Procolophonoidea represent the most successful radiation of Parareptilia that lived during the Permo-Triassic. They are one of the few vertebrate groups that survived the end-Permian extinction and are thus important for studying the recovery of the post-extinction terrestrial ecosystem. Here, we investigate the palaeobiology of three Triassic procolophonid parareptiles, namely Sauropareion anoplus, Procolophon trigoniceps and Teratophon spinigenis, from the Karoo Basin of South Africa, inferred from histological analyses of their limb bones. Results reveal that all three taxa exhibit parallel-fibered bone tissue. Growth rings are absent in the Early Triassic Sauropareion and Procolophon whereas annuli are present in the Middle Triassic Teratophon, even during early ontogeny, suggesting a difference in life histories. Morphology and bone histology imply fossorial lifestyles for all three taxa, suggesting that burrowing may have played an important role in their survival during the harsh post-extinction Triassic environment.
Les Procolophonidea représentent la plus grande radiation évolutive des Parareptiles permo-triasiques. Ils composent l’un des quelques groupes de vertébrés ayant survécu à l’extinction de la fin du Permien et sont donc importants pour étudier la récupération de l’écosystème terrestre après la crise biologique. Dans cet article, nous examinons la paléobiologie de trois parareptiles procolophonides triasiques, plus particulièrement Sauropareion amoplus, Procolophon trigoniceps et Teratophon spinigenis du bassin du Karoo en Afrique du Sud, déduite de l’analyse histologique des os de leurs membres. Les résultats révèlent que les trois taxa montrent un tissu osseux à fibres parallèles. Les anneaux de croissance sont absents chez Sauropareion et Procolophon, du Trias inférieur, tandis qu’ils sont présents chez Teratophon, du Trias moyen, même dans les stades précoces de l’ontogenèse, ce qui indiquerait une différence dans leurs histoires de vie. La morphologie et l’histologie osseuse impliquent un style de vie fouisseur pour les trois taxons, ce qui suggère que le fouissage peut avoir joué un rôle important dans leur survie dans les conditions environnementales sévères après la crise permo-triasique.
Procolophonidae, Procolophonid, Bone histology, End-Permian extinction, South Africa, Karoo BasinProcolophonidae, Procolophonide, Histologie osseuse, Extinction permo-triasique, Afrique du Sud, Bassin du KaroopresentedPresented by Philippe TaquetIntroduction
Parareptiles were a diverse group of reptiles with a global distribution whose first appearance dates back to the Earliest Permian, some 297 Ma (million years ago) (Tsuji and Müller, 2009). As the sister group of Eureptilia, they are one of the few major amniote clades that survived the end-Permian extinction (Ruta et al., 2011). This event occurred 252.6 Ma (Mundil et al., 2004) and is considered to be the greatest mass extinction in Earth's history. Although parareptiles such as the aquatic mesosaurs, lizard-like millerettids and large herbivorous pareiasaurs went extinct during the Early to Late Permian, the Procolophonoidea were the only parareptiles to survive the end-Permian extinction (Botha et al., 2007 and Ruta et al., 2011).
Two families are usually recognized in the Procolophonoidea, namely Owenettidae and Procolophonidae (Modesto and Damiani, 2007). The latter group (Fig. 1) comprises small, lizard-like parareptiles, all of which (apart from the Russian procolophonid Suchonosaurus Säilä, 2009) lived during the Early and Middle Triassic (Cisneros, 2008). Although the taxonomy of Procolophonidae has received more attention in recent years, due to the discovery of several new species (e.g., Coletta seca, Gow, 2000; Sauropareion anoplus, Modesto and Damiani, 2007; Phonodus dutoitorum, Modesto et al., 2010), the palaeobiology of this group remains enigmatic.
Studying the microstructure of bone provides information about the biology of an animal (Enlow and Brown, 1957 and Enlow and Brown, 1958). This technique can be used to assess growth rates, individual longevity and changes during ontogeny, information that cannot necessarily be gained using more traditional methods such as morphometrics and comparative analysis. The Triassic procolophonid parareptiles are a particularly interesting group as they were not severely affected by the environmental changes that resulted in the end-Permian extinction (Modesto and Damiani, 2003 and Modesto et al., 2001). Consequently, understanding their biology may provide clues as to why this group was left relatively unscathed by the extinction event.
Material and methods
Three species of procolophonid parareptiles were examined, namely Sauropareionanoplus and Procolophon trigoniceps from the Lower Triassic Lystrosaurus Assemblage Zone, and Teratophon spinigenis from the Middle Triassic Cynognathus Assemblage Zone, all from the Karoo Basin of South Africa (Fig. 1; Table 1). We spent two field seasons collecting postcranial material of P.trigoniceps for the purpose of thin sectioning. As this species is by far (by orders of magnitude) the most abundant Triassic procolophonid in Karoo strata, we were able to collect 18 limb bones for bone histological analysis. This study material includes several limb bones from single individuals as well as homologous elements from numerous specimens, allowing us to consider inter-elemental and inter-individual variation. In addition, this relatively large sample size includes limb bones of varying ontogenetic status facilitating an assessment of histological changes through ontogeny (Table 1). In contrast, only five specimens of S.anoplus and 11 specimens of T.spinigenis have been positively identified. Thus, only a single individual of S.anoplus and two individuals of T.spinigenis were available for thin sectioning (Table 1). All specimens were positively identified using associated skull material, apart from SAM-PK-7711, NMQR 3565 and NMQR 3555. The latter two specimens are postcranial material collected from the Katberg Formation (middle Lystrosaurus Assemblage Zone). They are identified as P.trigoniceps and distinguished from S.anoplus by the similarity of the interclavicles to known Procolophon interclavicles and the particularly robust humerus with a prominent entepicondylar foramen. Specimen SAM-PK-7711 is a large, almost complete procolophonid skeleton with no skull. deBraga (2003) included this specimen in his description of the postcrania of P.trigoniceps. However, it was collected from the Aliwal North Quarry in the Middle Triassic Cynognathus Assemblage Zone, which is above the known stratigraphic range of Procolophon (Botha and Smith, 2006). As the specimen is large and robust, Cisneros (2008) tentatively assigned the specimen to T.spinigenis, the largest procolophonid known from the Cynognathus Assemblage Zone. However, as Modesto and Damiani (2003) noted, all positively identified procolophonid taxa from the Cynognathus Assemblage Zone are based solely on skull material. Thus, Cisneros (2008) could not use any characters to unequivocally identify specimen SAM-PK-7711 as T.spinigenis. Consequently, the assignment of SAM-PK-7711 to T.spinigenis must remain tentative until more positively identifiable postcranial material of T.spinigenis is recovered. Despite the problematic specific identification of SAM-PK-7711, the specimen represents the largest, best preserved procolophonid known from the Middle Triassic Cynognathus Assemblage Zone, and can thus, provide important information regarding the biology of procolophonids from this biozone.
Limb bones were selected for thin sectioning because they contain the least secondary remodelling in the midshaft regions and consequently exhibit the most complete growth record of the animal (Francillon-Vieillot et al., 1990 and Horner et al., 1999). The bones were measured and photographed before sectioning, and ontogenetic age was estimated for each element from dimensions of the largest known specimens of P.trigoniceps and T.spinigenis. The largest known specimen of S.anoplus is the holotype SAM-PK-11192 and was still actively growing at the time of death (determined from the open axial neurocentral suture and incomplete ossification of the distal end of the associated humerus; Modesto and Damiani, 2007 and Modesto et al., 2001). Thus, all known specimens of Sauropareion are considered to be juveniles. The thin sectioning was conducted at the National Museum, Bloemfontein, following procedures outlined by Chinsamy and Raath (1992) with some minor modifications. The bone microstructure was viewed and photographed using a Nikon Eclipse 50i Polarizing microscope and DS-Fi1 digital camera. Bone histology terminology follows that of Francillon-Vieillot et al. (1990) and Reid (1996).
As the organization and density of the vascular canals in cortical bone is closely related to bone apposition rate (e.g., Amprino, 1947 and de Margerie et al., 2002), the area occupied by these canals in a given bone section provides a quantitative method for comparing vascular density between different taxa. This quantification reflects the maximum possible vascularization for each element, as the channels would have contained lymph and nerves as well as blood vessels (Starck and Chinsamy, 2002). The total canal area was quantified using the image analysis program NIH ImageJ, which was then divided by the total cortical area and expressed as a percentage. The higher the vascular density, the more porous the bone.
The structure of the bone wall of an animal varies according to factors such as lifestyle, ontogeny and biomechanical demands (e.g., Canoville and Laurin, 2010, Cubo et al., 2005, Germain and Laurin, 2005, Kriloff et al., 2008 and Wall, 1983). For example, a particularly thick cortex may reflect an aquatic (e.g., de Buffrénil et al., 1990, Hua and de Buffrénil, 1996 and Wall, 1983) or fossorial (burrowing) lifestyle (e.g. Biknevicius, 1993, Botha, 2003 and Lagaria and Youlatos, 2006). In this study, we report the thickness of the bone wall by calculating the diaphyseal cortical thickness or “k” (Currey and Alexander, 1985), which is the ratio between the inner diameter and outer diameter of the bone. Cortical thickness is thinnest when k tends towards 1 (i.e. no bone walls), and thickest when k tends towards 0 (i.e. solid bone) (Currey and Alexander, 1985).
Bone compactness (defined as “the ratio between the surface occupied by bone tissues and the total bone surface”, Germain and Laurin, 2005:337) was also calculated using the computer program Bone Profiler for Windows (Girondot and Laurin, 2003). Among other things, this software calculates the ratio between the mineralized tissue surface and the total cross-sectional surface and reveals the global compactness of the bone (Canoville and Laurin, 2010, Germain and Laurin, 2005, Girondot and Laurin, 2003 and Laurin et al., 2004). Compactness is lower towards 0 and higher towards 1.
ResultsLystrosaurus Assemblage Zone ProcolophonidsSauropareion anoplus
All known Sauropareion specimens, including NMQR 3602, are similar in size and considered to be juveniles. A transverse section through the midshaft of the humerus of NMQR 3602 reveals poorly preserved bone tissue, where only a few regions are preserved well enough for analysis. The bone contains a moderately thick bone wall (k = 0.56) and a large, clear medullary cavity that is devoid of bony trabeculae (Fig. 2A). The bone tissue consists of uninterrupted parallel-fibered bone (defined as a bone matrix consisting mostly of mutually parallel collagenous fibers, sometimes flattened osteocyte lacunae and simple primary vascular canals and/or primary osteons, Francillon-Vieillot et al., 1990 and Reid, 1996), as seen by the mass birefringence (Fig. 2B), with flattened or oval osteocyte lacunae. The osteocyte lacunae are organized in parallel rows. Sparse, simple, longitudinally or radially-oriented vascular canals (Fig. 2C, D) are distributed randomly throughout the cortex (average diameter 24 μm). Although the vascularization for the whole cortex could not be quantified, one field of view revealed that the canals occupied 3.4% of the cortical area.
Procolophon trigoniceps
The 18 Procolophon limb bones were assigned size classes based on the length of their associated skulls in proportion to the maximum known skull length, which is 78 mm (BP/1/4248) and considered to be an adult (Cisneros, personal communication, 2011). The size classes comprise sub-adult (31–59% maximum size; size class II), late sub-adult (60–79% maximum size; size class III) and adult (80–100% maximum size; size class IV) (Botha-Brink and Angielczyk, 2010). None of the specimens in this study fell into the juvenile age class (0–30% maximum size; size class I).
Size class II
Specimens NMQR 3608 and NMQR 3588 are the smallest individuals examined in this study and are estimated to be 40% and 46% of the maximum known size for Procolophon, respectively. The humerus from NMQR 3608 and the tibia from NMQR 3588 both contain relatively thin cortices and large free medullary cavities (although cortical thickness could not be quantified in NMQR 3608 due to incomplete preservation). The osteocyte lacunae are preserved only in patches. They are abundant, globular and randomly distributed throughout the cortex in a parallel-fibered bone matrix. Vascularization is poor (NMQR 3588 = 3.4% cortical porosity) and consists of longitudinally-oriented simple vascular canals (average diameter 22 μm). Growth rings in the form of annuli (narrow translucent zones consisting of parallel-fibered bone or lamellar bone with sparse, flattened osteocyte lacunae and corresponding to periods of slow growth, Francillon-Vieillot et al., 1990) or Lines of Arrested Growth (LAG, cementing lines that correspond to temporary, but complete cessations in growth, Francillon-Vieillot et al., 1990) are absent. There is no evidence of any secondary remodelling and the medullary margin lacks any circumferential endosteal lamellae.
Five specimens range from 51% to 57% maximum size. The cortices of all the limb bones are moderately thick and bone compactness values range from 0.576 to 0.791 (Table 1). The overall bone tissue consists of poorly vascularized (2.7% in tibia NMQR 3591) to relatively highly vascularized (6.7% in femur NMQR 3944b and 10.6% in femur NMQR 3555b) parallel-fibered bone (Fig. 3A–C). The osteocyte lacunae vary from flattened to globular in shape (Fig. 3D). They are highly abundant and randomly distributed in regions of the femora and humeri (Fig. 3E), but are also organized in parallel rows in some regions of the femora (Fig. 3C) and humeri and in most of the cortex in the radii, ulnae and tibiae. The vascular canals are mostly longitudinally-oriented simple canals (average diameter 25 μm), but form a reticular organization in the femora (average diameter 44 μm) and extend radially from the medullary cavity in the radii and tibiae. A few poorly-defined primary osteons are present in the humerus and femur of NMQR 3555, where they also become radially-oriented in the humerus. The primary osteons average 55 μm in diameter. Secondary osteons and growth rings were not observed in any of the limb bones. A thin layer of circumferential endosteal lamellae was observed in the perimedullary region of humerus NMQR 3944a (51% maximum size) and the humerus and femur of individual NMQR 3555 (57% maximum size). Sharpey's fibers (indicating regions of muscle insertions) were observed in the humeri, ulnae (Fig. 3F) and tibiae in the regions of the deltopectoral, ulnar and cnemial crests, respectively.
Size class III
Three specimens, namely NMQR 3945, SAM-PK-K10727 and NMQR 3622, are 62%, 73% and 77% of the maximum size respectively, and are thus classified as late sub-adults. The cortices of the bones in all specimens are moderately thick (k = 0.44 to 0.66; Table 1) and the medullary cavities are large and free of trabecular infilling. The bone tissue of all elements contains abundant, globular or flattened osteocyte lacunae in a parallel-fibered bone matrix (Fig. 4A–F). The vascular canals vary between longitudinally-oriented simple canals with short anastomoses (average diameter 17.6 μm) and radiating vascular canals (Fig. 4A–C, E). There is a clear decrease in the number of vascular canals towards the periphery of humerus NMQR 3622 (Fig. 4E). This region also shows a decrease in the number of osteocyte lacunae. Growth rings are absent in all elements and secondary remodelling was only observed in the ulna in the form of a few large resorption cavities in the perimedullary region. Sharpey's fibers were also observed in this element.
Size class IV
One radius in this study (NMQR 3676) was classified as 82% maximum size (Table 1). It is poorly preserved and incomplete, and only the proximal region could be thin sectioned. A relatively thin cortex reveals a poorly organized parallel-fibered bone tissue with numerous longitudinally and radially-oriented simple canals (cortical porosity 6.7%; average diameter 24 μm) (Fig. 4F). The medullary cavity is completely free of trabeculae and growth rings are absent.
Inter-elemental histovariation in Procolophon
Differences in vascular orientation and density were observed between the various Procolophon limb bones. The humeri and femora are more vascularized than the epipodial elements (radius, ulna, tibia). The femora contain a mixture of relatively large longitudinally and radially-oriented vascular canals as well as those in a reticular organization. In contrast the humeri, radii, the ulna and larger tibia contain primarily radially-oriented vascular canals (Fig. 5). The simple vascular canals observed in the radii, ulna and tibia are relatively smaller than those in the humeri and femora. Primary osteons, which are closely linked with rapid bone deposition rates (de Margerie et al., 2002), were observed in the propodial elements, but are absent from the epipodials. As vascularization is closely related to growth rates (Amprino, 1947 and de Margerie et al., 2002), the presence of primary osteons as well as the overall higher vascular density implies a relatively higher rate of bone deposition in the propodials than in the epipodials.
Cynognathus Assemblage Zone Procolophonids
SAM-PK-K10183 is a radius taken from a positively identified (associated with skull) specimen of T.spinigenis. The bone is approximately 55% of the maximum known size for this taxon. The cortex is notably thick (k = 0.32) and compact (C = 0.896), and the medullary cavity only contains one or two trabeculae. The bone tissue consists of a well-defined parallel-fibered bone matrix (Fig. 6A, B). The osteocyte lacunae are flattened and highly abundant. Vascularization is poor (2.5%) and consists of some longitudinally-oriented simple canals (average diameter 17 μm), but mostly radially-oriented canals that reach the periphery, giving the bone an uneven subperiosteal surface. A few primary and secondary osteons were observed in the inner cortex, and several large resorption cavities are present in the perimedullary region. A thin layer of circumferential endosteal lamellar bone was also observed. A few faint lines consisting of an increased abundance of osteocyte lacunae traverse the mid-cortex, suggesting some type of variation in growth rate. They do not appear to be annuli or LAG as the localized increased number of osteocytes suggests a temporary increase in growth rate. Prominent and abundant Sharpey's fibers were observed throughout the cortex (Fig. 6B).
The humerus and tibia of SAM-PK-7711, which have been tentatively assigned to T.spinigenis, revealed thick cortices (Table 1) surrounding mostly free medullary cavities. Some bony trabeculae traversed a portion of the medullary cavity in the tibial midshaft. The bone compactness values in the humerus and tibia are 0.834 and 0.833 respectively. Both humeral and tibial inner cortices (Fig. 6C–F) contain parallel-fibered bone tissue with relatively highly vascularized tissues with simple vascular canals (average diameter 36.3 μm in the humerus and 23.7 μm in the tibia), a few poorly developed primary osteons (average diameter 99 μm) and in the tibia, several small secondary osteons as well. Short anastomoses result in a reticular organization in the inner and mid-cortex of the humerus (Fig. 6C), whereas the tibia contains predominantly radially-oriented vascular canals. The inner bone tissue is interrupted by widely spaced annuli, but the annuli increase in number and become very closely spaced in the outer cortex in both elements (Fig. 6C, F). The vascular canals also decrease in size towards the periphery (average diameter 13 μm). Eight annuli were counted in the humerus, whereas only three annuli could be distinguished in the tibia prior to the onset of multiple, closely spaced annuli. Enlarged erosion cavities are present in the endosteal margins of both elements, but are more numerous in the tibia. Thin layers of inner circumferential lamellae surround the medullary cavities of both elements.
Inter-elemental histovariation in <italic>Cynognathus</italic> Assemblage Zone Procolophonids
The humerus of SAM-PK-7711 contains the highest vascularization amongst the Cynognathus Assemblage Zone elements. However, both the humerus and tibia of SAM-PK-7711 are notably more vascularized than the radius of SAM-PK-K10183 (Fig. 7). The vascular orientation also differs, where a reticular organization was observed in the inner and mid-cortex of the humerus, the canals radiate out from the medullary cavity in the tibia, and they are mostly longitudinally-oriented in the radius. The lower vascularization in the radius implies a slower overall growth rate for this element, compared to the humerus and tibia.
DiscussionTriassic procolophonid palaeobiology
The sparse simple vascular canals, absence of primary osteons and presence of highly organized osteocyte lacunae in the bone tissues of S.anoplus suggests that it grew more slowly than Procolophon or Teratophon, whose bone tissues exhibit more highly vascularized parallel-fibered bone. However, the juvenile status of the Sauropareion specimen NMQR 3602 complicates an assessment of the overall growth patterns of this taxon as a later growth spurt cannot be ruled out (as seen in Procolophon). It is possible that the slow growth observed in Sauropareion was affected by its small body size because within a given clade, smaller animals grow more slowly than their larger relatives (Case, 1978 and Padian et al., 2004). However, as fully adult individuals of Sauropareion have yet to be recovered, the maximum size of this taxon is currently unknown. Thus, more material is required before we can confirm that the slow growth observed in Sauropareion is related to small body size.
The bone tissues of P.trigoniceps revealed initial slow growth early in ontogeny, indicated by the presence of sparse simple vascular canals. However, the growth rate increased in the sub-adults where an increase in vascularization was observed. All the elements studied are characterized by uninterrupted parallel-fibered bone. The bone tissue becomes more organized and vascularization decreases towards the subperiosteal surface in the ontogenetically older elements. However, annuli and LAG are absent from all individuals studied. Annuli and LAG, or growth rings, reflect endogenous biological rhythms that are reinforced by external factors (Castanet and Baez, 1991). They correspond to temporary cessations in growth (Francillon et al., 1990) and experiments on extant animals have shown them to be seasonal (Hutton, 1986). Thus, the absence of growth rings in Procolophon suggests that this taxon either reached adult size within one year or its growth rate was not affected by seasonal variation. The largest known skull of Procolophon is 78 mm in length and corresponds to a snout-vent length of 500 mm (Cisneros, personal communication, 2011). Small extant squamates such as agamids, chamaeleonids and gymnophthalmids (maximum snout-vent length 100 mm) generally reach sexual maturity within one year (Castanet, 1994, Dunham et al., 1988 and James, 1991), whereas larger squamates such as Varanus niloticus (snout-vent length 1 m) usually reach sexual maturity after two years (Enge et al., 2004). The maximum known length of Procolophon falls between these ranges and although it may not reflect the maximum possible size of the genus, it can be considered an adult (based on morphology, Cisneros, personal communication, 2011). The bone tissues of Procolophon are notably more vascularized compared to those of extant squamates, indicating relatively higher growth rates (Amprino, 1947 and de Margerie et al., 2002). Thus, although maximum size was probably not achieved within one year, it is possible that sexual maturity was achieved within this time frame. Sexual maturity has been shown to be associated with a dramatic change to a slowly forming bone tissue in extant taxa (e.g., amphibians and reptiles; Castanet and Baez, 1991 and Castanet and Smirina, 1990; walrus Odobenus rosmarus, Klevezal, 1996) and possibly extinct taxa as well (non-avian dinosaurs, Reid, 1996, Sander, 2000; non-mammaliaform cynodont therapsids, Botha and Chinsamy, 2005 and Botha-Brink and Angielczyk, 2010). The clear increased organization of the osteocyte lacunae into parallel rows accompanied by a dramatic decrease in vascularization in the outer cortex of humerus NMQR 3622a (approximately 77% of the maximum known size) suggests that sexual maturity had been reached because growth had decreased dramatically. Thus, if Procolophon exhibited growth rings at all, it would have been particularly late in ontogeny (and after the onset of sexual maturity).
The bone tissues of the Middle Triassic procolophonid Teratophodon spinigenis in this study differ from those of the Early Triassic. Although the radius of SAM-PK-K10183 revealed poorly vascularized parallel-fibered bone, the tibia and humerus of SAM-PK-7711 revealed inner cortices of highly vascularized (9% average inner cortical porosity) parallel-fibered bone tissue with radially-oriented vascular canals in the tibia and a reticular vascular arrangement in the humerus. Annuli were observed traversing the inner and mid-cortex, indicating that growth was intermittent. The bone tissue becomes poorly vascularized and multiple, closely spaced annuli appear towards the subperiosteal surface in both elements, suggesting that sexual maturity had been reached in this individual. The presence of annuli in the inner cortex prior to sexual maturity however, suggests that the growth of Teratophon was intermittent, even during early ontogeny. The presence of at least three annuli in SAM-PK-7711 for example, indicates that it took at least three years for this individual to reach sexual maturity. This pattern differs from that seen in Procolophon where growth rings are absent throughout ontogeny (even after sexual maturity had been reached).
The two larger procolophonid taxa (Procolophon and Teratophon) exhibit tissues that are fairly distinct from those of other reptiles. The bone tissues of Sauropareion are comparable with similar-sized extant squamates as well as the Permian diapsids Youngina and Captorhinus (personal observation, 2010). These animals contain poorly vascularized or avascular simple lamellar or parallel-fibered bone (de Ricqlès, 1976, Enlow and Brown, 1957 and Laurin et al., 2011). However, it must be noted that all known specimens of Sauropareion are considered to be juveniles, and future recovery of more mature individuals will provide additional information on the overall growth patterns of this taxon. In contrast, the bone tissues of Procolophon and Teratophon differ from those of extant reptiles, in that the inner and mid-cortices of some elements are notably more vascularized (up to 10% cortical porosity) than even large Varanus species and crocodilians where juvenile cortical porosity only reaches 4.6% (1.6–1.9% in adults) (Chinsamy, 1993 and de Buffrénil et al., 2008). The reticular vascular organization observed in the Procolophon femora and Teratophon humerus is also highly unusual in reptiles and is usually only found in extinct archosaurs that exhibit fibro-lamellar bone (some basal archosauromorphs and non-avian dinosaurs, Botha-Brink and Smith, 2011 and de Ricqlès et al., 2008). Living crocodilians tend to exhibit poorly vascularized parallel-fibered or lamellar-zonal bone and the vascular orientation is predominantly longitudinal (Lee, 2004) even in juveniles less than one year old that exhibit fibro-lamellar bone (Horner et al., 2001). Few parareptiles have been subjected to bone histological analysis and thus, it is difficult to compare these procolophonids with other members of the group. De Ricqlès (1976) examined the limb bones of adult Pareiasaurus and more recently Scheyer and Sander (2009) studied the osteoderms of three pareiasaur species, namely Pareiasaurus, Bradysaurus and Anthodon. Both studies found poorly vascularized slowly forming lamellar-zonal bone tissues in these taxa. The vascular organization in the bone tissues of juvenile non-procolophonid parareptiles is not currently known, but hopefully, future research on these animals will confirm whether Procolophon and Teratophon can be distinguished from other medium to large Permian parareptiles (cf. Canoville and Chinsamy, 2011). It is possible that other small parareptiles (e.g. Australothyris, Millerettidae, other procolophonoids), most of which are similar in size to known individuals of Sauropareion (maximum known skull length 40 mm), exhibit relatively poorly vascularized parallel-fibered bone tissues, similar to this taxon. Simple poorly vascularized tissues are seen in numerous small extant animals such as lizards, moles, bats and the rhynchocephalian Sphenodon (Cubo et al., 2005, Enlow and Brown, 1957, Enlow and Brown, 1958 and Laurin et al., 2011). However, it should also be noted that recent studies have found vascular density to be more closely correlated with phylogeny or growth rate rather than body size (Cubo et al., 2005 and de Buffrénil et al., 2008).
Triassic procolophonid palaeoecology
Sauropareion does not have any distinct postcranial adaptations for limb-based digging such as a short humerus, which is shorter in length than the femur, an elongated acromion process on the scapula or an elongated olecranon process on the ulna (Hildebrand, 1985 and Kley and Kearney, 2007). However, it does have several features, such as a prominent spade-shaped skull, relatively large unguals (40% longer than the penultimate phalanges) and short, robust non-terminal phalanges (that would rigidify the manus and pes against forces incurred during digging), which suggests that it may have used head-assisted, fore- and hind limb scratch-digging (MacDougall et al., in press). Furthermore, the proportion of the epicondylar width to the total length of the humerus is 0.48, which falls within the range for scratch-diggers (which range from 0.2 to 0.7) and is well above that of most non-fossorial animals (≤ 0.2) (Hildebrand, 1985). The humerus of the juvenile Sauropareion individual examined in this study has a moderately thick cortex (k = 0.56), indicating that the propodials of this genus were relatively robust (compared to many extant iquanid lizards, which have thinner humeral cortices, average k = 0.68; Laurin et al., 2011). Thus, we support the proposal that Sauropareion may have been a scratch-digger that used its spade-shaped skull to aid in moving and packing soil, as has been observed in extant mammals such as moles and mole-rats (Hildebrand, 1985 and Wake, 1993).
Numerous studies have suggested that Procolophon was a burrower (e.g., Botha-Brink and Modesto, 2007, deBraga, 2003, Groenewald, 1991 and Miller et al., 2001) and there are several morphological characteristics of the skull and skeleton to support such a lifestyle. For example, deBraga (2003) noted that the short, triangular-shaped skull, concave, spade-shaped dorsal skull surface, distinct overbite (possibly to reduce ingestion of dirt), robust limb bones and large, broad unguals would have been useful for digging. Procolophon also has relatively short epipodials and a broad rib cage, features that are frequently observed in digging animals (Hildebrand, 1974), and the epicondylar width to humeral length ratio is 0.53, well within the range of scratch-diggers (Hildebrand, 1985). Furthermore, it is common for numerous Procolophon fossils to be collected in close association (e.g. “Procolophon hill” locality of Kitching, 1977) and some specimens have even been recovered from interpreted burrow casts (Groenewald, 1991). The humerus of Procolophon has a relatively thick cortex (average k = 0.49) and is thicker than many iguanid lizards (Laurin et al., 2011) including the large burrowing desert monitor Varanus griseus (k = 0.5072), which averages 1 m in snout-vent length. Thick cortices, which aid in countering large compressive stresses, have also been found in several extant digging mammals such as insectivores and rodents (Biknevicius, 1993 and Bou et al., 1990). Thus, the combined observations in taphonomic style, functional morphology and bone microstructure (moderately thick cortex and prominent Sharpey's fibers indicating the need for strong muscle insertions, which would be necessary for a demanding activity such as digging) supports previous suggestions that Procolophon was capable of burrowing and may have excavated burrows using both the head and forelimbs.
Several burrow casts have also been found in association with Teratophon specimens in the Cynognathus Assemblage Zone (personal observation, 2003). Teratophon has a particularly thick cortex in all the elements studied (average k = 0.3). The limb bones are thicker than the burrowing rodent Ctenomys (k = 0.5, Biknevicius, 1993), as well as many extant iguanid, anguid and teiid lizards, and is most similar to the burrowing V.griseus (k = 0.3) and marine iguana, Amblyrhynchus cristatus (k = 0.38), both of which have notably thick cortices (Laurin et al., 2011). The epicondylar width to humeral length ratio is 0.48, which is comparable to the pangolin (Hildebrand, 1985), which is fossorial. The morphology of Teratophon, which includes large, robust limbs and unguals, short robust non-terminal phalanges, and thickened cortices suggest that it was capable of digging the burrows found in association with it, and may also have been semi-fossorial (i.e. an animal that has some skeletal adaptations for digging, but not extreme morphological specializations; Dunn and Rasmussen, 2007), similar to Sauropareion and Procolophon. Moreover, individuals of Sauropareion, Procolophon and Teratophon tend to be found in groups (Kitching, 1977; personal observation, 2011). For example, three of the five known Sauropareion specimens were found within a few meters of one another. These accumulations are emphasized in Teratophon and particularly in Procolophon, which are often found grouped together in high abundance to form monospecific aggregations (Kitching, 1977). Burrowing has been suggested for other procolophonids as well, such as Hypsognathus fenneri (Sues et al., 2000), Koiloskiosaurus coburgensis (Botha-Brink and Modesto, 2007) and Leptopleuron lacertinum (Säilä, 2010). Most living reptiles are capable diggers, even those lacking skeletal modifications for digging (deBraga, 2003 and Voorhies, 1975). Thus the overall trend of increased robustness in procolophonids together with the various morphological and histological modifications in these taxa suggests that a fossorial lifestyle was a general behavioral trait in the Procolophonidae (deBraga, 2003).
Triassic procolophonids and the end-Permian extinction event
Although it has yet to be confirmed in Sauropareion (due to the lack of confirmed adult material), the absence of growth rings in Procolophon is noteworthy. Extant reptiles exhibit periodic decreases or cessations in growth during the unfavorable season (Peabody, 1961) and as the climate of the Early Triassic South African Karoo Basin was strongly seasonal (Smith and Botha, 2005), it is expected that Procolophon would have exhibited such growth rings. However, they are absent. In contrast, Teratophon grew intermittently, even during early ontogeny, similar to extant and most extinct reptiles. This suggests a difference in life history between Early and Middle Triassic South African procolophonids. The relatively high vascularization during early growth in Procolophon and Middle Triassic procolophonids, which is higher than that of extant reptiles, also suggests relatively rapid early growth as vascularization is closely related to growth rate (de Margerie et al., 2002), albeit in a parallel-fibered matrix, which represents slower growth rates than fibro-lamellar bone.
Burrowing has been shown to lower the extinction risk in extant mammals by providing a temporary refuge against predators and unexpected environmental changes (Liow et al., 2009). This behavior has also been proposed as a survival strategy for numerous Early Triassic vertebrates (e.g. the dicynodont Lystrosaurus, non-mammaliaform cynodonts, therocephalians) as a means of escaping the unpredictable environmental conditions of that time (Bordy et al., 2011, Botha and Smith, 2006 and Smith and Botha-Brink, 2009). The Early Triassic is characterized by extreme temperatures, aridity and unpredictable rainfall (Botha and Smith, 2006, Roopnarine et al., 2007 and Smith and Ward, 2001), but procolophonoids appear to have been relatively unaffected by the end-Permian extinction (Botha et al., 2007, Modesto et al., 2001 and Modesto et al., 2003). They are the only parareptile group that crossed the Permo-Triassic boundary and then radiated extensively during the Early Triassic. It is possible that early relatively rapid growth (compared to other non-archosaurian reptiles), constant growth rate (i.e. little susceptibility to seasonal fluctuations) and/or fossorial behavior were advantageous in the post-extinction environment, allowing Procolophon to become the most widespread and abundant parareptile of the Early Triassic.
Acknowledgments
Thank you to the National Museum, Bloemfontein and Iziko South African Museums for the loan of material. We thank J. Nyaphuli, J. Mohoi and N. Nthaopa of the National Museum, Bloemfontein for the mechanical preparation of the study material. Michel Laurin, Kevin Padian and two anonymous reviewers are kindly acknowledged for their helpful comments on an earlier draft of this manuscript. This project was funded by a joint research grant from the National Research Foundation of South Africa to J.B.B. and R.M.H.S. (UID65241).
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Phylogeny of Procolophonidae. Taxa examined in this study are in bold. Phylogeny taken from Cisneros (2008) and Tsuji and Müller (2009). Abbreviation: E: Eumetabolodon.
Phylogénie des Procolophonidae. Les taxa examiné dans cette étude sont en gras. La phylogénie est proposée d’après Cisneros (2008) et Tsuji et Müller (2009). Abréviation : E : Eumetabolodon.
Bone histology of Sauropareion anoplus, NMQR 3602. A. Transverse section of the humerus through the midshaft region showing a highly organized bone tissue with sparse vascular canals (arrows). B. Transverse section in polarized light showing parallel-fibered bone tissue. C. High magnification showing simple vascular canals. D. High magnification in polarized light with Lambda compensator, showing a parallel-fibered bone matrix. Abbreviation: mc: medullary cavity. Scale bars 100 μm.
Histologie osseuse de Sauropareion anoplus, NMQR. A. Section transversale de l’humérus à travers la région axiale montrant un tissu osseux très bien organisé avec des canaux vasculaires épars (flèches). B. Section transversale en lumière polarisée montrant un tissu osseux à fibres parallèles. C. Fort grossissement montrant des canaux vasculaires simples. D. Fort grossissement en lumière polarisée avec compensateur Lambda, montrant une matrice osseuse à fibres parallèles. Abréviation : mc : cavité médullaire. Barre d’échelle, 100 μm.
Bone histology of Procolophon trigoniceps. A. Femur of NMQR 3944b showing numerous large vascular canals. B. Femur of NMQR 3944b in polarized light with Lambda compensator, showing parallel-fibered bone. C. Femur of NMQR 3555b in polarized light with Lambda compensator showing numerous large vascular canals and highly organized osteocyte lacunae in parallel-fibered bone. D. Humerus of NMQR 3565a showing a mixture of oval (left) and flattened (right) osteocyte lacunae. E. Humerus of NMQR 3944a showing highly abundant randomly distributed osteocyte lacunae. F. Tibia of NMQR 3944c showing parallel-fibered bone and Sharpey's fibers (box). Abbreviation: mc: medullary cavity. Scale bars 100 μm.
Histologie osseuse de Procolophon trigoniceps. A. Fémur de NMQR 3944b montrant de nombreux grands canaux vasculaires. B. Fémur de NMQR 3944b en lumière polarisée avec compensateur Lambda, montrant que l’os est constitué, qu’il est constitué d’os à fibres parallèles. C. Fémur de NMQR 3555b en lumière polarisée avec compensateur lambda montrant de nombreux grands canaux vasculaires et des lacunes d’ostéocyte très bien organisées dans l’os à fibres parallèles. D. Humérus de NMQR 3565a montrant un mélange de lacunes d’ostéocyte ovales (à gauche) et aplaties (à droite). E. Humérus de NMQR 3944a montrant de très nombreuses lacunes ostéocytaire distribués au hasard. F. Tibia de NMQR 3944c montrant un os à fibres parallèles et des fibres de Sharpey (dans le carré blanc). Abréviation : mc : cavité médullaire. Barre d’échelle 100 μm.
Bone histology of Procolophon trigoniceps. A. Radius of SAM-PK-K10727b showing parallel-fibered bone with simple radial canals. B. Ulna of SAM-PK-K10727c showing radial simple canals in a poorly vascularized bone tissue. C. Ulna of SAM-PK-K10727c in polarized light with Lambda compensator showing parallel-fibered bone and an increase in osteocyte lacunae organization at the bone periphery (arrow). D. Ulna of SAM-PK-K10727c in polarized light showing parallel-fibered bone. E. Humerus of NMQR 3622a showing numerous radially-oriented vascular canals (white arrows) in the inner cortex and increased organization in the osteocyte lacunae with a dramatic decrease in vascularization (black arrow) in the outer cortex. F. Radius of NMQR 3676 showing relatively large vascular canals in parallel-fibered bone tissue. Abbreviation: mc: medullary cavity. Scale bars 100 μm, apart from (B) 500 μm.
Histologie osseuse de Procolophon trigoniceps. A. Radius de SAM-PK-K 10727b montrant un os à fibres parallèles avec de simples canaux radiaux. B. Ulna de SAM-PK-K 10727c montrant de simples canaux radiaux dans un tissu osseux faiblement vascularisé. C. Ulna de SAM-PK-K 10727c en lumière polarisée avec un compensateur lambda montrant un os à fibres parallèles et un accroissement dans l’organisation des lacunes d’ostéocyte à la périphérie de l’os (flèche). D. Ulna de SAM-PK-K 10727c en lumière polarisée montrant un os à fibres parallèles. E. Humérus de NMQR 3622a montrant de nombreux canaux vasculaires orientés radicalement (flèches blanches) dans le cortex interne et augmentation de l’organisation dans les lacunes d’ostéocyte avec diminution très importante de la vascularisation dans le cortex externe. F. Radius de NMQR 3676 montrant des canaux vasculaires relativement grands dans un tissu osseux à fibres parallèles. Abréviation : mc : cavité médullaire. Barres d’échelle 100 μm, sauf pour (B) 500 μm.
Diaphyseal cross-sections of Procolophon trigoniceps limb bones from ontogenetically youngest (left) to ontogenetically oldest (right). Note the radiating vascular canals in the ulna and larger humeri and radii, as well as the high reticular vascularization in the femora. Percentages indicate percentage maximum size. Scale bar 1 mm.
Coupes transversales diaphysaires dans des os de membre de Procolophon trigoniceps du plus jeune (à gauche) au plus vieux (à droite) ontogénétiquement parlant. À noter les canaux vasculaires rayonnants dans l’ulna et dans les grands humérus et radius, ainsi que la vascularisation hautement réticulée dans les fémurs. Les pourcentages sont ceux de la taille maximum. Barre d’échelle 1 mm.
Bone histology of Teratophon spinigenis and specimen SAM-PK-7711. A. Radius of SAM-PK-K10183 showing a poorly vascularized thick cortex with mostly radiating simple canals. Arrows indicate a change in bone tissue deposition rate. B. Radius of SAM-PK-K10183 in polarized light with Lambda compensator showing parallel-fibered bone and abundant osteocyte lacunae. Numerous Sharpey's fibers are also visible (box). Arrows indicate a change in bone tissue deposition rate. C. Humerus of SAM-PK-7711a taken slightly below the midshaft (hence the presence of bony trabeculae within the medullary cavity) showing highly vascularized inner bone tissue with a sub-reticular vascular arrangement and a poorly vascularized outer bone tissue with radiating simple vascular canals. Arrows indicate annuli. D. High magnification of humerus SAM-PK-7711a in polarized light with Lambda compensator taken at the midshaft showing highly vascularized parallel-fibered bone in the inner cortex. E. High magnification of humerus SAM-PK-7711a in polarized light taken at the midshaft showing parallel-fibered bone. F. Tibia of SAM-PK-7711b showing a radiating network of vascular canals and a prominence of annuli in the outer tissue. White arrows indicate annuli and black arrow indicates endosteal bone lining the medullary cavity. Abbreviations: mc: medullary cavity. Scale bars: (A, C, F) 500 μm; (B, D, E) 100 μm.
Histologie osseuse de Teratophon spinigenis et spécimen SAM-PK-7711. A. Radius de SAM-PK-K 10183 montrant un épais cortex faiblement vascularisé avec de simples canaux dont la plupart sont rayonnants. Les flèches indiquent un changement dans la vitesse de dépôt du tissu osseux. B. Radius de SAM-PK-K 10183 en lumière polarisée avec compensateur Lambda montrant un os à fibres parallèles et d’abondantes lacunes d’ostéocyte. De nombreuses fibres de Sharpey sont aussi visibles (rectangle blanc). Les flèches indiquent un changement dans la vitesse de dépôt du tissu osseux. C. Humérus de SAM-PK-7711a pris légèrement au-dessous de la mi-hauteur de l’axe (d’où la présence de travées osseuses au sein de la cavité médullaire) montrant un tissu osseux très vascularisé, avec un arrangement vasculaire sub-réticulé et un tissu osseux externe faiblement vascularisé, à simples canaux vasculaires rayonnants. Les flèches indiquent des anneaux. D. Fort grossissement d’humérus SAM-PK-7711a en lumière polarisée avec compensateur lambda pris à mi-hauteur de l’axe, montrant un os à fibres parallèles très bien vascularisés dans le cortex interne. E. Fort grossissement de l’humérus SAM-PK-K 77 11a en lumière polarisée, pris à mi-hauteur de l’axe montrant un os à fibres parallèles. F. Tibia de SAM-PK 7711b montrant un réseau rayonnant de canaux vasculaires et une proéminence d’anneaux dans le tissu externe. Les flèches blanches indiquent les anneaux et la flèche noire indique un os endostéen soulignant la cavité médullaire. Abréviations : mc : cavité médullaire. Barres d’échelle (A, C, F) 500 μm ; (B, D, E) 100 μm.
Diaphyseal cross-sections of Teratophon spinigenis limb bones from the radius of SAM-PK-10183, and the humerus and tibia of SAM-PK-7711 (tentative assignment). Note the high vascularization in the inner cortices of the humerus and tibia and radiating vascular canals in the outer cortices. Percentages indicate percentage maximum size. Scale bar 1 mm.
Coupes diaphysaires d’os de membre de Teratophon spinigenis, provenant de radius de SAM-PK-10183, d’humérus et de tibia de SAM-PK-7711 (identification incertaine). À noter la vascularisation importante des cortex internes d’humérus et de tibia et les canaux vasculaires rayonnants dans les cortex externes. Barre d’échelle 1 mm.
Specimens thin sectioned in this study. The percentage maximum size was estimated using the largest known specimens for each genus. Sauropareion anoplus and Procolophon trigoniceps are from the Lower Triassic Lystrosaurus Assemblage Zone and Teratophon spinigenis is from the Middle Triassic Cynognathus Assemblage Zone, all from the South African Karoo Basin. “k” refers to the ratio between the internal and external diameter of the bone (Currey and Alexander, 1985) and “C” refers to the global bone compactness (Girondot and Laurin, 2003), i.e. the ratio between mineralised bone surface and section (including the medullary area). Measurements are in millimeters.
Spécimens étudiés en lame mince. La taille maximum en pourcentage a été estimée en utilisant les plus grands spécimens connus pour chaque genre. Sauropareion anoplus et Procolophon trigoniceps proviennent de la zone d’assemblage du Trias inférieur à Lystrosaurus et Teratophon spinigenis est issu de la zone d’assemblage du Trias moyen à Cynognathus, tous du bassin du Karoo, en Afrique du Sud. « k » correspond au rapport entre diamètre interne et externe de l’os (Currey et Alexander, 1985) et « C » à la compacité globale de l’os (3), i.e. le rapport entre la surface et la section de l’os minéralisé (incluant la zone médullaire). Les mesures sont en millimètres. Comm. : Commonage ; Mbg : Middleburg District ; Rville : Rouxville District.