Skeletal development of the Mexican spadefoot, Spea multiplicata (Anura: Pelobatidae)

The larval chondrocranium of Spea multiplicata is described, as is the development and adult morphology of the skeleton. There are major modifications to the larval chondrocranium throughout development, including the presence of embryonic trabeculae in young tadpoles and significant reorganization of cartilaginous structures at metamorphosis. The first bone to ossify is the parasphenoid (Stage 35), followed by the presacral neural arches, ilium, and femur (Stage 36). By Stage 39, most of the postcranial elements have begun to ossify. Metamorphic climax is accomplished over three Gosner stages (39-41) and involves major modifications to the chondrocranium, as well as the appearance of three cranial elements (septomaxilla, nasal, and premaxilla). After metamorphosis, the exoccipital, vomer, dentary, angulosplenial, squamosal, pterygoid, sphenethmoid, ischium, and hyoid begin to ossify. The stapes, mentomeckelian, operculum, carpals, and tarsals do not appear until juvenile and adult stages. The development of the hyoid and cartilaginous condensations of the carpals and tarsals are described. In addition, phenotypic plasticity within the genus and the absence of a palatine (= neopalatine) bone are discussed.     

Comparative skeletogenesis of the Oriental Tree Frog Hyla orientalis (Anura: Hylidae)

The ontogeny of skeletal development of the Oriental Tree Frog, Hyla orientalis (Bedriaga, 1890), is followed from tadpole to froglet and compared with four other hylid species i.e., Hypsiboas lanciformis, Hypsiboas pulchellus, Phyllomedusa vaillanti and Pseudis platensis. Our analysis and comparison is based on cleared and double-stained specimens. The parasphenoid is the first skeletal element that ossified in Hyla orientalis is followed by the exoocipital, prootic, axial and appendicular skeletal elements, frontoparietal, nasal, upper jaw, squamosal, pterygoid, lower jaw, vomer and quadratojugal. Ossification initiated at early Stage 33 in Hyla orientalis whereas in other hylids it begins after Stage 37. Major transformations of the larval jaw were visible after Stage 42. Cranial ossifications were completed after appendicular and axial ossifications of Hyla orientalis. All skeletal elements ossified before the end of the metamorphosis, a unique feature of Hyla orientalis in comparison to the other hylids studied here.     

Osteological postcranial traits in hylid anurans indicate a morphological continuum between swimming and jumping locomotor modes

Anurans exhibit a particularly wide range of locomotor modes that result in wide variations in their skeletal structure. This article investigates the possible correlation between morphological aspects of the hylid postcranial skeleton and their different locomotor modes and habitat use. To do so, we analyzed 18 morphometric postcranial variables in 19 different anuran species representative of a variety of locomotor modes (jumper, hopper, walker, and swimmer) and habitat uses (arboreal, bush, terrestrial, and aquatic). Our results show that the evolution of the postcranial hylid skeleton cannot be explained by one single model, as for example, the girdles suggest modular evolution while the vertebral column suggests other evolutionary modules. In conjunction with data from several other studies, we were able to show a relationship between hylid morphology and habitat use; offering further evidence that the jumper/swimmer and walker/hopper locomotor modes exhibit quite similar morphological architecture. This allowed us to infer that new locomotor modalities are, in fact, generated along a morphological continuum. J. Morphol. 278:403–417, 2017. © 2017 Wiley Periodicals, Inc.     

Comparative ossification sequence and skeletal development of the postcranium of palaeognathous birds (Aves: Palaeognathae)

Palaeognaths constitute one of the most basal lineages of extant birds, and are also one of the most morphologically diverse avian orders. Their skeletal development is relatively unknown, in spite of their important phylogenetic position. Here, we compare the development of the postcranial skeleton in the emu (Dromaius novaehollandiae), ostrich (Struthio camelus), greater rhea (Rhea americana) and elegant crested‐tinamou (Eudromia elegans), focusing on ossification. All of these taxa are characterized by element loss in the appendicular skeleton, but there are several developmental mechanisms through which this loss occurs, including failure to chondrify, failure to ossify and fusion of cartilages prior to ossification. Further evidence is presented here to support a reduction in size of skeletal elements resulting in a delay in the timing of ossification. This study provides an important first look at the timing and sequence of postcranial ossification in palaeognathous birds, and discusses the influence of changes in the pattern of skeletal development on morphological evolution.     

Skeletal development in the Chinese soft‐shelled turtle Pelodiscus sinensis (Testudines: Trionychidae)

We investigated the development of the whole skeleton of the soft‐shelled turtle Pelodiscus sinensis, with particular emphasis on the pattern and sequence of ossification. Ossification starts at late Tokita‐Kuratani stage (TK) 18 with the maxilla, followed by the dentary and prefrontal. The quadrate is the first endoskeletal ossification and appears at TK stage 22. All adult skull elements have started ossification by TK stage 25. Plastral bones are the first postcranial bones to ossify, whereas the nuchal is the first carapacial bone to ossify, appearing as two unstained anlagen. Extensive examination of ossification sequences among autopodial elements reveals much intraspecific variation. Patterns of ossification of cranial dermal elements are more variable than those of endochondral elements, and dermal elements ossify before endochondral ones. Differences in ossification sequences with Apalone spinifera include: in Pelodiscus sinensis the jugal develops relatively early and before the frontal, whereas it appears later in A. spinifera; the frontal appears shortly before the parietal in A. spinifera whereas in P. sinensis the parietal appears several stages before the frontal. Chelydrids exhibit an early development of the postorbital bone and the palatal elements as compared to trionychids. Integration of the onset of ossification data into an analysis of the sequence of skeletal ossification in cryptodirans using the event‐pairing and Parsimov methods reveals heterochronies, some of which reflect the hypothesized phylogeny considered taxa. A functional interpretation of heterochronies is speculative. In the chondrocranium there is no contact between the nasal capsules and planum supraseptale via the sphenethmoid commissurae. The pattern of chondrification of forelimb and hind limb elements is consistent with a primary axis and digital arch. There is no evidence of anterior condensations distal to the radius and tibia. A pattern of quasi‐ simultaneity is seen in the chondrogenesis of the forelimb and the hind limb. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

A large‐scale survey of heterochrony in anuran cranial ossification patterns

Most anurans have a biphasic life cycle, which includes metamorphosis from a tadpole stage to an adult frog. This process involves extensive transformations of the cranial skeleton, which have been of long‐standing interest with respect to anuran skeletal evolution and taxonomy. In this study, large‐scale patterns of anuran skeletal ossification are assessed by collecting the most comprehensive data set on anuran cranial ossification to date from the literature, including data for 45 anuran and one caudate outgroup species. Ossification sequences were translated into event‐pair matrices for explorative phylogenetic analysis and phylogenetically informed parsimony search for heterochrony using the Parsimov algorithm. Rank variability of single bones across species was also analysed. Little phylogenetic signal was retrieved from a parsimony‐based phylogenetic analysis of event‐pairs, and only a few species that are generally agreed to be closely related are placed close to each other (e.g. some Pipidae and Costata). Parsimov analysis revealed some clade‐specific heterochrony in anuran clades of varying inclusiveness. Our results show that relating heterochronic changes in anuran cranial ontogeny to parameters such as direct development or miniaturization is problematic because of the high evolvability of cranial ossification sequences. Rank variation analysis suggests that anuran cranial bones are highly variable in their sequence positioning, possibly because tadpole and adult cranial morphology do not co‐evolve. Elements which are lost in some species ossify at the end of the sequence, providing evidence for the notion that failure of anuran cranial elements to ossify is due to processes of paedomorphosis.     

Early development of the postcranial skeleton of the pikeperch Sander lucioperca (Teleostei: Percidae) relating to developmental stages and growth

The early development of the postcranial skeleton (pectoral girdle, pelvic girdle, vertebral column and fins) in pikeperch (Sander lucioperca (L.)) was studied from hatching to days 47 and 43 post fertilization (dpf) at two different rearing temperatures, 15.5 and 18.0°C. Four embryonic and six larval stages were described, ranging from 3.4 ± 0.3 mm to 21.8 ± 2.1 mm in total length. The crucial point in larval development is swimbladder inflation, which enables larvae to swim energy efficiently. Until this time point, only the most essential skeletal elements to enable swimming movements have developed. As the larvae become neutrally buoyant, they grow and differentiate postcranial elements rapidly. Concurrently, swimming performance and foraging success seems to improve. A specific size is correlated with a distinct developmental stage defined by a set of traits that includes the skeletal elements. The developmental sequence of skeletal structures is temperature independent, although growth is slower and the individual developmental stages are reached later at 15.5°C than at 18.0°C. J. Morphol. 2012. © 2012 Wiley Periodicals, Inc.     

Muscle development in the abdominal region of Larval Hylidae (Amphibia: Anura)

Larval muscle development in the abdominal region of five species of hylid frogs (Scinax nasicum, S. fuscovarium, Hyla andina, Phyllomedusa boliviana, Gastrotheca gracilis) was studied using differential staining techniques. These five species represent three major hylid subfamilies. The development of the main abdominal muscles, the rectus abdominis, the two lateral muscles (obliquus externus and transversus), and the lateral pectoralis abdominalis is described. The number of myotomes of the rectus abdominis varies between five and six, and the abdominal muscles associated with the rectus abdominis (obliquus externus, pectoralis abdominalis, and rectus cervicis) vary interspecifically in time of appearance and configuration. The presence of gaps in the configuration of the rectus abdominis has been related to the lotic habits of the larvae. However, our observations indicate the presence of such gaps in larvae that inhabit lentic environments as well. These results suggest that the presence of these gaps is unrelated to larval habitat. There are relatively small differences in muscle morphology among these closely related species, which apparently cannot be explained by morphological adaptations related to their ecology. In the species studied, the number of elements that form the abdominal musculature in larvae is equal to that observed in adults. Likewise, the general morphology of the muscles is ontogenetically conserved. This suggests that both the axial skeleton and musculature are more ontogenetically conserved in relation to the substantial changes that are observed in the skull and head muscles of developing anurans. J. Morphol. 241:275–282, 1999. © 1999 Wiley‐Liss, Inc.     

Sequence of chondrocranial development in the oriental fire bellied toad Bombina orientalis

The vertebrate head as a major novelty is directly linked to the evolutionary success of the vertebrates. Sequential information on the embryonic pattern of cartilaginous head development are scarce, but important for the understanding of its evolution. In this study, we use the oriental fire bellied toad, Bombina orientalis, a basal anuran to investigate the sequence and timing of larval cartilaginous development of the head skeleton from the appearance of mesenchymal Anlagen in post-neurulation stages until the premetamorphic larvae. We use different methodological approaches like classic histology, clearing and staining, and antibody staining to examine the larval skeletal morphology. Our results show that in contrast to other vertebrates, the ceratohyals are the first centers of chondrification. They are followed by the palatoquadrate and the basihyal. The latter later fuses to the ceratohyal and the branchial basket. Anterior elements like Meckel's cartilage and the rostralia are delayed in development and alter the ancestral anterior posterior pattern observed in other vertebrates. The ceratobranchials I–IV, components of the branchial basket, follow this strict anterior–posterior pattern of chondrification as reported in other amphibians. Chondrification of different skeletal elements follows a distinct pattern and the larval skeleton is nearly fully developed at Gosner Stage 28. We provide baseline data on the pattern and timing of early cartilage development in a basal anuran species, which may serve as guidance for further experimental studies in this species as well as an important basis for the understanding of the evolutionary changes in head development among amphibians and vertebrates.     

Larval and metamorphic skeletal development in the fast-developing frog Pyxicephalus adspersus (Anura, Ranidae)

Pyxicephalus adspersus , is exceptional among living frogs. Embryonic development, larval phase, and metamorphosis can be completed in 17 days at a temperature of 29°C. The metamorphosis only takes 5 days. The present study shows that, despite the unusually short larval phase in P. adspersus, the state of skeletal differentiation reached at the end of metamorphosis is similar to that of other frog species. There is no shift of cranial bone formation postmetamorphosis as could have been expected and is known from other species. The majority of compared species are particularly similar in the sequence of bone formation in the postcranial skeleton. However, there are clear differences among species in the timing of these events relative to the larval growth trajectory, absolute time, and certain developmental markers, such as external limb differentiation. For example, skeletogenesis and externally visible limb differentiation are only loosely integrated. Interspecific comparisons show that, in P. adspersus, the early onset of skeletal ossification is an unusual feature among frogs. Freshly metamorphosed froglets of P. adspersus are already distinct from comparable stages of other species in having strong jaws, fang-like teeth, and a squamosal-maxilla contact. The latter stabilizes the maxillary arcade and the suspensorium and might relate to the ability to catch and swallow very large vigorous prey, such as siblings, shortly after metamorphosis. The presence of a complete set of dermatocranial elements and postmetamorphic ossification of only the sphenethmoid and operculum are considered plesiomorphic features, whereas the much less completely ossified skulls of metamorphosed froglets, particularly in Bufo and Hamptophryne, are likely apo- morphic developmental traits within the Anura. Accepted: 11 January 1999     

Hyobranchial and postcranial ontogeny of the temnospondylOnchiodon labyrinthicus (Geinitz, 1861) from Niederhäslich (Dohlen Basin, Autunian, Saxony)

Hyobranchium, postcranial skeleton, and developmental events during ontogeny of the temnospondylOnchiodon labyrinthicus from the Dohlen Basin (Autunian, Saxony) are described. At a skull length of approximately 20 mm, the scapulocoracoid appeared, but ossified very slowly. The ischium ossified distinctly later than the stout ilium and later than the scapulocoracoid. The stapes can be determined in specimens beyond 26 mm skull length, and the exoccipitals started to ossify probably at 40 mm, followed by the quadrate. Vertebral centra ossified in early juveniles at approximately 50 mm skull length. The larval hyobranchium with ossified basibranchial and ceratobranchials indicates strong suction feeding. The bony ceratobranchials were resorbed after the larval period. The poorly ossified postcranium suggests that juveniles lived semiterrestrially.     

Postembryonic ontogeny of the spadefoot toad,Scaphiopus intermontanus (Anura: Pelobatidae): Skeletal morphology

Postembryonic skeletal ontogeny of the pelobatid frog Scaphiopus intermontanus is described based on a developmental series of cleared-and-stained, whole-mount specimens. The focus is on laboratory-reared individuals fed a herbivorous diet as larvae. Although there is variation in the timing of ossification of individual skeletal elements relative to developmental stages based on external morphological criteria, the sequence of skeletal development generally is conservative. Compared with its close relative, S. bombifrons, ossifications that occur during prometamorphosis tend to be slightly delayed in S. intermontanus; however, cranial bones that ossify during late metamorphic climax in S. intermontanus are delayed until postmetamorphosis in S. bombifrons. The differences in timing between the two species are consistent, however, with differences observed between two developmental series of S. intermontanus raised at two different temperatures. Noteworthy features of skeletal development in S. intermontanus include: 1) presence of palatine ossifications that form from independent centers of ossification and soon fuse with the postnarial portion of the vomers to form the compound vomeropalatine bones; 2) compound sphenethmoid that may arise from four or more endochondral centers of ossification and one dorsal, dermal center of ossification; and 3) presence of transverse processes and vestigal prezygapophyses on the first postsacral vertebra. The morphology of the larval orbitohyoideus and interhyoideus muscles is compared. The record of skeletal ontogeny and muscle morphology presented herein for the herbivorous larval morph can serve as a baseline for comparisons with the ontogeny of the carnivorous larval morph of Scaphiopus. J. Morphol. 238:179–244, 1998. © 1998 Wiley-Liss, Inc.