Biological aspects of the Permian dicynodont Oudenodon (Therapsida: Dicynodontia) deduced from bone histology and cross-sectional geometry Jennifer Botha South African Museum, Iziko Museums of Cape Town, P.O. Box 61, Cape Town, 8000 South Africa. E-mail: jbotha@iziko.org.za Received 2 June 2003. Accepted 3 December 2003 INTRODUCTION The Dicynodontia are recognized as the most successful herbivorous therapsid group of the Late Permian (King 1990). They radiated into several, varied ecological niches and became the most numerous herbivorous tetrapods by the end of this period (Hotton 1986; King 1990). As a result of the highly varied and widespread nature of this group, the dicynodonts have received much attention in the literature, both systematically and morphologically (e.g. Angielczyk 2001; Cluver & Hotton 1983; Cluver & King 1983; Hotton 1986; Keyser 1975; Keyser & Cruickshank 1979; Rubidge & Sidor 2001). The focus of previous studies has been on cranial descriptions, locomotory modifica- tions and masticatory systems (e.g. Cluver 1971; Cluver & Hotton 1983; Cluver & King 1983; Cox 1998; Kemp 1982; Keyser 1975; King 1996; King et al. 1989), while other bio- logical traits, such as growth patterns and lifestyle habits, have been less extensively studied. A few studies, such as those of Chinsamy & Rubidge (1993), Enlow and Brown (1957) and Ricqlès (1972, 1976, 1991), have used bone histology to deduce the growth patterns of several dicynodont genera. However, these studies were not comprehensive examinations and thus provided limited information. In addition, only one type of element was usually examined, making it difficult to deduce generic patterns of growth. The lifestyle habits of a few dicynodonts such as Lystrosaurus (Brink 1951; Broom 1903; Groenewald 1991; King 1991; King & Cluver 1991), Cistecephalus (Cluver 1978) and Diictodon (Ray & Chinsamy 2003; Smith 1987) have been examined using burrow casts and functional anatomy to suggest specific modes of life. Oudenodon was a medium-sized dicynodont (skull length from 100–300 mm) whose skeletal remains have been excavated from Late Permian deposits in South Africa (Cluver & Hotton 1983). The morphology of the skull has been described in detail (Broom 1912; Cluver & Hotton 1983; Cluver & King 1983; Keyser 1975; Owen 1860) and distinctive features include a lack of teeth in both the upper and lower jaws, a deep and relatively narrow secondary palate, a sharp maxillary crest behind the caniniform process, the absence of maxillary tusks and narrow dentary tables on the dentaries (Cluver & Hotton 1983; Cluver & King 1983). Although the cranial morphology of Oudenodon (Cluver & Hotton 1983; Cluver & King 1983; Keyser 1975;) and to a lesser extent the postcranial skeleton (Broom 1901), have been examined, little pertaining to the biology of this genus has been discussed. Thus, there is inadequate infor- mation regarding the growth patterns and lifestyle habits of Oudenodon for deducing its overall biology. Bone histology is a well-established technique for exam- ining growth patterns and lifestyle habits of extinct animals (e.g. Enlow & Brown 1957; Reid 1996; Ricqlès 1976, 1980). The bone histology of Oudenodon has previ- ously been described by Ricqlès (1972) and Chinsamy & Rubidge (1993). Ricqlès (1972) examined a humerus and a femur, whereas Chinsamy & Rubidge (1993) used a humerus to interpret the growth patterns of Oudenodon. Although informative, both descriptions were brief and neither study considered inter-elemental histovariability. Although, Ricqlès (1972) examined a humerus and a femur, histological variation between the two elements was not discussed. It is becoming increasingly evident that inter-elemental histovariability should be considered when deducing the overall growth patterns of a genus (Botha 2002; Curry 1999; Horner et al. 1999, 2000; Starck & Chinsamy 2002; Ray et al., in press). A technique known as bone cross-sectional geometry can be used in conjunction with bone histology analysis to ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 37 Bone histology and cross-sectional geometry were used to examine the growth patterns and lifestyle habits of the Late Permian dicynodont, Oudenodon. Several limb bones were analysed, revealing rapidly deposited fibro-lamellar bone, interrupted by annuli or sometimes Lines of Arrested Growth. Peripheral slowly deposited parallel-fibred bone was observed in several elements. It is suggested that the initial growth of Oudenodon was rapid during the favourable growing season, but decreased or sometimes ceased completely during the unfavourable season. Growth was cyclical and may have been sensitive to environmental fluctuations. The slowly forming parallel-fibred bone towards the sub-periosteal surface in several elements indicates a permanent transition to slow growth and may reflect the onset of sexual maturity. Bone cross-sectional geometry results reveal a markedly thick cortex, indicating a possible modifica- tion for digging. These cross-sectional geometry values, in conjunction with the limb morphology, suggest that Oudenodon was fossorial. Keywords: Therapsida, Oudenodon, bone histology, growth patterns. provide information regarding an animal’s lifestyle. Studies have shown that a direct relationship exists between an animal’s lifestyle and the structural design of its bones (Bou et al. 1990; Fish 1993; Stein 1989; Wall 1983). For example, fossorial animals have thick, relatively short limb bones with a high force moment of their forelimb muscles for digging (Bou et al. 1990; Casinos et al. 1993). Equally, the bones of sirenians, cetaceans, crocodilians and certain aquatic birds have extremely high bone densi- ties to counteract buoyancy (Buffrénil et al. 1990; Hua & Buffrénil 1996). Osteological modifications of an extinct animal can therefore provide valuable information for determining the type of habitat an animal occupied. In a study conducted by Wall (1983), who examined the cortical thickness (bone wall) of 49 mammalian genera, it was found that most of the aquatic mammals studied had a significantly higher limb bone density than that of the terrestrial mammals. He proposed that if the compact bone wall exceeds 30% of the average diameter, the animal is aquatic or at least semi-aquatic, possibly as an adapta- tion to counteract buoyancy (Wall 1983). Magwene (1993) studied the bone cross-sectional geom- etry of several crocodilian, lizard, non-mammalian therapsid and mammalian femora and found that, on average, non-mammalian therapsids and mammals have thinner bone walls compared to crocodilians and lizards. He argued that non-mammalian therapsids and mammals have lighter bones as a weight-saving modifica- tion because they are subject to greater bending and torsional stresses due to their higher activity levels. In contrast, crocodilian and lizard limb bones are more robust and stiff as they have less active lifestyles (Magwene 1993). Magwene examined each group collec- tively, but when the results are examined according to life- style, 75% of the semi-aquatic crocodilians and lizards and all of the arboreal/fossorial lizards studied had a cortical thickness of more than 30%. Similarly, 38% of the fossorial/arboreal mammals had a cortical thickness that exceeded 30%, while several of the other fossorial mam- mals had a cortical thickness that was at least 28%. Thus, Wall’s ‘30%’ threshold appears adequate for indicating the approximate minimum cortical thickness required for aquatic lifestyles, as well as for fossorial or arboreal life- styles. Thus, bone cross-sectional geometry can be used to provide further information regarding the lifestyle habits of Oudenodon. MATERIALS AND METHODS The Oudenodon study elements, which were positively identified from associated cranial material, include sev- eral limb bones (humerus, femora, tibiae, fibulae). All specimens were recovered from the Dicynodon Assem- blage Zone, Balfour/Teekloof Formation, Beaufort Group of South Africa (Rubidge 1995). Limb bones were selected as they are the most readily preserved compared to other elements and they show the least secondary remodeling in the midshaft region (Francillon-Vieillot et al. 1990). Limb bones therefore provide the best record of the type of growth exhibited by the animal. Several different types of limb bones were included to ensure that inter-elemental histovariability was considered. The elements are from different individ- uals and represent various ontogenetic stages. Owing to their large size (approximate range between 90 and 160 mm in length) it is unlikely that any of the study elements represent juvenile individuals, they probably all represent subadult or adult individuals. Most of the limb bones were transversely sectioned in the midshaft region. Proximal or distal regions were also sectioned where possible, depending on the particular element (Table 1). Each region of bone to be sectioned was embedded in the clear resin, Impset 21, to prevent the bone from disintegrating during the process. Once the resin had set, the area to be sectioned was cut using a Blanes diamond-tipped saw. The cut surface was polished until smooth using a Logitech LP50 lapping machine and then mounted onto a petrographic glass slide using the resin adhesive, Epotek. Pressure was then applied to the sections to eliminate any bubbles. A thin section, approxi- mately 35 µm thick, was then cut using a Logitech CS10 cut-off diamond-tipped saw. The resulting thin sections were polished until smooth with the Logitech LP50 lapping machine and examined using a Leitz Laborlux K compound microscope. The bone histology was photo- graphed using a Nikon FinePix S1 Pro digital camera. Thin sections were also used to measure the cortical thickness of the midshaft region of each bone. The cortical thickness was measured in microns at four equidistant radial positions using an eyepiece micrometer in the Leitz Laborlux K compound microscope at ×40 magnification. The mean of these four measurements was divided by the mean bone diameter and the final value expressed as a percentage. 38 ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 Table 1. Oudenodon specimens used in this study and their localities. All specimens were recovered from the Dicynodon Assemblage Zone, Teekloof Formation, Beaufort Group of South Africa. SAM-PK-K refers to South African Museum, Iziko Museums of Cape Town, South Africa. SAM-PK-K4807 and SAM-PK-10019 consist of several disarticulated elements representing several individuals. Locality Specimen number Skeletal element Region sectioned Richmond SAM-PK-K4807a Femur Midshaft, proximal SAM-PK-K4807b Femur Midshaft, proximal SAM-PK-K4807c Femur Proximal SAM-PK-K4807d Fibula Midshaft, proximal SAM-PK-10019a Femur Midshaft, proximal SAM-PK-10019b Tibia Proximal SAM-PK-10019c Fibula Midshaft, proximal SAM-PK-10019d Humerus Distal Murraysburg SAM-PK-11141 Femur Distal midshaft RESULTS Bone histology A comprehensive analysis of the bone histology of the Oudenodon postcrania revealed moderately vascula- rized fibro-lamellar bone tissue, becoming parallel-fibred towards the periphery in some cases. Interruptions by annuli of lamellar bone or Lines of Arrested Growth (LAGs) were noted throughout the cortex in all elements. Some variation was noted between the different types of elements and will be described in detail below. Femur. (SAM-PK-11141, SAM-PK-K4807a, SAM-PK- K4807b, SAM-PK-K4807c, SAM-PK-10019a). The femora contain small medullary cavities, which are surrounded by notably thick cortices. The primary bone tissue is fibro-lamellar bone with longitudinally oriented primary osteons (Fig. 1A), but a laminar network is present in SAM-PK K4807b and SAM-PK-10019a (Fig. 1B). Annuli of lamellar bone or LAGs interrupt the fibro-lamellar bone at intervals. The globular osteocyte lacunae in the fibro- lamellar bone become flattened in the annuli. They have branched canaliculi, which radiate out in all direc- tions. Vascularization is generally moderate, decreasing towards the periphery in femora SAM-PK-11141, SAM-PK-K4807a and SAM-PK-K4807c where the overall bone tissue organization becomes parallel-fibred bone (Fig. 1C). In these regions of parallel-fibred bone, the sparse vascular canals become simple and the annuli are sometimes multiple (i.e. several annuli clustered together). Secondary remodeling with numerous second- ary osteons is observed surrounding the medullary cavity of femur SAM-PK-K4807b (Fig. 1D). Sharpey’s fibres are observed in femur SAM-PK-K4807a (Fig. 1E). Tibia. (SAM-PK-10019b). The tibia consists of a markedly thick cortex and a free medullary cavity is absent. Trabe- culae, lined with endosteal lamellar bone, fill the entire medullary cavity. The primary tissue consists of highly vascularized fibro-lamellar bone, which is interrupted by annuli (Fig. 2). Large, longitudinally oriented primary osteons, which form a laminar network in places, decrease in diameter towards the sub-periosteal surface. Fibula. (SAM-PK-10019c, SAM-PK-K4807d). The medul- lary cavities are completely filled with bony trabeculae (Fig. 3A). Secondary remodeling, with large resorption cavities is extensive. The moderately vascularized fibro- lamellar bone tissue contains distinct annuli of lamellar bone tissue, but becomes poorly vascularized parallel- fibred bone at the periphery of SAM-PK-10019c (Fig. 3B). Longitudinally oriented primary osteons in the fibro- lamellar bone are replaced by small, simple vascular canals that are sparsely distributed in the parallel-fibred region. Distinct Sharpey’s fibres are noted in SAM-PK- 10019c (Fig. 3B) and SAM-PK-K4807d. Humerus. (SAM-PK-10019d). The bone tissue consists of fibro-lamellar bone interrupted by annuli, similar to the rest of the study elements (Fig. 4). LAGs are absent. The tissue is highly vascularized near the medullary cavity, but becomes moderately vascularized towards the sub-periosteal surface. Longitudinal primary osteons characterize the fibro-lamellar bone. Secondary remodel- ing is extensive and a free medullary cavity is absent, which may be due to the section being taken from a more distal region compared to the other elements. Bone cross-sectional geometry The femur SAM-PK-K4807a has a cortical thickness of 46% and the cortical thickness of both femora SAM-PK- K4807b and SAM-PK-10019a is 39%. A mid-diaphyseal region was not available for femur SAM-PK-K4807c. Although midshaft regions of the fibulae were available for study, the medullary cavities were completely filled with bony trabeculae, making it impossible to discern a distinct transition between trabeculae and compact bone. Thus, the midshaft cortical thickness of these elements was not measured. Similarly, a free medullary cavity was absent from tibia SAM-PK-10019b. The cortical thickness of the humerus SAM-PK-10019d was not measured as a midshaft region was unavailable. DISCUSSION Bone histology Histological examination of the bones revealed rapidly deposited fibro-lamellar bone, indicating rapid growth. The primary bone tissue organization varied from lami- nar to longitudinally oriented primary osteons. Annuli of lamellar bone or LAGs were observed interrupting the fibro-lamellar bone, which indicates that growth slowed down or even ceased periodically. These observations agree with the findings of Ricqlès (1972) and Chinsamy & Rubidge (1993), although Ricqlès did not refer to any annuli or LAGs in the humerus. Ricqlès (1972) noted that the humerus used in his study was highly vascularized, which may indicate that this element was from a juvenile individual and growth may have been too rapid to exhibit growth rings. Although the overall bone tissue pattern observed in this study agrees with the findings of Ricqlès (1972) and Chinsamy & Rubidge (1993) there are some variations not previously noted. The most marked and significant varia- tion is the presence of slowly forming parallel-fibred bone at the periphery of several femora (SAM-PK-11141, SAM- PK-K4807a, SAM-PK-K4807c) and a fibula (SAM-PK- 10019c). This bone tissue indicates a marked decrease in overall growth and represents a permanent transforma- tion to slow growth. Ricqlès (1972) did not note parallel- fibred bone in his examination of the femur. A transition from rapidly to slowly forming bone tissue has been re- ported in the non-mammalian cynodonts Procynosuchus (Ray et al., in press) and Thrinaxodon (Botha & Chinsamy, in press). Such a feature has been documented in extant animals as well and it is suggested that this transition represents the onset of sexual maturity (Castanet & Baez 1991; Reid 1996; Sander 2000; Botha & Chinsamy, in press; Ray et al., in press). The parallel-fibred bone in Oudenodon may represent the onset of sexual maturity whereby growth continued after sexual maturity was reached, but at a much slower rate. It is suggested from the bone histology that femora SAM-PK-11141, SAM-PK-K4807a and SAM-PK-K4807c ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 39 represent adult individuals, whereas femora SAM-PK- K4807b and SAM-PK-10019a represent subadult individu- als. Parallel-fibred bone is absent from the latter two femora and although the vascularization is moderate, there is no decrease in vascular density towards the periphery, thus indicating continued active growth at the time of death. The moderate vascularization and abun- dant secondary osteons suggest that these two femora do not represent juvenile individuals, but the absence of peripheral, slowly forming parallel-fibred bone indicates that overall growth had not yet begun to slow down. The highly vascularized primary tissue with abundant primary osteons and absence of parallel-fibred bone in tibia SAM-PK-10019b suggests that this element is repre- sentative of an early subadult. The fibulae exhibit exten- sive secondary remodeling and are moderately vascula- rized. Fibula SAM-PK-10019c exhibits peripheral paral- lel-fibred bone, indicating that the overall growth rate had begun to slow down. These characteristics suggest that this element represents an adult individual. As paral- lel-fibred bone is absent from fibula SAM-PK-K4807d, it is probably a subadult. There is a slight decrease in 40 ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 Figure 1. Bone histology of the Oudenodon femora. A, SAM-PK-K4807c, showing fibro-lamellar bone with longitudinally oriented primary osteons, interrupted by multiple annuli and LAGs (arrowheads). Parallel-fibred bone occurs at the periphery. Scale bar = 636 µm. B, SAM-PK-10019a, showing fibro-lamellar bone in a laminar network. Scale bar = 636 µm. C, SAM-PK-K4807a, showing fibro-lamellar bone becoming poorly vascularized parallel-fibred bone towards the sub-periosteal surface (arrow). Scale bar = 610 µm. D, SAM-PK-K4807b, showing secondary osteons in the peri- medullary area (arrowheads). E, SAM-PK-K4807a, showing Sharpey’s fibres. Scale bar =635 µm. vascularization towards the sub-periosteal surface in humerus SAM-PK-10019d, but LAGs and parallel-fibred bone are absent. The presence of annuli and absence of LAGs indicates that growth slowed down periodically, but did not cease. These characteristics suggest that the humerus represents a subadult. Sharpey’s fibres were observed in several of the femora and fibulae. Chinsamy & Rubidge (1993) also noted Sharpey’s fibres in the Oudenodon humerus in their study. It is possible that the bones of Oudenodon had an unusually large proportion of Sharpey’s fibres. As Sharpey’s fibres represent areas of muscle insertion (Leeson & Leeson 1981), it is possible that Oudenodon had well-developed muscles to cope with digging. However, Chinsamy & Rubidge (1993) also noted Sharpey’s fibres in all the dicynodont humeri in their study. Thus, it is also possible that distinct Sharpey’s fibres are a common feature of dicynodont bone histology and most dicynodonts may have had particularly well-developed musculature to cope with their semi-erect posture. Such prominent Sharpey’s fibres have not yet been noted in non-mamma- lian cynodonts (Botha 2002) or gorgonopsians and therocephalians (Ray et al., in press). It is also possible that the larger dicynodonts in Chinsamy & Rubidge’s (1993) study had substantial muscles and thus distinct Sharpey’s fibres to cope with their large size. More studies on dicynodont bone histology, including multiple element analyses, are required to deduce whether this is the case. Inter-elemental histovariability It is becoming increasingly apparent, particularly from more recent studies including different types of elements, that inter-elemental histovariability has a significant effect on interpreting generic patterns of growth (Botha 2002; Curry 1999; Horner et al. 1999, 2000; Starck & Chinsamy 2002; Ray et al., in press). It is therefore essential to include several different types of elements in a bone histological study, although it is recognized that this may prove diffi- cult at times when fossil preservation is poor. Although the overall bone tissue organization is similar between the different types of Oudenodon elements in this study, some inter-elemental histological variation was noted. For example, parallel-fibred bone was not ob- served in the humerus SAM-PK-10019d, but a midshaft region was not available for study and only the distal metaphyseal region could be examined. It is possible that the midshaft region, which would have exhibited more primary tissue, contained parallel-fibred bone. This is unlikely however, as the parallel-fibred bone occurs at the periphery, a region which could be observed in the humerus. Furthermore, Ricqlès (1972) did not document ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 41 Figure 2. Oudenodon tibia SAM-PK-10019b, showing highly vascularized fibro-lamellar bone alternating with annuli of lamellar bone (arrow- heads). Scale bar = 454 µm. Figure 3. Bone tissue patterns of the Oudenodon fibulae. A, SAM-PK- 10019c, fibro-lamellar bone with longitudinally oriented primary osteons, becoming parallel-fibred bone with simple vascular canals towards the periphery. Scale bar = 434 µm. B, High magnification, show- ing prominent Sharpey’s fibres. Scale bar = 163 µm. Figure 4. Bone histology of the Oudenodon humerus SAM-PK-10019d, showing high vascularization in the inner and mid cortex, which de- creases slightly at the sub-periosteal surface. Two annuli (arrowheads) can be seen interrupting the fibro-lamellar bone. Scale bar = 515 µm. any parallel-fibred bone in the Oudenodon humerus in his study, neither was it noted in the study conducted by Chinsamy & Rubidge (1993). It is possible that both these elements as well as the humerus in this study were ontogenetically too young and thus depositing bone too fast to exhibit slowly forming parallel-fibred bone tissue. It is also possible that this may be an example of differential rates of bone growth between the various limb bones of a skeleton. It was noted in previous studies on non- mammalian cynodonts that proximal limb bones (i.e. humerus, femur) grew more quickly than distal limb bones (radius, ulna, tibia, fibula) (Botha 2002; Ray et al., in press). Distal limb bones were less vascularized and annuli and/or LAGs were more numerous and distinct compared to those in the proximal limb bones. These characteristics indicate that the distal limb bones were growing more slowly than the proximal limb bones. Similarly, Starck & Chinsamy (2002), in a study on extant Japanese quail (Coturnix japonica), found that the mid- diaphyseal regions of the humerus and femur increased in cross-sectional thickness faster than the radius, ulna or tarsometatarsus. The humerus of Oudenodon may be the last limb bone within an individual to exhibit paral- lel-fibred bone. Bone cross-sectional geometry Based on a specimen found in a terminal burrow, previ- ous studies have suggested that Oudenodon was fossorial. However, the suggestion was made on the basis of a juve- nile specimen that had been recovered from a burrow at the base of the Tropidostoma Assemblage Zone, Teekloof Formation, Beaufort Group, South Africa (Smith 1987). The identification of this juvenile specimen is uncertain and Oudenodon is as yet, unknown from the Tropidostoma Assemblage Zone. The bone cross-sectional geometry results in this study reveal a relatively thick cortex and may indicate a fossorial lifestyle. All the femoral cortical thickness values exceed 30%. Although the cortical thickness of the tibia and fibu- lae could not be quantified, the profusion of bony trabeculae within the medullary cavities would have provided extra strength and support to these elements. When comparing these results with other non-mamma- lian therapsids, Oudenodon exhibits a notably thick bone wall (Table 2). Few cortical thickness values have been documented in the literature, which makes comparison difficult, but it can be seen from Table 2 that the cortical thickness of the Oudenodon femora is notably higher than that of the Pristerognathus (Ray et al., in press) or Aeluro- gnathus (Magwene 1993) femora. Although only ulna and radial values are available for the gorgonopsian Scylacops, neither value exceeds 30%. These results indicate that Oudenodon exhibits a particularly thick bone wall, possibly for a specific mode of life. If these results are examined in conjunction with the morphological modifications described by Broom (1901), they suggest that Oudenodon was fossorial. Broom (1901) described the postcranial skeleton of Oudenodon and it appears to exhibit modifica- tions for a digging or fossorial lifestyle. The robust humerus has a well-developed delto-pectoral crest, the olecranon process on the ulna is greatly elongated and the radius and ulna are distally flattened. Furthermore, the broad, flat manus forms a large, flattened surface area and the phalanges end in large, distinct claws (Broom 1901). These morphological characteristics are typical of an animal that digs or burrows (Bargo et al. 2000; Yalden 1966). A positively identified specimen in a burrow com- plex could confirm this suggestion. Implications for Oudenodon biology The alternating bone tissue organization between rapidly deposited fibro-lamellar bone and slowly depos- ited lamellar bone within the annuli indicates that the growth of Oudenodon was cyclical. This bone tissue pattern is similar to those of Dicynodon, Aulacephalodon, Endothiodon, Cistecephalus and Kannemeyeria (Chinsamy & Rubidge 1993) as well as Diictodon (Ray & Chinsamy, in press). Experiments have revealed that seasonal fluctua- tions cause cyclical growth in extant reptiles (e.g. Castanet et al. 1993; Hutton 1986) and it is suggested that the cyclical growth patterns observed in these dicynodonts is due to a sensitivity to environmental fluctuations (Chinsamy & Rubidge 1993; Ray & Chinsamy, in press). As Oudenodon experienced a semi-arid climate with seasonal rainfall (Smith et al. 1993), it is possible that growth was influ- enced by seasonal fluctuations whereby the growth rate decreased or ceased during the unfavourable growing season. If Oudenodon was in fact fossorial, it may have 42 ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 Table 2. Cortical thickness of the Oudenodon elements compared with other non-mammalian therapsids (represented as a percentage). Scylacops and Pristerognathus values were taken from Ray et al. (in press) and the Aelurognathus value was taken from Magwene (1993). Note that the Pristerognathus and Aelurognathus femora have a markedly lower cortical thickness compared to the Oudenodon femora. Scylacops, Pristerognathus and Aelurognathus were designated as adults (Magwene 1993; Ray et al., in press). Genus Specimen number Skeletal element Cortical thickness (%) Oudenodon SAM-PK-10019a Femur 39 SAM-PK-K4807a Femur 45 SAM-PK-K4807b Femur 39 Scylacops SAM-PK-10188 Ulna 16 Radius 24 Pristerognathus SAM-PK-1157 Radius 18 Femur 15 Tibia 25 Fibula 25 Aelurognathus Femur 21 burrowed to escape harsh environmental conditions. However, the peripheral parallel-fibred bone has not been noted previously in any dicynodont genus. Either this feature is unique to Oudenodon or it is generally found only in certain types of elements and will be revealed in other dicynodonts in future studies. It is also possible that previous studies have not examined elements that have been ontogenetically old enough to exhibit slowly form- ing parallel-fibred bone. Peripheral rest lines were not observed in any of the Oudenodon study elements, which suggests that growth continued throughout life, but at a much slower rate once sexual maturity was reached. Thank you to Dr R. Smith of the South African Museum, Iziko Museums of Cape Town, for the loan of the study specimens. Mr Dave Wilson of the Geology Depart- ment, University of Cape Town, is acknowledged for preparing the thin sections and Mr Neville Eden of the Zoology Department, University of Cape Town, is thanked for his technical assistance with the photography. Thank you to Dr Alain Renaut of the Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, Johannesburg, and an anonymous reviewer for reviewing this manuscript. This research was supported by a post-doctoral fellowship grant from the National Research Foundation, South Africa GUN 2061695. REFERENCES ANGIELCZYK, K.D. 2001. Preliminary phylogenetic analysis and strati- graphic congruence of the dicynodont anomodonts (Synapsida: Therapsida). Palaeontologia africana 37, 53–79. BOTHA, J. 2002. The palaeobiology of the non-mammalian cynodonts deduced from bone microstructure and stables isotopes. Unpublished PhD thesis, University of Cape Town, Cape Town. BOTHA, J. & CHINSAMY, A. In press. Growth patterns of Thrinaxodon, a non-mammalian cynodont from the Early Triassic of South Africa. Palaeontology. BARGO, M.S., VIZCAÍNO, S.F., ARCHUBY, F.M. & BLANCO, R.E. 2000. Limb bone proportions, strength and digging in some Lujanian (Late Pleistocene-Early Holocene) mylodontid ground sloths (Mammalia, Xenarthra). Journal of Vertebrate Paleontology 20(3), 601–610. BOU, J., CASTIELLA, M.J., OCANA, J. & CASINOS, A. 1990. Multivariate analysis and locomotor morphology in insectivores and rodents. Zoologischer Anzeiger 225, 287–294. BRINK, A.S. 1951. On the genus Lystrosaurus Cope. Transactions of the Royal Society of South Africa 33, 107–120. BROOM, R. 1901. On the structure and affinities of Oudenodon. Proceed- ings of the Zoological Society, London 2, 162–190. BROOM, R. 1903. On the Structure of the shoulder girdle in Lystrosaurus. Annals of the South African Museum 4, 139–141. BROOM, R. 1912. On some new fossil reptiles from the Permian and Triassic beds of South Africa. Proceedings of the Zoological Society, London 1912, 859–876. BUFFRÉNIL, V., RICQLÈS, A. DE, RAY, C.E. & DOMNING, D.P. 1990. Bone histology of the ribs of the archaeocetes (Mammalia: Cetacea). Journal of Vertebrate Paleontology 10, 455–466. CASINOS, A., QUINTANA, C. & VILADIU, C. 1993. Allometry and adap- tation in the long bones of a digging group of rodents (Ctenomyinae). Zoological Journal of the Linnean Society 107, 107–115. CASTANET, J. & BAEZ, M. 1991. Adaptation and evolution in Gallotia lizards from the Canary Islands: age, growth, maturity and longevity. Amphibia-Reptilia 12, 81–102. CASTANET , J., VIEILLOT, H.F., MEUNIER, F. J. & RICQLÈS, A. DE. 1993. Bone and individual aging. Bone (bone growth). Bone 7, 245–283. CHINSAMY, A. & RUBIDGE, B.S. 1993. Dicynodont (Therapsida) bone histology: phylogenetic and physiological implications. Palaeontologia africana 30, 97–102. CLUVER, M.A. 1971. The cranial morphology of the dicynodont genus Lystrosaurus. Annals of the South African Museum 56(5), 155–274. CLUVER, M.A. 1978. The skeleton of the mammal-like reptile Cistecephalus with evidence for a fossorial mode of life. Annals of the South African Museum 76(5), 213–246. CLUVER, M.A. & HOTTON, N. 1983. The genera Dicynodon and Diictodon and their bearing on the classification of the Dicynodontia (Reptilia, Therapsida). Annals of the South African Museum 83(6), 99–146. CLUVER, M.A. & KING, G.M. 1983. A reassessment of the relationships of Permian Dicynodontia (Reptilia, Therapsida) and a new classifica- tion of dicynodonts. Annals of the South African Museum 91(3), 195–273. COX, C.B. 1998. The jaw function and adaptive radiation of the dicynodont mammal-like reptiles of the Karoo Basin of South Africa. Zoological Journal of the Linnean Society 122, 349–384. CURRY, K.A. 1999. Ontogenetic histology of Apatosaurus (Dinosauria: Sauropoda): new insights on growth rates and longevity. Journal of Vertebrate Paleontology 19(4), 654–665. ENLOW, D.H. & BROWN, S.O. 1957. A comparative histological study of fossil and recent bone tissues. Part II. The Texas Journal of Science 9, 136–214. FISH, F.E. 1993. Comparison of swimming kinematics between terrestrial and semiaquatic opossums. Journal of Mammalogy 74(2), 275–284. FRANCILLON-VIEILLOT, H., BUFFRÉNIL, V., CASTANET, J., GERAUDIE, J., MEUNIER, F.J., SIRE, J.Y., ZYLBERBERG, L. & RICQLÈS, A. DE. 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter, J.G. (ed.), Skeletal Biomineralization: patterns, Processes and Evolutionary Trends, 471–548. New York, Van Nostrand Reinhold. GROENEWALD, G.H. 1991. Burrow casts from the Lystrosaurus-Proco- lophon Assemblage-zone, Karoo Sequence, South Africa. Koedoe 34(1), 13–22. HORNER, J.R, RICQLÈS, A. DE & PADIAN, K. 1999. Variation in dino- saur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25, 295–304. HORNER, J.R., RICQLÈS, A. DE & PADIAN, K. 2000. Long bone histol- ogy of the hadrosaurid dinosaur Maiasaura peeblesorum: growth dynamics and physiology of an ontogenetic series of skeletal ele- ments. Journal of Vertebrate Paleontology 20, 115–129. HOTTON, N. 1986. Dicynodonts and their role as primary consumers. In: Hotton, N., Maclean, P.D., Roth, J.J. & Roth, E.C. (eds), The Ecology and Biology of Mammal-Like Reptiles, 71–82. Washington, Smithsonian Institution Press. HUA, S. & BUFFRÉNIL, V. DE. 1996. Bone histology as a clue in the inter- pretation of functional adaptations in the Thalattosuchia (Reptilia, Crocodylia). Journal of Vertebrate Paleontology 16, 703–717. HUTTON, J. M. 1986. Age determination of living Nile crocodiles from the cortical stratification of bone. Copeia 2: 332–341. KEMP, T.S. 1982. Mammal-like Reptiles and the Origin of Mammals. London, Academic Press. KEYSER, A.W. 1975. A re-evaluation of the cranial morphology and systematics of some tuskless Anomodontia. Memoires of the Geological Survey Republic of South Africa 67, 1–110. KEYSER, A.W. & CRUICKSHANK, A.R.I. 1979. The origins and classifica- tion of Triassic dicynodonts. Transactions of the Geological Society of South Africa 82, 81–108. KING, G.M. 1990. Life and Death in the Permo-Triassic: The Fortunes of the Dicynodont Mammal-like reptiles. Cape Town, South African Museum. KING, G.M. 1991. The aquatic Lystrosaurus: a palaeontological myth. Historical Biology 4(4), 285–322. KING, G.M. & CLUVER, M.A. 1991. The aquatic Lystrosaurus: an alterna- tive lifestyle. Historical Biology 4(4), 323–342. KING, G.M., OELOFSEN, B.W. & RUBIDGE, B.S. 1989. The evolution of the dicynodont feeding system. Zoological Journal of the Linnean Society 96, 185–211. KING, G.M. 1996. Reptiles and herbivory. London, Chapman and Hall. LEESON, T.S. & LEESON, C.R. 1981. Histology. London, W.B. Saunders. MAGWENE, P.M. 1993. What’s bred in the bone: histology and cross-sectional geometry of mammal-like reptile long bones-evidence of changing physiologi- cal and biomechanical demands. Unpublished MSc thesis, Harvard Uni- versity, Cambridge. OWEN, R. 1860. On some reptilian fossils from South Africa. Quarterly Journal of the Geological Society, London 16, 49–63. RAY, S. & CHINSAMY, A. 2003. Functional aspects of the postcranial anatomy of the Permian dicynodont Diictodon and their ecological implications. Palaeontology 46, 151–183. RAY, S., BOTHA, J. & CHINSAMY, A. In press. Bone histology and growth patterns of some nonmammalian therapsids. Journal of Verte- brate Paleontology. RAY, S. & CHINSAMY, A. In press. Diictodon feliceps (Therapsida, Dicynodontia): bone histology, growth and biomechanics. Journal of Vertebrate Paleontology. REID, R.E.H. 1996. Bone histology of the Cleveland-Lloyd dinosaurs and of dinosaurs in general, Part I: Introduction: Introduction to bone tissues. Geology Studies 41, 25–71. RICQLÈS, A. DE. 1972. Recherches paléohistologiques sur les os longs des tétrapodes III. – Titanosuchiens, Dinocéphales et Dicynodontes. Annales de Paléontologie 58, 1–60. RICQLÈS, A. DE. 1976. On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. In: Bellairs, A. D’a & Cox, C.B. (eds), Morphology and biology of reptiles, 123–150. London, Academic Press. ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44 43 RICQLÈS, A. DE. 1980. Tissue structures of dinosaur bone. Functional significance and possible relation to dinosaur physiology. In: Thomas, D.K. & Olson, E.C. (eds), A Cold Look at the Warm-blooded Dinosaurs, 103–139. Boulder, Westview Press. RICQLÈS, A. DE., MEUNIER, F.J., CASTANET, J. & FRANCILLON- VIEILLOT, H. 1991. Comparative microstructure of bone. In: Hall, B.K. (ed.), Bone Matrix and Bone Specific Products, 1–77. Boca Raton, CRC Press. RUBIDGE, B.S. (ed.). 1995. Biostratigraphy of the Beaufort Group (Karoo Supergroup). Pretoria, South African Committee for Stratigraphy, Biostratigraphic Series No. 1, 1–46. RUBIDGE, B.S. & SIDOR, C.A. 2001. Evolutionary patterns among Permo-Triassic therapsids. Annual Review of Ecology and Systematics 32, 449–480. SANDER, M.A. 2000. Longbone histology of the Tendaguru sauropods: implications for growth and biology. Paleobiology 26(3), 466–488. SMITH, R.M.H. 1987. Helical burrow casts of therapsid origin from the Beaufort Group (Permian) of South Africa. Palaeogeography, Palaeo- climatology, Palaeoecology 60, 155–170. SMITH, R.M.H., ERIKSSON, P. G. & BOTHA, W. J. 1993. A review of the stratigraphy and sedimentary environments of the Karoo-aged basins of southern Africa. Journal of African Earth Sciences 16: 143–169. STARCK, J.M. & CHINSAMY, A. 2002. Bone microstructure and develop- mental plasticity in birds and other dinosaurs. Journal of Morphology 254, 232–246. STEIN, B.R. 1989. Bone density and adaptation in semi-aquatic mammals. Journal of Mammalogy 70(3), 467–476. WALL, W.P. 1983. The correlation between limb-bone density and aquatic habits in recent mammals. Journal of Vertebrate Paleontology 57, 197–207. YALDEN, D.W. 1966. The anatomy of mole locomotion. Journal of Zoology 149, 55–64. 44 ISSN 0078-8554 Palaeont. afr. (December 2003) 39: 37–44