern and many other characteristics, these two species are very distant from an evolutionary point of view (by at least 100 million years). A prominent difference between the skeletons of medaka and zebrafish is the total absence of osteocytes in medaka (anosteocytic), while zebrafish bone contains numerous osteocytes (osteocytic). This fundamental difference suggests the possibility that the bony elements of their skeleton may be different in a variety of other aspects, structural, mechanical or both, particularly in heavily loaded bones like the vertebrae. Here we report on the results of a comparative study that aimed to determine the similarities and differences in medaka and zebrafish vertebrae in terms of their macro- to nanostructure, composition and mechanical properties. Our results reveal many similarities between medaka and zebrafish vertebrae, making the lack or presence of osteocytes the only major difference between the bones of these two species.     

Hyperossification in miniaturized toadlets of the genus Brachycephalus (Amphibia: Anura: Brachycephalidae): Microscopic structure and macroscopic patterns of variation

Species of the genus Brachycephalus, have a snout‐vent length of less than 18 mm and are believed to have evolved through miniaturization. Brachycephalus ephippium, is particularly interesting; because its entire skull is hyperossified, and the presacral vertebrae and transverse processes are covered by a dorsal shield. We demonstrate in this paper that, at the macroscopic level, a completely hyperossified skull and dorsal shield occur only in B. ephippium, but not in B. ferruginus, B. izechsohni, B. pernix, B. pombali, B. brunneus, B. didactylus, and B. hermogenesi. An intermediate condition, in which the skull is hyperossified but a dorsal shield is absent, occurs in B. vertebralis, B. nodoterga, B. pitanga, and B. alipioi. The microscopic structure of hyperossification was examined in skulls of B. ephippium and B. pitanga, revealing a complex organization involving the presence of Sharpey fibers, which in humans are characteristic of periodontal connections. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms

The dermal skeleton (=exoskeleton) has long been recognized as a major determinant of vertebrate morphology. Until recently however, details of tissue development and diversity, particularly among amniotes, have been lacking. This investigation explores the development of the dermatocranium, gastralia, and osteoderms in the American alligator, Alligator mississippiensis. With the exception of osteoderms, elements of the dermal skeleton develop early during skeletogenesis, with most initiating ossification prior to mineralization of the endoskeleton. Characteristically, circumoral elements of the dermatocranium, including the pterygoid and dentigerous elements, are among the first to form. Unlike other axially arranged bones, gastralia develop in a caudolateral to craniomedial sequence. Osteoderms demonstrate a delayed onset of development compared with the rest of the skeleton, not appearing until well after hatching. Osteoderm development is asynchronous across the body, first forming dorsally adjacent to the cervical vertebrae; the majority of successive elements appear in caudal and lateral positions. Exclusive of osteoderms, the dermal skeleton initiates osteogenesis via intramembranous ossification. Following the establishment of skeletal condensations, some preossified spicules become engorged with many closely packed clusters of chondrocyte-like cells in a bone-like matrix. This combination of features is characteristic of chondroid bone, a tissue otherwise unreported among nonavian reptiles. No secondary cartilage was identified in any of the specimens examined. With continued growth, dermal bone (including chondroid bone) and osteoid are resorbed by multinucleated osteoclasts. However, there is no evidence that these cells contribute to the rugose pattern of bony ornamentation characteristic of the crocodylian dermatocranium. Instead, ornamentation develops as a result of localized concentrations of bone deposited by osteoblasts. Osteoderms develop in the absence of osteoblastic cells, osteoid, and periosteum; bone develops via the direct transformation of the preexisting dense irregular connective tissue. This mode of bone formation is identified as metaplasia. Importantly, it is also demonstrated that osteoderms are not histologically uniform but involve a range of tissues including calcified and uncalcified dense irregular connective tissue. Between taxa, not all osteoderms develop by homologous processes. However, it is concluded that all osteoderms may share a deep homology, connected by the structural and skeletogenic properties of the dermis.     

Unique digestive system,trophic specialization,and diversification in the deep‐sea gastropod genus Scaphander

Dietary specialization is known to be important for the evolution of Cephalaspidea gastropods, but still little is known about the overall trophic interactions of the group and the putative role of trophic ecology on diversification. The genus Scaphander is a group of predominantly deep‐sea, infaunal cephalaspids with about 40% of its species (eight) occurring on the Atlantic Ocean. They are carnivorous and have a unique digestive system with a large, strongly muscularized gizzard containing three sizable and heavily calcified plates. This work aims to describe the diet of Scaphander, to evaluate if there is a functional relation between the anatomy of the digestive tract and exploitation of novel food resources, and to assess if dietary specialization may have played a role in the diversification of the Atlantic species of Scaphander. Gut contents were studied from 31 specimens representing seven of the Atlantic species using scanning electron microscopy and light microscopy. The chemical composition of the gizzard plates was analysed by X‐ray microanalysis and X‐ray powder diffraction. Foraminiferans, including agglutinating forms, were shown to be the most important food item for Scaphander; bivalves, gastropods, scaphopods, and polychaetes with calcareous tubes were also found to form part of the diet. The gizzard plates were shown to consist of a phosphate‐rich amorphous component and a crystalline component identified as fluorite (hardness 4; Moh's scale). It is suggested that the ability of Scaphander gastropods to prey upon organisms with hard tests, particularly agglutinating foraminiferans, is not only due to the hardness of the gizzard plates but to the cumulative effect of shape and hardness of the gizzard plates and relative size of the gizzard and associated musculature. No interspecific differences were found in the diet and morphology of the digestive tract, indicating that dietary specialization probably has not played a significant role in the diversification of Atlantic species of Scaphander. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 512–525.     

Phylogeography and phylogenetic relationships of Malagasy tree and ground boas

Three species of boid snakes are recognized in Madagascar, namely the genus Sanzinia (one species and two subspecies) and the genus Acrantophis (two species). In the present study, we studied the patterns of genetic variation of these species across Madagascar using a fragment of the mitochondrial 16S rRNA gene in 77 specimens. To support the phylogenetic relationships of the lineages identified, three further gene fragments (cytochrome b, 12S rRNA and c‐mos) were analyzed in a reduced but representative set of samples. The results obtained corroborate that the genus Sanzinia includes two highly divergent mitochondrial lineages that evolved independently from each other on the east versus the west side of Madagascar. Each of these lineages presents a further subdivision that separates northern from southern groups. The nuclear marker showed no variation among the Malagasy boas, indicating either very low substitution rates in this gene or relatively recent speciation events coupled with high mitochondrial substitution rates. Because the broad geographic sampling detected no admixture among haplotypic lineages within Sanzinia, it is hypothesized that these may represent distinct species. Deviant haplotypes of snakes morphologically similar to Acrantophis dumerili indicate that this taxon may be a complex of two species as well. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 640–652.