Caseidae

Caseidae are an extinct family of basal synapsids that lived from the Late Carboniferous to Middle Permian between about 300 and 265 million years ago. Fossils of these animals come from the south-central part of the United States (Texas, Oklahoma, and Kansas), from various parts of Europe (European Russia, France, Germany, Sardinia, and Poland), and possibly from South Africa if the genus ''Eunotosaurus'' is indeed a caseid as some authors proposed in 2021. Caseids show great taxonomic and morphological diversity. The most basal taxa were small insectivorous and omnivorous forms that lived mainly in the Upper Carboniferous and Lower Permian, such as '' Eocasea'', '' Callibrachion'', and '' Martensius''. This type of caseid persists until the middle Permian with ''Phreatophasma'' and may be ''Eunotosaurus''. During the early Permian, the clade is mainly represented by many species that adopted a herbivorous diet. Some have evolved into gigantic forms that can reach in length, such as '' Cotylorhynchus hancocki'' and '' Alierasaurus ronchii'', making them the largest Permian synapsids. Caseids are considered important components of early terrestrial ecosystems in vertebrate history because the numerous herbivorous species in this family are among the first terrestrial tetrapods to occupy the role of primary consumer. The caseids experienced a significant evolutionary radiation at the end of the early Permian, becoming, with the captorhinid eureptiles, the dominant herbivores of terrestrial ecosystems in place of the edaphosaurids and diadectids.

In 2016 and 2022, paleontologists proposed a semiaquatic lifestyle for the most derived genera like ''Cotylorhynchus'' and ''Lalieudorhynchus'', but this hypothesis is disputed by other researchers.

With a fossil record spanning from the Late Carboniferous to the Middle Permian, caseids are one of the basal synapsids groups (formerly known as “pelycosaur”) having the largest stratigraphic range. They also represent one of only two basal synapsid groups (along with the Varanopidae) to survive in therapsid-dominated terrestrial communities. Thus, the last known caseids come from the strata of the middle Permian (Upper Roadian-Wordian) of France and European Russia, where they cohabited notably with dinocephalians. These last caseids still show a certain morphological diversity with medium to large herbivores ('' Ennatosaurus'' and '' Lalieudorhynchus''), as well as small predatory or omnivorous forms such as ''Phreatophasma'' and possibly ''Eunotosaurus''. Caseids are so far unknown in Upper Permian strata and probably disappeared at the end of the Middle Permian. They were replaced by pareiasaurs (with similar dentition) and dicynodonts.

Description

Caseids measured from less than to in length. They had a small head wider than high and with a forward-inclined snout, a very short neck, a long tail, robust forelimbs, and a body of variable proportions depending on their diet. Small insectivorous species like '' Eocasea'' had an unexpanded trunk. Others with an omnivorous diet like '' Martensius'' had a barely enlarged rib cage, a more elongated skull, smaller nostrils, and a snout less inclined forward than in herbivorous caseids. The latter were characterized by their disproportionately small skull compared to the size of the body. The postcranial skeleton indeed shows a spectacular increase in the volume of the rib cage, which becomes very wide and barrel-shaped, probably to accommodate a particularly developed intestine, necessary for the digestion of high-fiber rich plants. In these forms, the skull has very large external nostrils and a very short facial region with a strong forward inclination of the end of the snout which clearly overhangs the dental row. The temporal fenestrae are also relatively large (especially in '' Ennatosaurus''), the supratemporals are large in size, and, on the occipital surface, the paroccipital processes are massively developed, establishing strong supporting contacts with the squamosals. The dorsal surface of the skull is covered with numerous small pits. These suggest the presence of large scales on the head of these animals. Numerous labial foramina running parallel to the ventral edge of the premaxilla and maxilla, as well as along the dorsal edge of the dentary, suggest the presence of scaly "lips" which must have concealed the dentition when the jaws were closed. The teeth, simply conical and pointed in insectivorous species, adopt in herbivorous species a leafy or spatulate morphology and are provided with more or less numerous cuspules. Numerous small teeth also adorned several bones of the palate. Herbivorous species do not show a simple evolutionary trend towards increasing tooth complexity. Thus, the teeth of the basal taxa ''Casea'' and '' Arisierpeton'' have three cuspules just like in the more derived forms ''Cotylorhynchus'' and '' Caseopsis''. ''Ennatosaurus'' and '' Euromycter'', which occupy an intermediate phylogenetic position, have teeth bearing 5 to 7 cuspules and 5 to 8 cuspules respectively. '' Angelosaurus'', one of the most derived caseids, has teeth with 5 cuspules. In ''Angelosaurus'' the teeth have a bulbous morphology with very short and wide crowns. Their sturdiness and the significant wear they show indicate that ''Angelosaurus'' must have fed on tougher plants than those on which most other herbivorous caseids fed. Herbivorous caseids also show very different dietary adaptations from those seen in another group of basal synapsids, the Edaphosauridae. The latter had, in addition to the marginal dentition, a dental battery made up of numerous teeth located both on the palate and on the inner surface of the lower jaws. In herbivorous caseids, the palatal teeth are smaller, and the inner surface of the lower jaws bears no teeth. Instead of a dental battery, they had a massive tongue (as indicated by the presence of a highly developed hyoid apparatus found in ''Ennatosaurus'' and ''Euromycter'') perhaps rough, with which they had to compress food against the palatal teeth.

The forelimbs of caseids are often more robust than the hindlimbs. It has indeed been observed that the bones of the forelimbs gained in robustness from the beginning of the evolution of the group, before the appearance of large species, while the hindlimbs remained slenderer. These characteristics suggest that the initial strengthening of the forelimbs was probably related to a particular function such as digging, and that this trait was later exapted by more derived and larger caseids to support their weights of up to several hundred kilograms. During their evolutionary history, caseids also show a reduction in their phalangeal formula. The most basal caseids like ''Eoasea'', '' Callibrachion'', and ''Martensius'' possessed the plesiomorphic condition of early amniotes with a phalangeal formula of 2-3-4-5-3 for manus and 2-3-4-5-4 for pes. In ''Euromycter'' the manus has a formula of 2-3-4-4-3 (the pes is unknown). In the more derived forms like ''Cotylorhynchus'' the manus and pes show a phalangeal formula of 2-2-3-3-2. Along with this reduction in the number of phalanges, the proportions of the autopods also change in derived caseids with metacarpals, metatarsals, and phalanges becoming shorter and broader. At the extreme of this specialization the genus ''Angelosaurus'' has short, broad, and smooth ungual phalanges which resemble hooves rather than claws.

Footprints

Many vertebrate tracks have been proposed as belonging to Caseidae. In the early 2000s, large footprints known as '' Brontopus giganteus'' from the Permian Lodève basin in southern France were considered to belong either to a caseid or dinocephalian therapsid. In 2019, Lorenzo Marchetti and colleagues, however, determined that dinocephalians were most likely the trackmakers of the ichnogenus ''Brontopus''. In 2012, Rafael Costa da Silva and colleagues proposed that the ichnogenus '' Chelichnus'', widely distributed in Permian desert facies (fossil dunes) of Europe, North America and South America, could represent caseids footprints. In 2019, Marchetti and colleagues, however, reinterpreted ''Chelichnus'' as a ''nomen dubium'' and a taphotaxon, this type of track showing false anatomical features generated by locomotion on sandy inclined paleosurface. In 2014, Eva Sacchi and colleagues described the ichnotaxon '' Dimetropus osageorum'' from about a hundred isolated footprints and several trackways from the early Permian Wellington Formation in Oklahoma. The morphological study of these footprints and their comparison with tetrapod skeletons revealed that they probably belong to a large caseid comparable in size to '' Cotylorhynchus romeri'' (the latter from more recent strata). According to Sacchi and colleagues, some footprints from the Lodève Basin (unspecified geological formation) are similar to those from the Wellington Formation and these authors designate them as ''Dimetropus'' cf. ''osageorum''. The study by Sacchi et al. also demonstrates that the ichnogenus ''Dimetropus'' exhibits great morphological variation and that its producers can be assigned to different zoological groups among non-therapsid synapsids and not just Sphenacodontidae as once thought. In 2021, Rafel Matamales-Andreu and colleagues assigned footprints found in the Lower Permian (Artinskian-Kungurian) Port des Canonge Formation in Mallorca to a caseid. These footprints resemble those of ''D. osageorum'' but they also have differences. These footprints are left in open nomenclature as cf. ''Dimetropus'' sp.. They are, however, smaller than those of ''D. osageorum'' and would have been produced by a caseid of modest size with proportions comparable to '' Ennatosaurus''.

Paleobiology

Diets

During their evolutionary history, caseids shifted from faunivorous to herbivorous diet, a pattern that also occurred independently in other Carboniferous and Permian tetrapod groups such as Captorhinidae and Edaphosauridae. Earliest and most basal caseids, such as the late Carboniferous '' Eocasea'' and the early Permian '' Callibrachion'' had an unexpanded rib cage and dentition composed of very small conical teeth suggesting an insectivorous diet. Another basal caseid, '' Martensius'', has a slightly enlarged barrel-shaped trunk and dentition in which teeth indicative of an insectivorous diet in juveniles have been ontogenetically replaced in adults by teeth suggesting an omnivorous diet. In ''Martensius'', the adult was still able to feed on insects, but it also possesses a draft of the herbivorous diet specializations present in later caseids, such as a relatively short, slightly forward-inclined snout, and a dentition that is almost homodont in the upper jaws and completely homodont in lower jaws. The sequence of dental trait acquisition in ''Martensius'' suggests that intestinal vegetation processing preceded oral processing in the evolution of caseid herbivory. A juvenile insectivorous diet would have provided the opportunity for successful introduction into the intestine of microorganisms capable of endosymbiotic cellulolysis, particularly if the prey ingested were herbivorous insects which harbor such microorganisms in their viscera. Subsequently, the caseids adopted a strictly herbivorous diet and evolved into gigantic forms. These herbivorous caseids had spatulate teeth equipped with more or less numerous cuspules and a very enlarged and barrel-shaped rib cage which must have housed highly developed intestines necessary for the digestion of plants with low nutritional value. This adaptation would partly explain the diversification and expansion of the group at the end of the Lower Permian and during the Middle Permian, because it allowed them to exploit a fiber-rich plant resource that had by then become abundant and widespread. Nevertheless, small probably faunivorous caseids like ''Phreatophasma'' seem to have persisted until the Middle Permian.

Semiaquatic vs terrestrial lifestyle

Caseids are generally considered primarily terrestrial animals. Everett C. Olson in particular considered that the degree of ossification of the skeleton, the relatively short feet and hands, the massive claws, the limbs with very powerful extensor muscles, and the solid sacrum, strongly suggested a terrestrial lifestyle. Olson did not rule out that the caseids spent some time in water, but he considered locomotion on land to be an important aspect of their lifestyle. It has been suggested that the very powerful forelimbs, with strong and very tendinous extensor muscles, as well as very massive claws, could be used to dig up roots or tubers. However, the very short neck implied a low amplitude of vertical movements of the head which precluded the large species from feeding at ground level. Another hypothesis suggests that the caseids could have used their powerful forelimbs to fold large plants towards them, which they would have torn off with their powerful claws. Other hypotheses suggest that some caseids such as ''Cotylorhynchus'' used their limbs with powerful claws to defend themselves against predators, or during intraspecific activities linked in particular to reproduction. According to Olson, an interesting thing about this, is that almost all known specimens of the species '' Cotylorhynchus hancocki'' have one to ten ribs broken and healed during life. Finally, for some authors, the large derived caseids would have been semiaquatic animals that used their hands with large claws like paddles, which could also be used to manipulate the plants on which they fed.

In 2016, Markus Lambertz and colleagues questioned the terrestrial lifestyle of large caseids like ''Cotylorhynchus''. These authors showed that the bone microstructure of the humerus, femur and ribs of adult and immature specimens of '' Cotylorhynchus romeri'' resembled that of aquatic animals more than that of terrestrial animals, the bones having a very spongy structure, an extremely thin cortex, and having no distinct medullary canal. This low bone density would have been a handicap for animals weighing several hundred kilos with a strictly terrestrial lifestyle. Lambertz et al. also argued that the joints between the vertebrae and the dorsal ribs allowed only small ranges of motion of the rib cage, thus limiting costal ventilation. To overcome this, they proposed that a proto- diaphragm was present to facilitate breathing, especially in aquatic environment. These authors also consider that the arid paleoclimates to which the caseid deposits correspond are not incompatible with an aquatic lifestyle of these animals. These paleoenvironments in fact included a significant number of water bodies (rivers, lakes and lagoons). The arid conditions could have been the reason why the animals would sometimes congregate and eventually die. In addition, arid environments have a low density of plants, which would require even more locomotor effort to find food. Thus, for Lambertz et al., large caseids like ''Cotylorhynchus'' must have been mainly aquatic animals that only came on dry land for the purposes of reproduction or thermoregulation.

This hypothesis is however disputed by Kenneth Angielczyk and Christian Kammerer as well as by Robert Reisz and colleagues based on paleontological and taphonomic data combined with the absence in these large caseids of morphological adaptations to an aquatic lifestyle. According to Angielczyk and Kammerer, the low bone density of caseids identified by Lambertz et al. does not resemble that of semiaquatic animals, which tend to have a more strongly ossified skeleton to provide passive buoyancy control and increased stability against current and wave action. ''Cotylorhynchus'' bone microstructure is more similar to what is seen in animals living in the open ocean, such as cetaceans and pinnipeds, which emphasize high maneuverability, rapid acceleration and hydrodynamic control of buoyancy. However, the caseid morphology was totally incompatible with a pelagic lifestyle. Thus, due to these unusual data, Angielczyk and Kammerer consider that the available evidence is still insufficient to question the more widely assumed terrestrial lifestyle of caseids. Robert Reisz and colleagues also dispute the supposed semiaquatic lifestyle of the caseids on the fact that the latter possess no morphological adaptations to an aquatic lifestyle and, in the case of the species ''Cotylorhynchus romeri'', on the interpretation that this animal lived in a dry environment for part of the year as indicated by the presence of numerous skeletons of the amphibian '' Brachydectes'' preserved in aestivation and of the lungfish '' Gnathorhiza'', another well-known aestivator.

In 2022, Werneburg and colleagues proposed a somewhat different semiaquatic lifestyle, in which large caseids like '' Lalieudorhynchus'' (whose bone texture is even more osteoporotic than in ''Cotylorhynchus'') would be ecological equivalents of modern hippos, passing part of their time in the water (being underwater walkers rather than swimming animals) but coming on dry land for food.

Evolution

Caseids first appear in the fossil record at the end of the Carboniferous and are already present in both North America and Europe with small predatory forms like '' Eocasea'' and '' Datheosaurus''. These faunivorous caseids also exist at the beginning of the lower Permian, such as '' Callibrachion'', and may have existed until the base of the middle Permian with ''Phreatophasma''. During the Permian, the representatives of the clade mainly evolved towards herbivory. These herbivorous caseids experienced an important evolutionary radiation during the second half of the lower Permian by becoming, with the moradisaurine captorhinid eureptiles, the main herbivores of terrestrial ecosystems instead of edaphosaurids and diadectids. The decline of edaphosaurids and the propagation of caseids coincides with an aridification of the environment that occurred from the Artinskian and which would have favored the caseid expansion. Sedimentological and taphonomic data indicate that the majority of edaphosaurids favored humid habitats (their remains are found mainly in lacustrine and marshy deposits) while herbivorous caseids generally lived in drier biotopes where ponds and streams water were ephemeral. The last caseids date from the Middle Permian and are mainly known in Europe with ''Phreatophasma'' and '' Ennatosaurus'' from the Roadian-Wordian of Russia, '' Alierasaurus'' from the Roadian-(Wordian?) of Sardinia, and '' Lalieudorhynchus'' from the late Wordian-early Capitanian of southern France. In North America, '' Angelosaurus romeri'' and '' Cotylorhynchus bransoni'' from the Chickasha Formation in Oklahoma probably date to the early Roadian, while the caseids from the San Angelo Formation in Texas are slightly older and may straddle the Kungurian-Roadian boundary but it is not yet clear whether they date from the latest Kungurian or from the earliest Roadian.

Paleobiogeography

Caseid fossils have been found in the southern and central United States (Texas, Oklahoma, Kansas), France, Germany, Poland, Sardinia, and European Russia. This geographical distribution corresponds to the paleoequatorial belt of Pangaea during the Carboniferous and the Permian, with the exception of the Russian localities which were located at the level of the 30th parallel north where a more temperate climate prevailed. The absence in Russia of terrestrial vertebrate localities prior to the Kungurian does not allow us to know the precise moment of the arrival of caseids in this region of the world. According to Werneburg and colleagues, the presence of caseids at this paleolatitude suggests their possible existence in the temperate regions of Gondwana. A possible Gondwanan occurrence was proposed as early as the 1990s by Michael S.Y. Lee and in 2021 by Asher J. Lichtig and Spencer G. Lucas, who reinterpreted the middle Permian taxon ''Eunotosaurus'' from South Africa as a small burrowing caseid. Between these two dates, other researchers classified ''Eunotosaurus'' as a parareptile or a pantestudines. If the first three authors are correct, ''Eunotosaurus'' would be the first caseid found in the Southern Hemisphere and the last known representative of the family with a latest Capitanian age for the most recent specimens. Elsewhere in Gondwana, the presence of the ichnotaxon '' Dimetropus'' in the Permian of Morocco suggests the future discovery of basal synapsids (including caseids) in the Permian basins of North Africa, which were also part of the paleoequatorial belt and constituted one of the main migratory routes between the Northern and Southern Hemispheres.

Phylogeny

The family Caseidae was erected by Samuel Wendell Williston in 1911. In 1940, Alfred Sherwood Romer and L.W. Price placed Caseidae and Edaphosauridae in the same suborder, which they named Edaphosauria. This group is now abandoned, the edaphosaurids being closer to the Sphenacodontia (with which they form the clade Sphenacomorpha) than to the caseids. The latter are grouped with the Eothyrididae in the clade Caseasauria, which represent the most basal synapsids.

The first phylogenetic analysis of caseids was published in 2008 by Hillary C. Maddin and colleagues. In this analysis, the genus '' Oromycter'' occupies the most basal position within the clade. '' Ennatosaurus'' is the sister group of a clade containing '' Cotylorhynchus romeri'' and '' Angelosaurus dolani''. This analysis reveals for the first time the paraphyly of the genus ''Casea'', the species ''“Casea” rutena'' representing a distinct genus which will be named in 2011 '' Euromycter''.

Below is the first cladogram of caseids published by Maddin et al. in 2008.

Another phylogenetic analysis carried out in 2012 by Benson includes the genus '' Trichasaurus'' which occupies an intermediate position between ''Casea broilii'' and ''“Casea” rutena''. ''Ennatosaurus'' is identified as the sister group of a clade including ''Angelosaurus'' and the three species of ''Cotylorhynchus''. Within the latter genus, ''Cotylorhynchus romeri'' is the sister group of the two species ''C. hancocki'' and ''C. bransoni''.

Below is the cladogram of Caseasauria published by Benson in 2012.

In 2015, Marco Romano and Umberto Nicosia published the first cladistic study including almost all Caseidae (with the exception of '' Alierasaurus ronchii'' from Sardinia, then considered too fragmentary). This study again resolves the genus ''Casea'' as paraphyletic, with the species ''“Casea” nicholsi'' representing a distinct unnamed genus. In their most parsimonious analysis, '' Ruthenosaurus'' is closely related to ''Cotylorhynchus hancocki''. ''Ennatosaurus'' occupies a higher position than in previous analyses, and is identified as more closely related to '' Angelosaurus dolani''. However, the close relationship between ''A. dolani'' and ''Ennatosaurus'' may be biased by the extreme incompleteness of the material from the North American species.

Below is the cladogram of caseids published by Romano and Nicosia in 2015.

A phylogenetic analysis published in 2016 by Neil Brocklehurst and colleagues includes for the first time the genera '' Callibrachion'' and '' Datheosaurus'' which are identified as basal caseids occupying an intermediate position between ''Eocasea'' and ''Oromycter''.

Below is the phylogenetic analysis published by Neil Brocklehurst and colleagues in 2016.

In 2017 Romano and colleagues published the first phylogenetic analysis including the genus '' Alierasaurus''. The latter is recovered as the sister taxon of the genus ''Cotylorhynchus''.

Below is the phylogenetic analysis published by Romano and colleagues in 2017.

In describing the species '' Martensius bromackerensis'' in 2020, Berman and colleagues published two cladograms in which ''Martensius'' is identified as one of the most basal caseids, and is positioned just above the Late Carboniferous '' Eocasea martini''. In the first cladogram, the position of the remaining caseids is poorly resolved. In the second cladogram, ''Casea broilii'' is positioned above ''Martensius bromackerensis'', and is followed by a polytomy between '' Oromycter dolesorum'', '' Trichasaurus texensis'', and a clade of remaining caseid. Within these remaining taxa, a sequence of branching taxa begins with ''Casea nicholsi'', followed by '' Euromycter rutenus'', then '' Ennatosaurus tecton'', then '' Angelosaurus romeri'', then an apical clade of the three ''Cotylorhynchus'' species plus '' Alierasaurus ronchii''. In this final clade, ''Cotylorhynchus hancocki'' and ''C. bransoni'' are sister taxa and the clade forms a polytomy with ''C. romeri'' and ''Alierasaurus ronchii''.

Below are the two caseid cladograms published by Berman and colleagues in 2020.

In 2022, Werneburg and colleagues described the genus '' Lalieudorhynchus'' and published a phylogenetic analysis which concluded that the genera ''Angelosaurus'' and ''Cotylorhynchus'' are paraphyletic and are represented only by their type species. In this analysis, ''Cotylorhynchus romeri'' is positioned just above the genus ''Angelosaurus'', and forms a polytomy with a clade containing ''Ruthenosaurus'' and '' Caseopsis'' and another clade containing ''Alierasaurus'', the two other species of ''Cotylorhynchus'' and ''Lalieudorhynchus''. Within this latter clade, ''Alierasaurus'' is the sister group of ''“Cotylorhynchus” bransoni'' and a more derived clade including ''Lalieudorhynchus'' and ''“Cotylorhynchus” hancocki''.

Below is the cladogram published by Werneburg and colleagues in 2022.

Notes

References

External links

Tree of Life

{{Taxonbar, from=Q132725

Caseasauria
Prehistoric synapsid families
Taxa named by Samuel Wendell Williston