ABSTRACT. Mesosaurs are basal amniotes that lived in an extended epicontinental sea resulting from Devonian and Carboniferous glaciations reported in Southern Gondwana. Previously considered to be marine animals, this interpretation is not supported by their skeletal anatomy, and was updated to a more semiaquatic style, prompting increased interest for mesosaur studies. Recently, transverse fractures and weak ossified areas at the subcentral surface of some caudal vertebrae have been interpreted as fracture planes related to a putative capability of autotomy in mesosaurs. We reassess the data used in support of caudal autotomy and identify the constraining morphological features of the involved vertebrae that contradict the development of such ability in mesosaurs. Moreover, we analyze the physiological and behavioral negative consequences that the loss of part of the tail would represent for aquatic and semiaquatic animals. The fact that no extant taxa living in these environments developed caudal autotomy supports our interpretations. We present an alternative hypothesis that suggests the presence of multipartite caudal centra represented by pleurocentrum and intercentrum arranged in the way expected for a reverse embolomerous pattern, previously undescribed for early stegocephalians or amniotes. However, a rapid revision of specialized literature suggests that the pattern could have been present in other basal amniotes and the possibility deserves additional studies, mainly in juvenile individuals. Our reinterpretation of the structure of mesosaur caudal vertebrae supports the proposed morphological plasticity observed in many clades of basal stegocephalians and amniotes and would match the recently suggested phylogenetic affinities of mesosaurs with respect to taxa that are close to, or part of the amniote stem under some phylogenies.
KEYWORDS: Mesosauridae, vertebral patterns, caudal vertebrae, autotomy, Gondwana.
RÉSUMÉ. Les mésosaures sont des amniotes basaux qui vivaient dans une mer épicontinentale étendue résultant des glaciations du Dévonien et du Carbonifère signalées dans le sud du Gondwana. Pendant longtemps, ils ont été interprétés comme des animaux marins, mais cette interprétation, non étayée par leur anatomie squelettique, a été abandonnée par certains auteurs qui proposent un style davantage semi-aquatique, ce qui a généré une recrudescence d’intérêt notable pour les études sur les mésosaures. Récemment, des fractures vertébrales dans la zone sous-centrale de certaines vertèbres caudales ont été interprétées comme des plans de fracture liés à une capacité putative d’autotomie chez les mésosaures. Nous réévaluons l’hypothèse proposée et retrouvons plusieurs facteurs contraignant la morphologie des vertèbres impliquées dans le processus autotomique, en plus des conséquences négatives physiologiques et comportementales que la perte d’une partie de la queue représenterait pour des animaux aquatiques et semi-aquatiques. Le fait qu’aucun taxon vivant dans ces environnements n’ait développé d’autotomie caudale soutient nos interprétations. Par conséquent, nous présentons une hypothèse alternative qui suggère la présence de centres caudaux multipartites représentés par un pleurocentrum et un intercentrum disposés de la manière attendue pour un motif embolomère inverse, précédemment inédit chez les premiers stégocéphales ou amniotes. Notre réinterprétation des vertèbres caudales du mésosaure fournit de nouvelles preuves de la plasticité morphologique proposée observée dans de nombreux clades de stégocéphales basaux et correspond aux affinités phylogénétiques récemment suggérées entre les mésosaures et des taxons qui sont proches de la souche des amniotes ou qui en font partie dans certaines phylogénies.
MOTS CLÉS: Mesosauridae, modèles vertébraux, vertèbres caudales, autotomie, Gondwana.
Since its discovery about two centuries ago, Gervais (1865) for the first time, Cope (1886) who considered mesosaurs as possessing a unique skeletal morphology consisting of a mixture of anatomical features characteristic of both aquatic and terrestrial reptiles and who placed them tentatively in the “Batrachia”. He based this relationship on the distinctive small size of the centrum of dorsal vertebrae relative to the swollen neural arch, a feature more commonly observed in seymouriamorphs and diadectomorphs rather than in reptiles and other basal amniotes (Carroll & Baird 1972; Clark & Carroll 1973; Carroll 1982). However, the vertebral morphology and other osteological characters used in early paleontological studies that sought to establish the affinities of mesosaurids to diapsids or synapsids, were ignored in recent phylogenetic studies that instead linked them to the stem sauropsids or to the parareptiles (e.g. Gauthier et al. 1988a, b, c; Laurin & Reisz 1995; Modesto 1996, 1999; Laurin & Piñeiro 2017, 2018; MacDougall et al. 2018, among others). Their specialized (although not yet completely known) cranial morphology, with a long snout bearing slender and thin teeth, posteriorly placed nares, and pachyosteosclerotic ribs and vertebrae, were considered as adaptations for a marine environment (Araújo 1977; Oelofsen 1981; Oelofsen & Araújo 1983; Modesto 1996, 1999, 2010), which implied that mesosaurids were the first amniotes to return to water. However, these hypotheses were not universally accepted, and some workers proposed that mesosaurids were semiaquatic animals that may have retained this lifestyle from their ancestors (see Romer 1947; Piñeiro et al. 2016, 2021; Núñez Demarco et al. 2022).
To confidently infer the lifestyle of an ancient extinct species, detailed anatomical studies of the skeleton in individuals representing different ontogenetic stages are necessary. These studies can be complemented with paleoenvironmental interpretations of the geological setting of their fossilization. The reliability of these inferences also depends on the size of the studied sample and the quality of preservation. Other associated fossils from the surrounding matrix and from the entire stratigraphic sequence can help constrain paleoenvironmental conditions as well as the establishment of biostratigraphic correlations. These data sources have long been available for studying the lifestyle of mesosaurs and have been used to support the aforementioned hypotheses, although many of them remain controversial.
A recent study by MacDougall et al. (2020) reassessed previously suggested hypotheses that mesosaurids retained caudal autotomy as a defensive response against predators, a controversial possibility that is revisted in the present contribution. As we argue below, this mechanism is not as plausible in aquatic, tail-propelled animals (see Villamil et al. 2015) as in terrestrial ones that rely on limbs for locomotion.
Caudal autotomy is the voluntary shedding of the tail through specialized vertebrae that develop fracture planes and/or areas of bone weakness, and a series of muscles and blood vessels that automatically constrict to limit the loss of soft tissues. Among reptiles, this phenomenon is unknown in crocodiles and turtles but widespread within squamates where it serves as a defensive behavior that favors escape from predators (i.e., Gordeevaet al. 2020). The splitting can be either intravertebral or intervertebral; the first pattern is the most common in squamates, except in agamids, which have developed intervertebral caudal autotomy (Ananjeva et al. 2021).
Romer (1956) initially suggested that some lines of fracture and poorly ossified areas observed in the centrum of some mesosaurid caudal vertebrae implied a potential capability for caudal intravertebral autotomy. This hypothesis was followed by MacDougall et al. (2020) as a possible condition characterizing mesosaurids based on the fact that other Paleozoic amniotes, such as the captorhinid LeBlanc et al. 2018) Heaton 1979; Dilkes & Reisz 1986), show similar lines of fractures in the centrum of some vertebrae, interpreted as evidence for autotomy (Romer 1956; Heaton & Reisz 1980; LeBlanc et al. 2018). For captorhinids, which are often suggested to have been terrestrial, autotomy is a plausible explanation for the fracture planes observed in isolated caudal vertebrae. However, for aquatic or semiaquatic taxa for which the tail plays an essential role in swimming, tail loss can be disadvantageous (Fleming et al. 2013). The absence of fracture planes in all the extant aquatic taxa, including marine mammals and snakes, and also their absence in the caudal vertebrae of the marine iguana (Arrivillaga & Brown 2020). The only exception may be the water anole (Talavera et al. 2021).
The mesosaurid tail is almost completely preserved in many specimens, with putative fracture planes observed in nearly all of the caudal vertebrae. Thus, if autotomy did occur in mesosaurids, more than half of the tail could have been lost. This would represent a significant physiologic cost as the tail served as the main swimming organ for mesosaurids (Modesto 1996; Villamil et al. 2015). MacDougall et al. (2020) acknowledged this issue and suggested that the role of the tail in mesosaurid locomotion had been previously exaggerated, and that propulsion in the water could have been achieved by their paddle-like limbs. In addition, MacDougall et al. (2020) concluded that autotomy cannot be definitively proven in mesosaurids, and the presence of fracture planes could be a relictual condition.
The aim of this contribution is to review the morphological, physiological and behavioral implications of tail autotomy in extinct aquatic forms such as
To assess the biological significance of the observed fracture planes in some mesosaurid caudal vertebrae, a comparative morphological analysis was conducted across a large dataset comprising over 700 specimens. This dataset includes both isolated elements representing various positions in the tail and articulated tails containing the complete caudal series.
A parasagittal histological slide of the caudal vertebrae from specimen MCN-PV-20.007-P was prepared. Due to the exceptionally thin nature of the fossil material, which matches the thickness of the diamond saw employed, only one section was produced. Subsequently, images were captured using a magnifying glass and microscope in both normal and polarized light.
Piñeiro et al. (2021) recently proposed that Verrière & Fröbisch (2022) and that is accepted here. Therefore, throughout this study, the terms “mesosaurid” or ”mesosaur” are used to refer exclusively to this taxon.
The analyzed
Table 1).
This diverse sample encompasses caudal vertebrae and tails from both adult and juvenile individuals, preserved at different ontogenetic stages.
Specimens of different sizes and attributable to different stages of development were analyzed under a NIKON HFX-DX stereoscopic microscope equipped with camera lucida and Infinity Analyze software for the analysis. This setup facilitated the capture of photographs and the creation of drawings to document the anatomical features of the studied vertebrae. In some instances, more time-intensive methods were utilized, involving the careful removal of surrounding sediment from 3D-preserved specimens. One of these 3D specimens was sectioned to produce a thin section along a longitudinal, parasagittal plane of mid-distal caudal vertebrae, allowing for the study of their microstructure and ossification processes. All specimens from Uruguayan (FC-DPV), and Brazilian (GP-2E, DNPM and MCN-PV) collections, as well as those from the SMF-R collection in Germany, were examined directly, whereas specimens from other collections were studied using photographs kindly provided by the respective curators (refer to the Acknowledgements section for further details).
To compare with both extant and extinct taxa for which autotomy has been suggested or observed, we provide a concise description of the anatomical characteristics and structural arrangement of the vertebral segments that can be identified in the mesosaurid tail.
The first seven to ten caudal vertebrae (observed intraspecific numerical variations may reflect sexual dimorphism; see Shine et al. 1999) constitute a specialized string characterized by the presence of ribs firmly attached to the short transverse processes, the lack of haemal arches (chevrons) and also the absence of “fracture/suture planes”. However, in mesosaurs the last vertebrae of the pygal segment can carry an haemal arch.
This configuration follows the previously documented trait of basal stegocephalians, in which all presacral vertebrae, as well as the first caudals, bear ribs (Romer 1947).
The ribs of the first five caudal vertebrae are long, stout and bent posteriorly, as is also observed for instance in captorhinids (Heaton & Reisz 1980; Berman & Reisz 1986), diadectids (Berman & Henrici 2003) and seymouriamophs (Berman et al. 1987). From the sixth to the ninth or tenth vertebrae, the ribs abruptly decrease in size with the last three either bent anteriorly or pointing laterally (Fig. 1). These anteriormost nine to ten caudal vertebrae may be considered as the “pygal-like” segment, which in extant squamates possessing intravertebral autotomy, is associated with the insertion of the caudofemoralis longus muscle, and thus autotomy cannot occur in vertebrae of this segment which is typically characterized by the absence of fracture planes (Ritzman et al. 2012).
Due to the presence of long and firmly fused ribs, a condition which is morphologically similar to that observed in the posterior dorsal vertebrae (Fig. 1), the ribs of the first ten caudal vertebrae of mesosaurs are often preserved parallel to the stratification, and thus, the vertebrae are mostly exposed in ventral or dorsal view, or in a frontal or antero/postero-lateral view on rare occasions. This makes it challenging to confirm the existence of potential “fracture planes” (from now on referred to as “fracture/suture planes”) within these anteriomost caudal vertebrae. However, some fortuitous isolated vertebrae recognized as part of the “pygal segment” because they bear short transverse processes carrying a rib, show that there are no central fractures in these vertebrae at the mid-centrum area. The presence of haemal arches in the last vertebrae of the “pygal-like” segment can also be confirmed by examining these isolated vertebrae (Fig. 2C, D).
The putative “fracture/suture planes” described by MacDougall et al. (2020) as evidence for autotomy in mesosaurs are present in vertebrae placed posterior to the last vertebra of the pygal segment. This vertebral segment will be known as the postpygal string and is characterized by vertebrae with diminutive transverse processes in the cranialmost segments (or none whatsoever, farther caudally), and are predominantly preserved in lateral view (Fig. 3).
The mesosaurid “postpygal” segment is formed by at least 56 vertebrae, some of which articulate with short ribs, if at all, but this condition is gradually lost in caudal direction. Most of them also bear haemal arches (chevrons); and only the last five or six vertebrae near to the tip of the tail are simplified and lack neural spines or haemal arches (Fig. 3B, C).
This distribution indicates that Romer 1947). Moreover, based on the described general pattern for mesosaur caudal vertebrae, it is possible to identify the relative position of isolated caudal vertebrae in the tail, and also determine if it is part of the “pygal-like” or the “post-pygal” series through the orientation of the transverse processes and ribs and by the presence/absence of haemal arches (Fig. 3).
The described morphological pattern of these regions in mesosaurs is notably different from that observed in most extant reptiles that can autotomize their tails, where haemal arches are almost always absent from the pygal segment. The anole Cuvier & Voight 1832) is an exception, because of the presence of chevrons in the posteriormost vertebrae of the pygal segment characterized by the lack of transverse processes and the absence of fracture planes, although in some other squamate species, the posterior vertebrae of the series may exhibit both features (Ritzman et al. 2012).
The number of vertebrae in the pygal series varies among taxa, but a pygal region is always retained in taxa that undergo tail autotomy, as these vertebrae do not develop fracture planes. Therefore, autotomy is produced through fractures present in just a few vertebrae in the postpygal series and the split occurs immediately posterior to the short transverse processes (Gilbert et al. 2013).
For extinct taxa, one of the few suggested cases of autotomy is found among the captorhinids. However, the presence of autotomy in this taxon is uncertain, both because function is never known with certainty in extinct taxa (it is inferred, rather than observed) but more specifically because in Heaton & Reisz 1980; Dilkes & Reisz 1986; LeBlanc et al. 2018).
This is not the expected pattern, but it can be possibly influenced by the fragmentary nature of the studied materials. This prevents morphological comparisons between transitional presacrals, sacrals and the first caudals, which hampers establishing the position of the vertebrae bearing the fracture planes, along the tail. Many conclusions in this regard, like the interpretation of a “pygal” segment composed of five vertebrae (LeBlanc et al. 2018), are based on articulated fragmentary remains which putatively included vertebrae from the eighth to the fourteenth out of an estimated total of 60 or more caudal vertebrae (Heaton & Reisz 1980).
The case of
Potential autotomy in microsaurian lepospondyls
Within lepospondyls, autotomy and tail regeneration have been reported in the microsaurian Carroll & Gaskill 1978; Milner 2008; Olori 2015; Fröbisch et al. 2015; Vos et al. 2018). Unlike recent salamanders that exhibit intervertebral splitting, in Vos et al. 2018. Olori (2015) shows photographs of th vertebra, seem to be a taphonomic feature common in vertebrae preserved in ventral view, where only the central part of the centrum is visible; the rest of the skeleton is covered by sediment. Therefore, the available images do not allow making definitive conclusions. The images provided by Milner (2008) are similarly inconclusive; that study investigated if the length of the tail in Milner 2008)Vos et al. (2018: fig. 6) are drawn as fused to the posterior region of the vertebral centrum, suggesting the presence of a reversed position of the intercentrum in the microsaur
Potential autotomy in marine early diapsids?
In the literature on marine mosasauroids, ichthyopterygians and sauropterygians, there is no mention of caudal vertebral structures (i.e., fracture planes) suggesting autotomy. The pygal segment appears to be formed by more than five vertebra in several of the revised sauropterygian taxa (e.g. Liu et al. 2021; Wolniewicz et al. 2023). The anteriormost transverse processes are relatively short and laterally directed in the pygals but they become wider and shorter in the postpygal series to gradually transform into short nubbins in the posteriormost vertebrae. The information on the nature of the haemal arches in ichthyopterygians and sauropterygians is scarce and ambiguous. Within mosasauroids, the pygal segment seems to be short in many species, and the hemal arches, when preserved in the postpygal string, seem to be articulated or fused to the posterior end of the vertebral centrum, as could be observed from many described taxa (see Williston 1898; Osborn 1899; Bell & Polcyn 2005; Kear 2006; Druckenmiller & Russell 2009; Konishi et al. 2012; Carpenter 2017; among others).
All the vertebrae within the “postpygal” series display a distinctive “fracture/suture” line or a weakly ossified area crossing the centra (Fig. 3), which has been interpreted as “fracture plane” for a potential development of autotomy in mesosaurs (Romer 1956; MacDougal et al. 2020). This structure resembles an incompletely closed suture that separates two regions of different sizes within the centrum, with the anteriormost part being slightly larger (Fig. 4). Conversely, some partial strings of the mesosaur tail have fortuitously split sagittally or parasagittally, creating taphonomic counterparts that reveal their internal anatomy. These counterparts expose structures such as what we prove by SEM analyses to be phosphatized remains of the notochordal tissues and the neural chord preserved within the neural canal (Figs 5; 6). The notochord is visible as a continuous structure along the dorsal vertebral series (Fig. 5E, F), although it appears as to have been interrupted at the middle of the caudal vertebrae, just where the “fracture/suture” line separates anterior and posterior central areas (Fig. 5A-D, G, H). This apparent interruption of the notochord may be related to the presence of the two primitive bones in the centrum formation, in vertebrae of the postpygal caudal series of mesosaurs. The thin section suggests that the notochord could remains continuous, although reduced to a thin thread at the level of the fracture plane area of each vertebra, which is probably a condition that was reestablished during ontogeny after the fusion between pleurocentrum and intercentrum was completed (Figs 5; 6).
Among extant amphibians and reptiles that have evolved tail autotomy, a series of morphological adaptations minimize trauma for the involved tissues (Gilbert et al. 2013).
The fracture planes and areas of bone weakness in some caudal vertebrae indicate the location where the split occurs if the animal perceives threat from a predator. The “fracture/suture” planes observed by MacDougal et al. (2020) in mesosaurs are similar to each other; they occur in most, if not all postpygal vertebrae, and do not affect the neural arch, contrary to what is typically observed in all extant vertebrates adapted to caudal autotomy to avoid predation, where the fracture plane penetrates the neural arches (Silva et al. 2021).
The mesosaurid tail is a very important organ of the body, since it is longer than the remaining body length and it presumably had an important propulsive function during swimming (Modesto 1996; Villamil et al. 2015; Núñez Demarco et al. 2018, but see MacDougall et al. 2020).
Another factor to take into account is the morphology and orientation of the zygapophyses, which also play a crucial role in conferring stability to the vertebral column during locomotion. In mesosaurs, the trunk vertebrae have laterally placed and almost horizontal prezygapophyses and posteroventrally inclined postzygapophyses at the base of swollen neural arches, which allow significant lateral movement while restricting rotation of the vertebral column (Olson 1976).
A notable morphological change occurs at the beginning of the “postpygal segment” of the tail, where the vertebrae become laterally constricted, and the articular facets of the pre-and post- zygapophyses are positioned close to the sagittal plane, with the prezygapophyses oriented dorsomedially and the postzygapophyses facing ventrolaterally. This arrangement likely permits only moderate lateral movements while limiting rotation (Olson 1976), a pattern that is typical of taxa performing anguilliform movements, which presumably occurred also in mesosaurs (Villamil et al. 2015). This morphology is favorable to an ambush-like predation strategy on fast prey like the juvenile pygocephalomorph crustaceans fossilized within the same beds as mesosaurids (Silva et al. 2017).
The loss of a long tail like that of mesosaurs would also alter the body mass distribution, affecting the balance and stability during locomotion (Gillis & Higham 2016). The incidence of these effects has been studied, for instance, in terrestrial and aquatic Marvin 2010).
Furthermore, the biomechanical changes resulting from the tail loss could lead to isolation of the animals due to the inability to maintain a normal locomotion. This would not only affects aspects such as feeding, self-protection and reproductive strategies (Shine et al. 1999), but might also influences their social behavior (Gillis & Higham 2016). In the case of mesosaurs, gregarious and/or parental care behaviors have been proposed, perhaps during the reproductive season and shortly after birth when adults and their offspring are found together (Piñeiro et al. 2012a, b).
MacDougall et al. (2020) tentatively suggested that “autotomy” may have been functional in juvenile individuals, and that it may have become more difficult in adults.
Indeed, the hypothesis of autotomy as a defense mechanism that is more developed in juveniles (Savvides et al. 2018) could have been advantageous in mesosaurs if cannibalism occurred, but this may have been lost during ontogeny as it occurs in recent reptiles, especially considering that no predator of adult mesosaurs is known to occur in their environment.
Intriguingly, “fracture/suture” lines seem to be less prominent in very young mesosaurs with respect to what is shown in adult or subadult individuals (see Fig. 7). This may be due to the fact that the skeletons of juveniles are poorly ossified and the preservation potential is low (Fig. 7A-C); this therefore would prevent the retention of some features with the same detailed precision as in more ossified specimens. Perhaps as previously suggested, fracture-suture planes may be acquired later in the ontogeny (Williston 1925), but most probably it is due to a taphonomic influence giving some fortuitous findings of isolated caudal vertebrae of juvenile mesosaurids from the Mangrullo Formation of Uruguay, where the fracture planes are perfectly observed, as shown in Figure 7D.
Mesosaurs have no known predators and this conclusion may not be related to collecting biases, as all the organisms cohabiting with mesosaurs in the Mangrullo Formation had the potential to be preserved, including insect and plant soft tissues as wings and leaves (Piñeiro 2006). Even though, parental care has been previously suggested for mesosaurs based on the high number of fossils that show a hatchling-early juvenile-adult association. These are particularly well-documented in areas that may have been breeding grounds, such as the Mangrullo Formation Konservat Lagerstätte, where a mesosaur egg containing a foetus has appeared (Piñeiro et al. 2012a).
One of the many taxonomically relevant characters of Palaeozoic tetrapods or stegocephalians, depending on the nomenclature used (Laurin 2020a, b), is the morphology of the vertebral column. Although three basic patterns were recognized for basal tetrapods, a great variability exists among and within the different taxa, which has been attributed to substantial morphological plasticity in early vertebrates (Herbst & Hutchinson 2018) (Fig. 8). Thus, in addition to the vertebral types: 1) rhachitomous (large intercentrum and smaller dorsal paired pleurocentra); 2) embolomerous (pleurocentrum and intercentrum present but the former is dominant); and 3) stereospondylous (one element is dominant, normally the intercentrum (Laurin 1998; Witzmann et al. 2013; Konietzko-Meier et al. 2014), other vertebral morphologies have been described, such as the gastrocentrous vertebrae (pleurocentrum is much larger than the intercentrum), monospondylous (a single holospondylous segment) and diplospondylous (a variation of the embolomerous type, with both disk-shaped intercentrum and pleurocentrum perforated by the notochord) (Gadow 1896; Romer 1947, 1956; Holmes 1989; Pierce et al. 2013; Danto et al. 2017).
Whereas the rhachitomous construction is usually considered the ancestral condition by most authors (e.g. Laurin 1998; Pierce et al. 2013), a few other studies have suggested the embolomerous type as the vertebral pattern from which all other were derived (Romer 1947). Moreover, although the rhachitomous type is characteristic of temnospondyls, and the embolomerous pattern is closer to either amniotes (under the “Temnosponyl Hypothesis”, abbreviated as TH below; Ruta & Coates 2007), or Tetrapoda (under the “Lepospondyl Hypothesis”, abbreviated LH below; Marjanović & Laurin 2019), both patterns can be found in some taxonomically diverse clades (Romer 1947). Furthermore, the monospondylous type is more frequently found in most lepospondyls, but some “microsaurs” have a small intercentrum and an embolomerous condition appears to be present in Archerontiscus (Carroll 1969). Additionally, Shishkin (1989) and Pierce et al. (2013) described a reverse rhachitomous pattern where the pleurocentrum occupies an anterior position in the centrum, whereas the intercentrum is posterior. According to Pierce et al. (2013), this last pattern is present in
Taking into account the counter-arguments against the hypothesis that suggests tail autotomy for mesosaurs when facing predation danger, and considering the unconservative traits of mesosaurs, as well as their aquatic (or semiaquatic) lifestyle in which the tail plays a crucial role in locomotion (Villamil et al. 2015), it is worth exploring alternative explanations for the presence of “fracture/suture” lines in their caudal vertebrae.
According to Gadow’s (1933) classical contribution about the “evolution of the vertebral column”, which continues to inspire research on vertebral evolution and structure (e.g. Wake & Wake 2000; Danto et al. 2017), the changes observed in vertebral construction within the evolutionary history of vertebrates are reflected in some ontogenetic stages, variability along the vertebral column, and may also reflect selective pressures. For instance, the tail may retain plesiomorphic characters that are eliminated in other parts of the skeleton, so that the tail appears to be “more primitive” than the trunk (Gadow 1933). The centrum and the entire vertebra develop from sclerotomes that divide themselves into two halves; the posterior half fuses to the anterior one of the immediately more caudal sclerotome, and this recombined unit develops into a vertebra (Turner & Sidor 2018). Therefore, the diplospondylous vertebrae are formed by parts of two sclerotomes in the way that their anterior part comes from the posterior half of a sclerotome and the posterior part is formed by the anterior half of the next (caudal) esclerotome. According to Gadow (1933), the anterior part of the vertebra reduces in size during tetrapod evolution, while the posterior becomes dominant. In mesosaurs, the centrum of most caudal vertebrae seems to be divided into two parts of different sizes, with the posterior being smaller. Therefore, the “fracture/suture line” seen in the mesosaur caudal centra that splits them into anterior and posterior halves might represent the suture between the large, anterior element (pleurocentrum) and the smaller posterior one (intercentrum).
This new hypothesis is consistent with the presence of pleurocentrum and intercentrum in the postpygal caudal series of mesosaurs, but their spatial arrangement may differ from a more conventional pattern of some other amniotes. If we accept the premise that the bone articulating with the haemal arch is the intercentrum, while the one supporting the neural arch is the pleurocentrum (Romer 1956), then the mesosaur centrum is composed of an intercentrum in a posterior position and a pleurocentrum in an anterior position (Fig. 8G), which until now appeared to be an unusual configuration for Amniota (Figs 4; 8), but see below.
It might be suggested that mesosaur caudal vertebrae exhibit a reverse rhachitomous condition as described by Shishkin (1989). However, in the rhachitomous condition, neither the intercentrum nor the pleurocentrum form closed ossified rings. Thus, the mesosaur caudal vertebrae are better interpreted as displaying an embolomerous condition reversed from the conventional pattern that occurs in long-tailed Upper Carboniferous or early Permian stegocephalians (Gadow 1933). Therefore, such a configuration is plausible, and our observations support this suggestion (Fig. 4). Indeed, it is unclear if embolomerous or rhachitomous vertebral organizations represent the ancestral condition in the phylogenetic hypotheses proposed for basal tetrapods (e.g. Romer 1947; Danto et al. 2017), although the rhachitomous morphotype has been most recently accepted (e.g. Laurin 1998). This pattern is otherwise unknown among amniotes, but it has been described for Devonian and Early Carboniferous stem-tetrapods and may be plesiomorphic for stegocephalians (Pierce et al. 2013).
The puzzling aspect of the two central elements in vertebrae of the “postpygal” segment of the mesosaur tail is seen as a putative reversal in the anatomical arrangement, with the intercentrum articulating most tightly with the pleuroentrum cranial to it. However, as noted in previous studies (i.e., Gadow 1933), intercentra are usually more closely integrated to the preceding vertebra than to the succeeding. This is reminiscent of the pattern found inHolmes 1984). The condition in
This interpretation reinforces the ancestral variability observed in vertebral centrum types (Fig. 8), which has been widely accepted as a characteristic of early stegocephalians and early reptiles (e.g. many “adult” procolophonids as well as protorothyridids possess sutured but unfused intercentra and pleurocentra, at least in the trunk vertebrae, as indicated in a personal comment of anonymous reviewer 1) (see also Gadow 1896; Carroll 1968, 1989; Shishkin 1989; Pierce et al. 2013; Danto et al. 2017; among many others).
To further test our hypothesis about the multipartite configuration of the mesosaur caudal centra, we produced a parasagittal thin section of three postpygal caudal vertebrae, possibly from the middle-posterior region of the column (Fig. 6A).
The vertebrae are very compact, based on comparisons with extant taxa (de Buffrénil et al. 2021), as expected for mesosaurs (Villamil et al. 2015). Most of the neural arch and bone bordering the purported fracture/suture line is compact bone (see also MacDougall et al. 2020: fig. 3), but the bone is more spongy (but still fairly compact) in the middle of the centrum and at the base of the neural arch (Fig. 6A, B). The fracture/suture line is present in all three sectioned vertebral centra. The posterior element in each centrum is smaller (shorter) and it bears the haemal arch (chevron). The notochordal canal is partially preserved in all three vertebrae, and is visible especially in the first one on the left side of Figure 6B.
The mesosaur first caudal vertebrae, here referred as the “pygal-like” segment, are holospondylous, a condition that is common in Amniota, where the pleurocentrum is the dominant bone and the intercentrum has been reduced in size, lost or fused to the pleurocentrum, and the centrum becomes as formed by a single element, which presumably is a pleurocentrum (Carroll 1968, 1989). The presence of a single central bone is a condition known as holospondylous or monospondylous; thus, both terms can be used.
Our observations suggest that the holospondylous condition in trunk and pygal mesosaur vertebrae could derive from, or it is equivalent to a reverse embolomerous condition, which is seen in the tail of mesosaurs and may reflect the ancestral condition. However, as demonstrated above in the previous section, the functional integration between intercentrum and pleurocentrum in juvenile specimens of early amniotes deserves to be re-examined.
The gastrocentrous pattern, typical of many amniotes, also characterizes the vertebrae of some lepospondyls (Holmes 1989; Laurin 1998; Danto et al. 2017). Among lepospondyls, tuditanomorph microsaurs retain intercentra, while Archerontiscus displays a vertebral embolomerous configuration (Carroll 1969; Danto et al. 2017). This variability in vertebral centrum pattern supports the high plasticity suggested by Pierce et al. (2013) for Carboniferous tetrapods (or stegocephalians), and our interpretation of the mesosaurid caudal vertebral configuration suggests that this evolutionary lability extended into basal amniotes.
Our data on the structure of caudal vertebrae of mesosaurs is congruent and complementary with those provided by MacDougall et al. (2020), given that the views are slightly different; the section shown by MacDougall et al. (2020: fig. 3) appears to be slightly parasagittal, or slightly oblique, with the left part showing the notochordal canal, which is not visible to the right. Thus, both reports show a core of trabecular bone covered by compact bone, and an unossified zone that separates a cranial and a caudal part of the centrum for more than half of its height.
Our observations are also reminiscent, but to a lesser extent, of the caudal centra of LeBlanc et al. (2018) and plausibly interpreted as adapted for caudal autotomy. LeBlanc et al. 2018: fig. 1f), but even in longitudinal, horizontal sections (LeBlanc et al. 2018: fig. 2; erroneously called “transverse sections” in the legend).
However, while our anatomical observations are broadly congruent, our functional and evolutionary interpretations differ rather sharply. We do not interpret these structures of the mesosaur caudal vertebrae as adaptations for autotomy (although this is a plausible interpretation for MacDougall et al. (2020: 5), three points militate against autotomy in mesosaurs.
First, the girdles (notably, the pelvic girdle, which is most relevant to this argument) are relatively small in mesosaurs (no larger than in Cisuralian terrestrial amniotes) (Modesto 2010). Marine reptiles that rely only or mostly on limbs for aquatic locomotion have expanded girdles, which serve for attachment of the appendicular muscles. This is especially obvious in Plesiosauria (O’Keefe 2002), which had a relatively small tail and obviously relied mostly on limbs to swim. The unexpanded gridles of mesosaurs do not suggest particularly powerful limbs.
Second, the negative allometry of the limb growth pattern compared to overall length reported by Verrière & Fröbisch (2022) militates for a decreasing role of limbs in aquatic locomotion through ontogeny. This also suggests that the limbs were not the primary thrust providers, although it is likely that they were involved in steering and may have provided additional thrust in some situations.
Third, disadvantageous or even simply unneeded adaptations for autotomy should be eliminated fairly quickly by natural selection. MacDougall et al. (2020: 2) suggested that “mesosaurs would have been theoretically capable of caudal autotomy, but likely did not utilize the behaviour.” We find this unlikely. Bone is a metabolically costly tissue to produce, and it is typically optimized to resist mechanical strain to which it is exposed through normal physical activity (de Buffrénil et al. 2021). Rupture planes weaken bones (vertebrae, in this case) and are detrimental if they are not required, especially because in that case, additional bone must be deposited to compensate for the weakness induced by this suboptimal structure.
Our observations support this conclusion to an extent, given that the caudal vertebrae of mesosaurs are very compact (Fig. 6), although this could also simply reflect the pachyosteosclerosis found in much of the mesosaur skeleton. Nevertheless, the contrast with the much less compact LeBlanc et al. (2018) is startling. Thus, if a putative terrestrial ancestor of mesosaurs had such fracture planes, these planes would have been quickly eliminated by natural selection. It is unlikely that the highly specialized morphotype of mesosaurs (most notably in their skull and long, slender teeth) arose without a similar optimization of vertebral structure for their lifestyle. Eliminating unneeded weakness (fracture planes) would presumably have occurred early in that process because that would have been a very cost-effective solution and given that mesosaur presacral vertebrae lacked fracture planes, all the required genes would have been present.
This last counter-argument begs the question of the function of this strange vertebral structure. Did it allow additional flexibility, notably between the pleurocentrum linked to the neural arch, and the intercentrum linked to the hemal arch, especially in young mesosaurs? Such flexibility might have been accomplished by relative movement between elements as long as they remained unfused, and by slight bending of bone (to a much reduced extent), after such a fusion occurred. This question deserves additional scrutiny, but will require additional ontogenetic and anatomical data, as well as biomechanical modeling to solve.
The enigmatic structure of caudal vertebrae of mesosaurs could also reflect a primitive condition as suggested above (which is not mutually exclusive of the hypothesis that it conferred additional flexibility).
Less probable, its presence in this taxon could also perhaps reflect the reduction of ossification that often accompanies a return to an aquatic lifestyle in tetrapods (Laurin et al. 2004), a pervasive phenomenon that was noticed long ago (Williston 1911). However this hypothesis is unlikely given the pachyosteosclerotic condition of most of the axial skeleton of mesosaurs, even from the earliest post-hatching stages (Piñeiro et al. 2012b).
If early developmental stages of early amniotes retained such a vertebral structure (a hypothesis that would require exceptional preservation of unmineralized tissues of embryos or potentially early juveniles to test), the adaptation for caudal autotomy in captorhinids may have involved retention of this early developmental structure.
Despite the reverse embolomerous condition described herein for the mesosaur caudal vertebrae, the architectural construction of the tail does not differ substantially from that observed in most groups of early amniote taxa. For instance, the caudal region, when preserved, is composed of vertebrae possessing an intercentrum positioned anterior to the pleurocentrum, as also occurs in the dorsal vertebral segment. Moreover, the intercentrum of vertebrae positioned posterior to the proximal string (pygal) with a variable number of elements, carries the haemal arches even near the tip of the tail (Heaton & Reisz 1980). However, a rapid revision of the available previous literature (old and more recent) shows that the mesosaur configuration could have been present in the caudal vertebrae of other basal tetrapod taxa. Starting with the study of Everett Olson (1936) on the axial musculature in early tetrapods, we can see some clues: caudal vertebrae assigned to Olson (1936: 280) and their haemal arches are fused to the posterior end of the centrum. The same condition is apparently present in the synapsid Sumida (1989: 155, fig. 4) and could have been developed in earlier taxa such as the seymouriamorphs, as documented by Laurin (1996: 658, fig. 5) for
In basal diapsids, there seems to be an anterior “pygal segment”, although it is shorter than that observed in Peabody 1952; Reisz 1981). Furthermore, the possibility of development of autotomy was suggested for Vaughn 1955: pl. 2).
Another interesting case is that of Berman & Reisz 1992), This suggests a reverse embolomerous condition in the more anterior vertebrae, but a return to the normal configuration at the posterior region. More recently, Colbert & Olsen 2001: fig. 9C). The hypothesis of autotomy suggested for captorhinids (i.e., LeBlanc et al. 2018) is difficult to ascertain because of the fragmentary nature of the analyzed specimens, as explained above. But taking into account the obvious presence of fracture-suture lines in most of the caudal vertebrae shown by LeBlanc et al. 2018) and the articulation of the haemal arches to the posterior end of the centrum observed in the string of caudal vertebrae belonging to a juvenile individual shown (LeBlanc et al. 2018: fig. 4b), it may be not surprising that capthorinids, diadectids, seymouriamorphs and some synapsids may have had the reverse embolomerous condition, but it was not previously detected.
Although mesosaurs are most frequently considered to be specialized aquatic amniotes (Araújo 1977; Oelofsen 1981; Modesto 1996, 1999; among others), they display a combination of primitive and derived characters, perhaps associated to a progressive although incomplete adaptation of an aquatic lifestyle (Núñez Demarco et al. 2018). However, the extent of such an adaptation in mesosaurs is not completely clear. It is true that some of the mesosaur features reveal limited capability for terrestrial locomotion, a trait also observed in numerous Carboniferous stegocephalians, such asSmithson 1989; Piñeiro et al. 2016; Herbst & Hutchinson 2018). The last two taxa, despite being outside Amniota, exhibit terrestrial specializations like the development of an amniotic tarsus with precursor bones arranged in the normal position of the astragalus and calcaneum but showing different stages of fusion with the intermedium and the fibulare (see figure 10 in Piñeiro et al. 2016). But mesosaurs may not have developed capabilities to an exclusively fully aquatic lifestyle, and they presumably inhabited shallow, plausibly hypersaline water. This is suggested by the the presence of pachyosteosteosclerosis in this taxon, a condition which was suggested to be developed in animals adapted to shallow aquatic environments (Houssaye 2009; Canoville & Laurin 2010). This hypothesis could be linked to the progressive draught of the Mangrullo and Irati seas, as was suggested in previous papers based on solid evidence suggesting an increasing of the water salinity and the deposition of evaporitic gypsum crystals (Piñeiro et al. 2012b, 2025; Petri et al. 2022).
Transitional features in mesosaurs have been interpreted as suggestive of possible affinities with other aquatic to semiaquatic taxa, such as the recumbitrostran microsaur lepospondyls (Piñeiro et al. 2016; Núñez Demarco et al. 2022), which were recently considered by some authors as being part of the stem of Amniota (Pardo et al. 2017). However, affinities between mesosaurs and recumbirostran microsaurs may be unlikely given that extensive phylogenetic analyses recovered the former as amniotes, close to the base of Sauropsida or at the base of Parareptilia. Furthermore, the position of recumbirostran microsaurs has been far more controversial; they are stem-amphibians according to Marjanović & Laurin (2019), but crown-amniotes according to Pardo et al. (2017) and Mann et al. (2023), among others.
However, mesosaurs have retained many ancestral characters, including: 1) the presence of five phalanges in the fifth pedal toe, whereas just four or three are observed in most tetrapods and basal amniotes (Clack et al. 2022); 2) a longer metatarsal V. Among basal stegocephalians, a long toe V, which is the longest of the pedal series, is a condition only present in the anthracosaur Silvanerpeton miripedes Clack, 1994 (Clack 1994; Ruta & Clack 2006) and the embolomerous Archeria Case 1915 (see Clack et al. 2022). While this character can be autapomorphic for mesosaurs or it can be an adaptation to an aquatic (or semi-aquatic) lifestyle, it is only shared with basal taxa; and 3) mesosaurs displayed an isometric growth pattern, a condition that could be considered of uncertain polarity, given that it is documented in few taxa, but that currently is only observed in basal or stem amniote taxa. The isometry is particularly marked at the level of limbs, as observed in microsaurs and other lepospondyls, sharply contrasting with the allometric pattern characterizing other early amniotes (Núñez Demarco et al. 2022).
According to a recent taxonomic review of Piñeiro et al. 2021; but see also Verrière & Fröbisch 2022), reducing even more the already low diversity in early tetrapods observed during the lifespan of mesosaurs in Southern Gondwana. Whereas mesosaur phylogenetic affinities remain controversial, a putative relationship between mesosaurs and the basalmost amniote groups seems possible, even at the level of the amniote stem group (Piñeiro et al. 2016; Núñez Demarco et al. 2022, but see also Pardo et al. 2017).
Other hypotheses have suggested a position on the reptilian stem (Laurin & Reisz 1995; Laurin & Piñeiro 2017) or at the base of Parareptilia (Modesto 2006), but they would have to be revised by including recently published new data about mesosaur anatomy, ontogeny, taxonomy and physiology.
Indeed, mesosaurs have always appeared as a very basal group in the main known phylogenetic trees on amniote relationships, either as basal sauropsids or as basal parareptiles (regarding that the later are also basal sauropsids), and that signal should be taken into account in future studies.
In this study, we reassess the proposed hypothesis that mesosaurs had developed caudal autotomy. Our investigation focuses on examining the biomechanical and behavioral consequences of tail loss in aquatic or semiaquatic taxa, demonstrating that no extant taxa with these lifestyles display autotomy, which appears to be restricted to terrestrial tetrapods. Our analysis reveals that mesosaurs may display a previously undocumented vertebral type in their caudal vertebrae consisting of a multipartite centrum formed by an intercentrum partially fused to the pleurocentrum, which is surprisingly located anterior (cranial) to it. The identification of these bones relies on the fact that the intercentrum carries a long chevron, while the pleurocentrum supports the neural arch. This novel vertebral arrangement is consistent with a reverse embolomerous type, which possibly occurred in other basal amniotes, as we preliminarily demonstrated in this work, but it may not have been detected because of taphonomic biases (the tail is incomplete or absent in most fossil tetrapods), and because it is often unclear to which pleurocentrum the intercentrum is functionally most tightly linked. These results support the plasticity and variability suggested to characterize the vertebral centrum configuration in basal tetrapods, which may have extended into basal amniotes, and which needs to be better documented to improve our understanding of vertebral evolution (Buckley et al. 2013). This study also makes one wonder if there has been overgeneralizations in whether the amniotic centrum is primarily pleurocentral in nature, especially in the early amniote members (Reviewer 1, personal communication).
We are indebted to the editor and Mr Xavier Jenkins (Idaho State University) and Dr Christian Sidor (University of Washington) that handled and made a very constructive revision of this manuscript, from which this contribution was greatly improved. We thanks Ana María Ribeiro (Seção de Paleontologia do Museu de Ciências Naturais/SEMA, Porto Alegre, RS.) for kindly provide the mesosaur specimens for the thin sections and Marina Bento Soares for allowing one of the authors (DMDF) to prepare them at the Laboratório de Paleohistologia do Museu Nacional/UFRJ, in the framework of the project: FAPERJ E-26/010.002178/2019. We also thank Erin Maxwell (Staatliches Museum für Naturkunde, Stuttgart, Germany) for kindly provide photographs of the mesosaur specimen shown in Figure 4 of this article. Comisión Sectorial de Investigación Científica (SCIC, Annual Grant to GP), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) – Brasil, Grant 153647/2024-8 for B. D. M. partially funded this research.
Fig. 1. —
A, GP-2E 653a, posterior region of presacral series, pelvic girdle and hind limbs, and anterior part of the tail showing only nine caudal vertebrae carrying ribs, which decrease in size posteriorly;
B, GP-2E 674b showing aggregation of juvenile and adult individuals. The whole “pygal-like” segment (ten vertebrae) is preserved. Scale bars: A, 30 mm; B, 10 mm.
Fig. 2. —
A,
B, FC-DPV 2206;
C, FC-DPV 2467;
D, FC-DPV 2231. These specimens show the presence of transverse processes and associated ribs (
yellow arrowheads), as well as a haemal arch (
red arrowheads) in the preserved vertebrae. They must consequently be part of the last of the “pygal-like” series because the anterior portion of that segment lack chevrons, whereas in the postpygal vertebrae, transverse processes are very poorly developed, if at all. Scale bars: 10 mm.
Fig. 3. —
A, SMNS 51560. Photograph of an almost complete skeleton of a subadult specimen showing the very long tail of mesosaurs, which exceeds the length of the skull plus the thoracic region. The end of the “pygal” segment and the beginning of the postpygal region (
white arrows) is identified by the presence of vertebrae showing the centrum divided in two areas by a subcentral “fracture/suture line”;
B, detailed view of the tail of SMNS 51560 with the outline of bones highlighted;
C, interpretive drawing of
B; the pygal segment (
pys) and the limi with the postpygal vertebrae are delimited by
bracketand
arrowrespectively, in
red color. Scale bars: 30 mm.
Fig. 4. —
A, MCN-2242, caudal fragment of six articulated vertebrae showing the conspicuous fracture/suture lines dividing the centrum into two consecutive regions (
black arrow) that look like distinct bones. In this specimen, the morphology of the vertebrae indicates that they are from the middle region of the tail (see
MacDougall
et al.
2018);
B, interpretive drawing of the specimen in
A, indicating the bones that form the caudal centrum in the post-pygal region;
C, FC-DPV 2094. Isolated caudal vertebra from the postpygal segment of the tail of a mature mesosaur. Note that the taphonomic dislocation between the anterior and posterior parts of the centrum (
white arrow) was produced following the “fracture/suture line” that characterizes these vertebrae;
D, interpretive drawing of
Cshowing the bones involved in the dislocation;
E, FC-DPV 2205. Caudal fragment consisting of five articulated vertebrae bearing their respective haemal arches. The “fracture/suture” area (
white arrow) is not as noticeable as in
A, but it is still fairly obvious;
F, interpretive drawing of
E, indicating the bones present in the mesosaur caudal centrum. Abbreviations:
ic, intercentrum;
pl, pleurocentrum. Scale bars: 10 mm.
Fig. 5. —
A-
D, photographs of isolated caudal vertebra belonging to vertebrate collection of Facultad de Ciencias, Montevideo, Uruguay (FC-DPV), showing the preserved space for the neural canal (
nc) and the discontinued notochord at the middle of the vertebral centrum (
n) in all of them;
E, isolated string of of MCN-PV 2158 A-A’, consisting of twelve dorsal vertebrae showing phosphatized notochordal tissues. Note that the notochord is clearly continuous through the complete sequence (
red arrow);
F, interpretive drawing of
E, showing the notochord detached in pink and the neural chord in blue, the
black arrowindicates the cranial direction;
G, isolated string including at least seven caudal vertebrae from the medio-distal region of the tail of MCN-PV 2158 A-A’. Some discontinuities (
red arrow) can be clearly seen in the notochord throughout the tail elements;
H, interpretive drawing of
G, showing the notochord detached in
pinkand the neural chord in
blue. The
black arrowindicates the cranial direction. Scale bars: A-D, 5 mm; E-G, 10 mm.
Fig. 6. —
A, MCN-PV-20007. Photograph of the complete specimen consisting in a caudal series that includes part of the pygal-like vertebrae (
black arrowindicating the last of these vertebrae) and part of the postpygal series. The vertebrae used for the thin section are the three enclosed by a white bracket on the left side;
B, picture of the thin section under polarized light. The integration of the two bones into a single element can be seen at the roughly central area of the centrum. Scale bars: A, 5 mm; B, 1 mm.
Fig. 7. —
A, FC-DPV 2318, almost complete right part of a skeleton (the left part was cut by a caterpillar machine) from the Mangrullo Formation of Uruguay. It can be appreciated that the suture-fracture plane (
arrows) is not as obvious in these vertebrae as it is seen in adult mesosaurs from the same location;
B, SMF-R 4512, almost complete very young individual from the Irati Formation of Brazil. Despite the apparent good preservation of the skeleton, the typical fracture plane is only observed in some of the caudal vertebrae (
arrow);
C, AMNH 23795, an early juvenile mesosaur from the Irati Formation of Brazil showing the same unnoticiable suture-fracture plane in vertebrae from the postpygal segment;
D, photographs of several isolated caudal vertebrae belonging to very young (juvenile) mesosaur specimens. Note that they are not part of the last caudal segment of adult mesosaurs because in such vertebrae the dorsal spine is bent posterior to almost remains in contact with the dorsal surface of the neural arch, or it is absent, a feature that is not present in the specimens shown herein. Scale bars: A-C, 20 mm; D, 5 mm.
Fig. 8. — Schematic drawings of the caudal vertebral morphotypes described for various stegocephalians, including amniotes:
A, rhachitomous;
B, reverse rhachitomous;
C, embolomerous (
D, gastrocentrous (
E, stereospondylous (
MetopasaurusLydekker, 1890);
F, holospondylous;
G, reverse embolomerous? (
Shishkin (1989); Embolomerous vertebrae are modeled after
Panchen (1966); gastrocentrous vertebrae are modeled after
Klembara & Bartík (1999); stereospondylous vertebrae are based on
Sulej (2007).
Journal of Developmental Biology9 (3): 32.
https://doi.org/10.3390/jdb9030032
Anais do Academia Brasileira Ciências48: 91-116.
Amblyrhynchus cristatus(Reptilia: Squamata: Iguanidae), from Isla Santa Cruz, Galápagos Islands.
Reptiles & Amphibians27 (3): 415-418.
https://doi.org/10.17161/randa.v27i3.14858
American Journal of Science
s3-37 (220): 310-313.
https://doi.org/10.2475/ajs.s3-37.220.310
— On a new genus of Iguanidae.
Zoological Journal
2: 204-208.
https://www.biodiversitylibrary.org/page/2255463
Dallasaurus turneri, a new primitive mosasauroid from the Middle Turonian of Texas and comments on the phylogeny of Mosasauridae (Squamata).
Netherlands Journal of Geosciences84 (3): 177-194.
https://doi.org/10.1017/S0016774600020965
Journal of Paleontology77 (1): 172-188.
https://doi.org/10.1666/0022-3360(2003)077<0172:HOTAAS>2.0.CO;2
Annals of the Carnegie Museum55 (1): 1-28.
https://doi.org/10.5962/p.215200
—
Dolabrosaurus aquatilis
, a small lepidosauromorph reptile from the Upper Triassic Chinle Formation of North-Central New Mexico.
Journal of Paleontology
66 (6): 1001-1009.
https://www.jstor.org/stable/1305953
Seymouria sanjuanensis(Amphibia, Batrachosauria) from the Lower Permian Cutler Formation of north-central New Mexico and the occurrence of sexual dimorphism in that genus questioned.
Canadian Journal of Earth Sciences24 (9): 1769-1784.
https://doi.org/10.1139/e87-169
— Permische Stegocephalen und Reptilien aus Texas.
Palaeontographica
51 (2-3): 1-120.
Frontiers in Zoology10 (17): 1-8.
https://doi.org/10.1186/1742-9994-10-17
Biological Journal of the Linnean Society100 (2): 384-406.
https://doi.org/10.1111/j.1095-8312.2010.01431.x
Tylosaurus proriger. Honors College Theses, Georgia, 284 p.
https://digitalcommons.georgiasouthern.edu/honors-theses/284
Pantylus.
Canadian Journal of Zoology46 (6): 1175-1192.
https://doi.org/10.1139/z68-168
Journal of Paleontology43 (1): 151-170.
https://www.jstor.org/stable/1302357
—The Order Microsauria
.
Memoirs of the American Philosophical Society
126: 211 p.
Annual Review of Ecology and Systematics13: 87-109.
https://www.jstor.org/stable/2097063
Historical Biology3 (1-2): 1-25.
https://doi.org/10.1080/08912968909386511
Bulletin of the Museum of Comparative Zoology at Harvard College143 (5): 321-364.
https://www.biodiversitylibrary.org/page/4638368
— A revision of the Cotylosauria of North America.
Carnegie Institution of Washington publication
145: 1-122.
https://doi.org/10.5962/bhl.title.45604
Bulletin of the Museum of Comparative Zoology at Harvard College144 (5): 353-407.
https://www.biodiversitylibrary.org/page/4227877
Silvanerpeton miripedes, a new anthracosauroid from the Viséan of East Kirkton, West Lothian, Scotland.
Transactions of the Royal Society of Edinburgh84 (3-4): 369-376.
https://doi.org/10.1017/S0263593300006179
Nature
418: 72-76.
Communications Biology5 (1): 1-10.
https://doi.org/10.1038/s42003-022-03199-x
American Museum Novitates3334: 1-24.
https://doi.org/10.1206/0003-0082(2001)334<0001:ANAUAR>2.0.CO;2
— Descriptions of extinct Batrachia and Reptilia from the Permian Formation of Texas.
Proceedings of the American Philosophical Society
17: 505-530.
https://doi.org/10.5962/bhl.title.104569
Proceedings of the American Philosophical Society23 (121): 1-21.
https://www.jstor.org/stable/982910
— Third contribution to the history of the Vertebrata of the Permian formation of Texas.
Proceedings of the American Philosophical Society
20 (112): 447-461.
https://www.jstor.org/stable/982692
— The reptilian order Cotylosauria.
Proceedings of the American Philosophical Society
34 (149): 436-457.
https://www.jstor.org/stable/982900
—
Das Thierreich, geordnet nach seiner Organisation : als Grundlage der Naturgeschichte der Thiere und Einleitung in die vergleichende Anatomie
(Nach der zweiten, vermehrten Ausgabe übersetzt und durch Zusätze erweitert / von F.S. Voigt. edition).
Journal of Morphology278 (9): 1262-1283.
https://doi.org/10.1002/jmor.20709
— On a Terrestrial Mollusk, a Millepede, and new Reptiles, from the Coal Formation of Nova Scotia.
Quarterly Journal of the Geological Society, London
16: 268-277.
Vertebrate Skeletal Histology and Paleohistology.CRC Press, Boca Raton, Florida: xii + 825.
https://books.google.fr/books?id=tJcwEAAAQBAJ
Eocaptorhinus laticeps(Williston).
Canadian Journal of Earth Sciences23 (9): 1288-1296.
https://doi.org/10.1139/e86-124
Journal of Paleontology83 (6): 981-989.
https://doi.org/10.1666/09-014.1
Physiological and Biochemical Zoology86 (6): 645-658.
https://doi.org/10.1086/673864
— Deep-time evolution of regeneration and preaxial polarity in tetrapod limb development.
Nature
527: 231-234.
https://doi.org/10.1038/nature15397
Philosophical Transactions of the Royal Society, Series B187: 1-57.
https://doi.org/10.1098/rspl.1895.0044
The Evolution of the Vertebral Column: A Contribution to the Study of Vertebrate Phylogeny. Cambridge University Press, 378 p.
Cladistics4 (2): 105-209.
https://doi.org/10.1111/j.1096-0031.1988.tb00514.x
in
M. J. (ed.),
BentonThe phylogeny and classification of the tetrapods. Volume 1: amphibians, reptiles, birds. Vol. 1. Clarendon Press, Oxford: 103-155.
in
M. J. (ed.),
BentonThe phylogeny and classification of the tetrapods, Volume 1: amphibians, reptiles, birds. Clarendon Press, Oxford. Systematics Association Special Volume 35A: 103-155.
Mesosaurus tenuidensreptile fossile de l’Afrique australe.
Académie des Sciences et Lettres de Montpellier, Mémoires de la Section des Sciences6 (2): 169-175.
Physiological and Biochemical Zoology86 (6): 631-644.
https://doi.org/10.1086/673889
Journal of Experimental Biology219 (16): 2416-2422.
https://doi.org/10.1242/jeb.124024
Biology Bulletin47: 389-398.
https://doi.org/10.1134/S1062359020040068
—
Catalogue of the specimens of amphibia in the collection of the British Museum. Part II. Batrachia Gradientia
. Order of the Trustees, London, 72 p.
https://www.biodiversitylibrary.org/page/41684042
Bulletin of the Oklahoma Geological Survey127: 1-84.
Eocaptorhinus laticeps(Williston).
Journal of Paleontology54 (1): 136-143.
Crassigyrinus scoticusfrom computed tomography.
Earth and Environmental Science Transactions of the Royal Society of Edinburgh109 (1-2): 157-175.
https://doi.org/10.1017/S1755691018000804
Proterogyrinus scheeleiRomer, and the early evolution of tetrapods.
Philosophical Transactions of the Royal Society B306 (1130): 431-527.
https://doi.org/10.1098/rstb.1984.0103
Historical Biology2 (2): 111-124.
https://doi.org/10.1080/08912968909386495
— The skull and the axial skeleton of the Lower Permian anthracosauroid amphibian
Archeria crassidisca
Cope.
Palaeontographica, Abteilung A.
207: 161-206.
Integrative Zoology4 (4): 325-340.
https://doi.org/10.1111/j.1749-4877.2009.00146.x
— Ueber
Gephyrostegus bohemicus
n. g. n. sp.
Zeitschrift der Deutschen Geologischen Gesellschaft
54: 127-132.
— On the fish-like tail in the ichthyostegid stego-cephalians, with descriptions of a new stegocephalian and a new crossopterygian from the Upper Devonian of East Greenland.
Meddelelser om Grønland
114 (12): 1-90.
Palaeontology49 (4): 837-856.
https://doi.org/10.1111/j.1475-4983.2006.00569.x
DiscosauriscusKuhn, a seymouriamorph tetrapod from the Lower Permian of the Boskovice Furrow (Czech Republic).
Transactions of the Royal Society of Edinburgh90 (4): 287-316.
https://doi.org/10.1017/S0263593300002649
Biological Journal of the Linnean Society112 (4): 747-764.
https://doi.org/10.1111/bij.12301
Platecarpus tympaniticus(Squamata, Mosasauridae): osteology of an exceptionally preserved specimen and its insights into the acquisition of a streamlined body shape in mosasaurs.
Journal of Vertebrate Paleontology32 (6): 1313-1327.
https://doi.org/10.1080/02724634.2012.699811
— Labyrinthodontia,
inQuenstedt W.
(ed.), Fossilium Catalogus, I. Animalia, 61.W. Junk, Berlin
: 1-114.
— New Mid-Pennsylvanian reptiles from Kansas, Trans.
Kansas Academy of Science
47: 381-390.
Ariekanerpeton, a Lower Permian seymouriamorph (Tetrapoda: Seymouriamorpha) from Tadzhikistan.
Journal of Vertebrate Paleontology16 (4): 653- 665.
https://doi.org/10.1080/02724634.1996.10011355
Annales des Sciences Naturelles, Zoologie, Paris, 13e Série19 (2): 99-114.
https://doi.org/10.1016/S0003-4339(98)80004-X
Stegocephali,
inde Queiroz K., Cantino P. D. & Gauthier J. A. (eds),
Phylonyms: A companion to the PhyloCode. CRC Press, Boca Raton, Florida: 741-745.
https://doi.org/10.1201/9780429446276
Tetrapoda,
inde Queiroz K., Cantino P. D. & Gauthier J. A. (eds),
Phylonyms: A companion to the PhyloCode. CRC Press, Boca Raton, Florida: 759-764. https://doi.org/10.1201/9780429446276
Frontiers in Earth Science5 (88): 1-13.
https://doi.org/10.3389/feart.2017.00088
— Response: Commentary: A reassessment of the taxonomic position of mesosaurs, and a surprising phylogeny of early amniotes.
Frontiers in Earth Science
6 (99):1-9.https://doi.org/10.3389/feart.2018.00099
Zoological Journal of the Linnean Society113 (2): 165-223.
https://doi.org/10.1111/j.1096-3642.1995.tb00932.x
Paleobiology30 (4): 589-613.
https://doi.org/10.1666/0094-8373(2004)030<0589:TEOLBM>2.0.CO;2
Scientific reports8 (1): 3328.
https://doi.org/10.1038/s41598-018-21526-3
Scientific reports11 (1): 21818.
https://doi.org/10.1038/s41598-021-01309-z
—
Catalogue of the Fossil Reptilia and Amphibia in the British Museum (Natural History). Part IV. Containing the orders Anomodontia, Ecaudata, Caudata, and Labyrinthodonta, and Supplement
.Trustees, London:
1-295.
https://doi.org/10.5962/bhl.title.61848
Frontiers in Earth Science6: 99.
https://doi.org/10.3389/feart.2018.00099
Scientific reports10 (1): 1-9.
https://doi.org/10.1038/s41598-020-63625-0
Odonterpeton triangularefrom the Pennsylvanian of Linton, Ohio, and major features of recumbirostran phylogeny.
Zoological Journal of the Linnean Society197 (3): 64-655.
https://doi.org/10.1093/zoolinnean/zlac043
PeerJ6: e5565.
https://doi.org/10.7717/peerj.5565
Copeia2010 (3): 468-474.
https://doi.org/10.1643/CP-09-188
Microbrachis(Tetrapoda; Microsauria).
Lethaia41 (3): 257-261.
https://doi.org/10.1111/j.1502-3931.2007.00049.x
Mesosaurus tenuidensand
Stereosternum tumidum(Amniota: Mesosauridae) from the Lower Permian of Gondwana. PhD thesis, University of Toronto, XVIII + 279 p.
https://library-archives.canada.ca/eng/services/services-libraries/theses/Pages/item.aspx?idNumber=46559855
Stereosternum tumidumCope.
Palaeontologia africana35: 7-19.
Mesosaurus tenuidens: implications for relationships and palaeobiology.
Zoological Journal of the Linnean Society146: 345-368.
https://doi.org/10.1111/j.1096-3642.2006.00205.x
Mesosaurus tenuidensfrom the Gondwanan Permian.
Journal of Vertebrate Paleontology30 (5): 1378-1395.
https://doi.org/10.1080/02724634.2010.501443
Frontiers in Earth Science12: 1155806.
https://doi.org/10.3389/feart.2024.1155806
Mesosaurusa fully aquatic reptile?
Frontiers in Ecology and Evolution6 (109): 1-25.
https://doi.org/10.3389/fevo.2018.00109
Acta Palaeontologica Polonica67 (2): 509-542.
https://doi.org/10.4202/app.00931.2021
An Anatomical and Systematic Study of the Family Mesosauridae (Reptilia, Proganosauria) with Special Reference to its Associated Fauna and Palaeoecological Environment in the Whitehill Sea. PhD thesis, University of Stellenbosch, 259 p.
Revista Brasileira de Geociências13 (1): 1-6.
https://doi.org/10.25249/0375-7536.19831310106
Paleobiology28 (1): 101-112.
https://doi.org/10.1666/0094-8373(2002)028<0101:TEOPAP>2.0.CO;2
Microbrachisand
Hyloplesion(Tetrapoda: Lepospondyli) and implications for the developmentalpatterns of extinct, early tetrapods.
PLoS ONE10 (6): e0128333. 1-69.
https://doi.org/10.1371/journal.pone.0128333
Journal of Morphology59 (2): 265-311.
https://doi.org/10.1002/jmor.1050590204
inBellairs A. & Cox B. (eds),
Morphology and Biology of Reptiles. Vol. 3. Linnean Society of London, Dorchester: 1-30.
Memoirs of the American Museum of Natural History1 (IV): 167-188.
Eogyrinus attheyi.
Journal of Zoology150 (2): 199-222.
https://doi.org/10.1111/j.1469-7998.1966.tb03004.x
Nature546: 642-645.
https://doi.org/10.1038/nature22966
Petrolacosaurus kansensisLane, a Pennsylvanian reptile from Kansas.
Paleontological Contributions1: 1-41.
Journal of Sedimentary Research92 (11): 1053-1070.
https://doi.org/10.2110/jsr.2022.011
Nature494 (7436): 226-229.
https://doi.org/10.1038/nature11825
inVeroslavsky G., Ubilla M. & Martínez S. (eds),
Cuencas sedimentarias de Uruguay: Geología, Paleontología y Recursos Minerales–Paleozoico. Vol. 3. Dirac–Facultad de Ciencias, Montevideo: 257-278.
Acta Palaeontologica Polonica57 (2): 299-318.
https://doi.org/10.4202/app.2010.0113
Historical Biology24 (6): 620-630.
https://doi.org/10.1080/08912963.2012.662230
PeerJ4: e2036.
https://doi.org/10.7717/peerj.2036
Stereosternumand
Brazilosaurusvalid taxa?
Revista Brasileira de Paleontologia24 (3): 205-235.
https://doi.org/10.4072/rbp.2021.3.04
Fossil Studies3 (1): 1-24 p.
https://doi.org/10.3390/fossils3010001
University of Kansas Publications of the Museum of Natural History7: 1-74.
Journal of Systematic Palaeontology22 (1):
https://doi.org/10.1080/14772019.2023.2296078
Anolis carolinensis).
The Anatomical Record295 (10): 1596-1608.
https://doi.org/10.1002/ar.22524
Bulletin of the Museum of Comparative Zoology99 (1): 1-368.
Osteology of the Reptiles. University of Chicago Press, Chicago, 772 p.
Kirtlandia10: 1-16.
Silvanerpeton miripedes, a stem amniote from the Lower Carboniferous of East Kirkton, West Lothian, Scotland.
Transactions of the Royal Society of Edinburgh: Earth Sciences97: 31-63.
https://doi.org/10.1017/S0263593300001395
Journal of Systematic Palaeontology5 (1): 69-122.
https://doi.org/10.1017/S1477201906002008
Ethology Ecology & Evolution31 (1): 12-27.
https://doi.org/10.1080/03949370.2018.1477836
Proceedings of the Royal Society of London. Series B: Biological Sciences266 (1434): 2147-2151.
https://doi.org/10.1098/rspb.1999.0901
Progress in Zoology35: 180-195.
Frontiers in Earth Science5 (23): 1-22.
https://doi.org/10.3389/feart.2017.00023
Micrablepharus atticolus(Squamata, Gymnophthalmidae).
Diversity13 (11): 562.
https://doi.org/10.3390/d13110562
Nature342: 676-677.
https://doi.org/10.1038/342676a0
Scottish Journal of Geology26: 137-138.
https://doi.org/10.1144/sjg26020137
Metoposaurus, a temnospondyl from the late Triassic of Poland.
Palaeontologia Polonica64: 29-143.
Varanosaurus acutirostris(Amniota, Synapsida).
Journal of Vertebrate Paleontology9 (4): 451-458.
https://doi.org/10.1080/02724634.1989.10011777
Behavioral Ecology and Sociobiology75: 1-10.
https://doi.org/10.1007/s00265-021-02982-w
inKalandadze N. N., Očev V. G., Tatarinov L. P., Čudinov P. K. & Šiškin M. A. (eds),
Verhnepermskie i mezozoijskie zemno−vodnye i presmykaû
ŝ
iesâ CCCP. Nauka, Moskva: 73-92. [in Russian].
Journal of Zoology304 (1): 13-20.
https://doi.org/10.1111/jzo.12519
Araeoscelisrestudied.
Bulletin of the Museum of Comparative Zoology113 (5): 305-467.
PeerJ10: e13866.
https://doi.org/10.7717/peerj.13866
Mesosaurus tenuidens(Gervais 1867) from Uruguay.
Historical Biology28 (7): 963-971.
https://doi.org/10.1080/08912963.2015.1075018
Microbrachis pelikaniand comparison with extant salamanders and squamates.
Journal of Zoology304: 34-44.
https://doi.org/10.1111/jzo.12516
Zoology—Analysis of Complex Systems103: 68-88.
Philosophical Transactions of the Royal Society(B) 214 (411-420): 189-257.
https://doi.org/10.1098/rstb.1926.0006
University Geological Survey of Kansas4 (5): 81-347.
—New or little known Permian vertebrates. Pariotichus.
Biological Bulletin
17 (3): 241-255.
https://doi.org/10.2307/1536117
Cacops,
Demospondylus; new genera of Permian vertebrates.
Geological Society of America Bulletin21: 249-284.
American Journal of Science31: 378-398.
https://doi.org/10.2475/ajs.s4-31.185.378
inGregory W. K. (ed.), Harvard University Press, Cambridge, Massachusetts, 300 p.
Anatomical Histologia Embyologia43 (2): 90-102.
https://doi.org/10.1111/ahe.12050
eLife12: e83163.
https://doi.org/10.7554/eLife.83163