Evidence from South Africa for a protracted end-Permian extinction on land.

Earth's largest biotic crisis occurred during the Permo-Triassic Transition (PTT). On land, this event witnessed a turnover from synapsid- to archosauromorph-dominated assemblages and a restructuring of terrestrial ecosystems. However, understanding extinction patterns has been limited by a lack of high-precision fossil occurrence data to resolve events on submillion-year timescales. We analyzed a unique database of 588 fossil tetrapod specimens from South Africa's Karoo Basin, spanning ∼4 My, and 13 stratigraphic bin intervals averaging 300,000 y each. Using sample-standardized methods, we characterized faunal assemblage dynamics during the PTT. High regional extinction rates occurred through a protracted interval of ∼1 Ma, initially co-occurring with low origination rates. This resulted in declining diversity up to the acme of extinction near the Daptocephalus-Lystrosaurus declivis Assemblage Zone boundary. Regional origination rates increased abruptly above this boundary, co-occurring with high extinction rates to drive rapid turnover and an assemblage of short-lived species symptomatic of ecosystem instability. The "disaster taxon" Lystrosaurus shows a long-term trend of increasing abundance initiated in the latest Permian. Lystrosaurus comprised 54% of all specimens by the onset of mass extinction and 70% in the extinction aftermath. This early Lystrosaurus abundance suggests its expansion was facilitated by environmental changes rather than by ecological opportunity following the extinctions of other species as commonly assumed for disaster taxa. Our findings conservatively place the Karoo extinction interval closer in time, but not coeval with, the more rapid marine event and reveal key differences between the PTT extinctions on land and in the oceans.

Extreme growth plasticity in the early branching sauropodomorph Massospondylus carinatus.

There is growing evidence of developmental plasticity in early branching dinosaurs and their outgroups. This is reflected in disparate patterns of morphological and histological change during ontogeny. In fossils, only the osteohistological assessment of annual lines of arrested growth (LAGs) can reveal the pace of skeletal growth. Some later branching non-bird dinosaur species appear to have followed an asymptotic growth pattern, with declining growth rates at increasing ontogenetic ages. By contrast, the early branching sauropodomorph Plateosaurus trossingensis appears to have had plastic growth, suggesting that this was the plesiomorphic condition for dinosaurs. The South African sauropodomorph Massospondylus carinatus is an ideal taxon in which to test this because it is known from a comprehensive ontogenetic series, it has recently been stratigraphically and taxonomically revised, and it lived at a time of ecosystem upheaval following the end-Triassic extinction. Here, we report on the results of a femoral osteohistological study of M. carinatus comprising 20 individuals ranging from embryo to skeletally mature. We find major variability in the spacing of the LAGs and infer disparate body masses for M. carinatus individuals at given ontogenetic ages, contradicting previous studies. These findings are consistent with a high degree of growth plasticity in M. carinatus.

Osteohistology reveals the smallest adult Jurassic sauropodomorph.

The earliest sauropodomorphs were small omnivores (less than 10 kg) that first appeared in the Carnian. By the Hettangian, early branching sauropodomorphs (EBSMs) were globally distributed, had variable postures, and some attained large body masses (greater than 10 tonnes). Small-bodied EBSMs like Massospondylus carinatus (less than 550 kg) persist at least until the Pliensbachian at nearly all dinosaur-bearing localities worldwide but are comparatively low in alpha diversity. One potential reason for this is competition with other similarly sized contemporary amniotes, including Triassic gomphodont cynodonts, Jurassic early branching ornithischians, herbivorous theropods and potentially early crocodylomorphs. Today's herbivorous mammals show a range of body size classes (less than 10 g to 7 tonnes), with multiple species of small herbivorous mammals (less than 100 kg) frequently co-occurring. Comparatively, our understanding of the phylogenetic distribution of body mass in Early Jurassic strata, and its explanatory power for the lower thresholds of body mass in EBSMs, needs more data. We osteohistologically sectioned a small humerus, BP/1/4732, from the upper Elliot Formation of South Africa. Its comparative morphology and osteohistology show that it represents a skeletally mature individual of a new sauropodomorph taxon with a body mass of approx. 75.35 kg. This makes it one of the smallest known sauropodomorph taxa, and the smallest ever reported from a Jurassic stratum.

Rapid turnover of top predators in African terrestrial faunas around the Permian-Triassic mass extinction.

Catastrophic ecosystem disruption in the late Permian period resulted in the greatest loss of biodiversity in Earth's history, the Permian-Triassic mass extinction (PTME).1 The dominant terrestrial vertebrates of the Permian (synapsids) suffered major losses at this time, leading to their replacement by reptiles in the Triassic.2 The dominant late Permian predatory synapsids, gorgonopsians, were completely extirpated by the PTME. The largest African gorgonopsians, the Rubidgeinae, have traditionally been assumed to go extinct at the Permo-Triassic boundary (PTB).3,4,5 However, this apparent persistence through the sustained extinction interval characterizing the continental PTME6 is at odds with ecological theory indicating that top predators have high extinction risk.7 Here, we report the youngest known large-bodied gorgonopsians, gigantic specimens from the PTB site of Nooitgedacht 68 in South Africa. These specimens are not rubidgeine, and instead are referable to Inostrancevia, a taxon previously thought to be a Russian endemic.8 Based on comprehensive review of the South African gorgonopsian record, we show that rubidgeines were early victims of ecosystem disruption preceding the PTME and were replaced as top predators by Laurasian immigrant inostranceviines. The reign of this latter group was short-lived, however; by the PTB, gorgonopsians were extinct, and a different group (therocephalians) became the largest synapsid predators, before themselves going extinct. The extinction and replacement of top predators in rapid succession at the clade level underlines the extreme degree of ecosystem instability in the latest Permian and earliest Triassic, a phenomenon that was likely global in extent.

Origins of slow growth on the crocodilian stem lineage.

Crocodilians grow slowly and have low metabolic rates similar to other living reptiles, but palaeohistology indicates that they evolved from an ancestor with higher growth rates.1,2,3,4,5 It remains unclear when slow growth appeared in the clade due to the sparse data on key divergences among early Mesozoic members of their stem lineage. We present new osteohistological data from a broad sample of early crocodylomorphs, evaluated in a phylogenetic context alongside other pseudosuchians. We find that the transition to slow-growing bone types during mid-late ontogeny occurred around the origin of Crocodylomorpha during the Late Triassic. Earlier-diverging pseudosuchians had high maximum growth rates, as indicated by the presence of woven bone during middle and (sometimes) late ontogeny.6,7,8,9 Large-bodied pseudosuchians in particular exhibit some of the fastest-growing bone types, giving evidence for prolonged, rapid growth. By contrast, early-branching crocodylomorphs, including a new large-bodied taxon, had slow maximum rates of bone deposition, as evidenced by the presence of predominantly parallel-fibered or lamellar bone tissue during middle-late ontogeny. Late Triassic crocodylomorphs show skeletal anatomy consistent with "active" terrestrial habits,10,11,12 and their slow growth rates reject hypotheses linking this transition with sedentary, semiaquatic lifestyles or sprawling posture. Faster-growing pseudosuchian lineages go extinct in the Triassic, whereas slow-growing crocodylomorphs do not. This contrasts with the Jurassic radiation of fast-growing dinosaurs on the bird-stem lineage,13 suggesting that the End-Triassic mass extinction initiated a divergent distribution of growth strategies that persist in present-day archosaurs.

Mercury evidence from southern Pangea terrestrial sections for end-Permian global volcanic effects.

The latest Permian mass extinction (LPME) was triggered by magmatism of the Siberian Traps Large Igneous Province (STLIP), which left an extensive record of sedimentary Hg anomalies at Northern Hemisphere and tropical sites. Here, we present Hg records from terrestrial sites in southern Pangea, nearly antipodal to contemporaneous STLIP activity, providing insights into the global distribution of volcanogenic Hg during this event and its environmental processing. These profiles (two from Karoo Basin, South Africa; two from Sydney Basin, Australia) exhibit significant Hg enrichments within the uppermost Permian extinction interval as well as positive Δ199Hg excursions (to ~0.3‰), providing evidence of long-distance atmospheric transfer of volcanogenic Hg. These results demonstrate the far-reaching effects of the Siberian Traps as well as refine stratigraphic placement of the LPME interval in the Karoo Basin at a temporal resolution of ~105 years based on global isochronism of volcanogenic Hg anomalies.

Rapid growth preceded gigantism in sauropodomorph evolution.

Sauropod dinosaurs include the largest land animals to have walked the earth, mostly weighing 10-70 tons (e.g., Sander et al.1 and Carballido et al.2). Osteohistology suggests that derived physiological traits evolved near the origin of sauropod gigantism, including both rapid and uninterrupted growth from juvenile to adult with little developmental plasticity.1,3,4 This differs from the slower, seasonally interrupted growth of their direct ancestors, as evident in most non-sauropodan sauropodomorphs, which also show developmental plasticity in some groups. Accelerated but seasonally interrupted growth is present in Lessemsauridae, the sister clade to Sauropoda, which also attained giant adult body sizes (>10 tons).5 These observations suggest a correlation between giant size and accelerated growth. However, testing this evolutionary connection has been limited by the incomplete understanding of the growth patterns in some of the closest non-giant relatives of sauropods. We present the osteohistology of two such taxa, Aardonyx celestae and Sefapanosaurus zatronensis. Both exhibit highly vascularized woven-parallel complexes, with fibrolamellar complexes during early to mid-ontogeny, containing regular growth marks. These observations provide strong evidence for rapid but seasonally interrupted growth with limited developmental plasticity (indicated by the regular spacing of growth marks). Combined with our review of early branching sauropodomorph osteohistology, these results show that highly accelerated growth rates originated among smaller, non-sauropodan sauropodomorphs weighing 1 to 2 tons but preceded the origins of giant size (>10 tons). Therefore, the capacity for rapid bone tissue formation, a derived aspect of rapid growth seen in sauropods, did not evolve specifically to enable giant body sizes but may have been a prerequisite for them.

Interelemental osteohistological variation in Massospondylus carinatus and its implications for locomotion.

Massospondylus carinatus Owen, 1854 is an iconic basal sauropodomorph dinosaur from the Early Jurassic of southern Africa. Over 200 specimens have been referred to this taxon, spanning the entire ontogenetic series from embryo to adult. Consequently, it provides an ideal sample for investigating dinosaur developmental biology, including growth patterns and growth rates, through osteohistological analysis. Massospondylus carinatus was the first early-branching sauropodomorph dinosaur for which a femoral growth series was sampled. Since then, growth series of other non-avian dinosaur taxa have shown that growth plasticity, interelemental variation, and ontogenetic locomotory shifts can complicate our understanding of growth curves and patterns. To investigate these questions further, it is necessary to sample multiple skeletal elements from multiple individuals across a large range of sizes, something that is often hindered by the incompleteness of the fossil record. Here, we conducted a broad, multielement osteohistological study of long bones (excluding metapodials) from 27 specimens of Massospondylus carinatus that span its ontogenetic series. Our study reveals substantial variations in growth history. A cyclical woven-parallel complex is the predominant bone tissue pattern during early and mid-ontogeny, which transitions to slower forming parallel-fibred bone during very late ontogeny. The bone tissue is interrupted by irregularly spaced cyclical growth marks (CGMs) including lines of arrested growth indicating temporary cessations in growth. These CGMs show that the previously recorded femoral growth plasticity is also visible in other long bones, with a poor correlation between body size (measured by midshaft circumference) and CGM numbers. Furthermore, we found that the growth trajectory for an individual can vary depending on which limb element is studied. This makes the establishment of an accurate growth curve and determination of the onset of reproductive maturity difficult for this taxon. Finally, we found no evidence of differential growth rates in forelimb vs hindlimb samples from the same individual, providing further evidence falsifying hypothesised ontogenetic postural shifts in Massospondylus carinatus.

The paleobiology and paleoecology of South African Lystrosaurus.

Lystrosaurus was one of the few tetrapods to survive the end-Permian mass extinction (EPME), the most catastrophic biotic crisis in Phanerozoic history. The significant increased abundance of this genus during the post-extinction Early Triassic recovery period has made Lystrosaurus an iconic survivor taxon globally and ideal for studying changes in growth dynamics during a mass extinction. There is potential evidence of a Lilliput effect in Lystrosaurus in South Africa as the two Triassic species that became highly abundant after the EPME are relatively smaller than the two Permian species. In order to test this hypothesis a detailed examination of the body size and life history of Permo-Triassic Lystrosaurus is required. In this study, the basal skull length and growth patterns of the four South African Lystrosaurus species from the Karoo Basin, L. maccaigi, L. curvatus, L. murrayi and L. declivis, were examined using cranial measurements and bone histology. The basal skull length measurements show that the Triassic species are smaller than the Permian species and supports previous studies. The osteohistology examination of all four species reveal rapidly forming fibrolamellar bone tissues during early to mid-ontogeny. Growth marks are common in L. maccaigi and L. curvatus, but rare and inconsistent in the purely Triassic L. murrayi and L. declivis. The inconsistency of the growth marks in these latter two taxa suggests the presence of developmental plasticity. This feature may have been advantageous in allowing these species to alter their growth patterns in response to environmental cues in the post-extinction Early Triassic climate. An overall transition to slower forming parallel-fibered bone is observed in the largest individuals of L. maccaigi, but absent from the limb bones of the other species. The absence of such bone tissue or outer circumferential lamellae in L. curvatus, L. murrayi and L. declivis indicates that even the largest collected specimens do not represent fully grown individuals. Although L. murrayi and L. declivis are smaller in size, the lack of a growth asymptote in the largest specimens indicates that adult individuals would have been notably larger and may have been similar in size to large L. maccaigi and L. curvatus when fully grown. Thus, the previously described Lilliput effect, recognized by some authors in the Karoo fossil record (such as the therocephalian Moschorhinus kitchingi), may be a product of high juvenile excess mortality in the Triassic rather than a strict "dwarfing" of Lystrosaurus species. The lifestyle of Lystrosaurus was also re-examined. Although previous studies have proposed an aquatic lifestyle for the genus, the similar morphology and bone microanatomy to several other large terrestrial Permo-Triassic dicynodonts supports a fully terrestrial mode of life.

Tooth replacement patterns in the Early Triassic epicynodont Galesaurus planiceps (Therapsida, Cynodontia).

Sixteen specimens of the Early Triassic cynodont Galesaurus planiceps (including eight that were scanned using micro-computed tomography) representing different ontogenetic stages were assembled to study the dental replacement in the species. The growth series shows that the incisors and postcanines continue to develop and replace, even in the largest (presumably oldest) specimen. In contrast, replacement of the canines ceased with the attainment of skeletal maturity, at a basal skull length of ~90 mm, suggesting that Galesaurus had a finite number of canine replacement cycles. Additionally, the functional canine root morphology of these larger specimens showed a tendency to be open-rooted, a condition not previously reported in Mesozoic theriodonts. An alternating pattern of tooth replacement was documented in the maxillary and mandibular postcanine series. Both postcanine series increased in tooth number as the skull lengthened, with the mandibular postcanine series containing more teeth than the maxillary series. In the maxilla, the first postcanine is consistently the smallest tooth, showing a proportional reduction in size as skull length increased. The longer retention of a tooth in this first locus is a key difference between Galesaurus and Thrinaxodon, in which the mesial-most postcanines are lost after replacement. This difference has contributed to the lengthening of the postcanine series in Galesaurus, as teeth continued to be added to the distal end of the tooth row through ontogeny. Overall, there are considerable differences between Galesaurus and Thrinaxodon relating to the replacement and development of their teeth.

Ontogenetic and inter-elemental osteohistological variability in the leopard tortoise Stigmochelys pardalis.

Testudines are a group of reptiles characterized by the presence of a shell covered by keratinous shields. Stigmochelys pardalis is the most widely distributed terrestrial testudine in southern Africa. Although relatively common with some life history traits being well known, the growth of this species has yet to be studied in any detail. The bone microanatomy of this clade differs from that found in other amniotes, where terrestrial species tend to display characteristics normally seen in aquatic species and vice versa. A detailed histological analysis of the limb bones of S. pardalis reveals extensive variation through ontogeny. Cortical bone becomes increasingly thicker through ontogeny and is finally resorbed in the late sub-adult stage, resulting in a thin cortex and a large infilled medullary cavity. The predominant bone tissues are parallel-fibred and lamellar-zonal for the forelimbs and hind limbs respectively. The oldest individual displayed an External Fundamental System indicating that the growth rate had decreased substantially by this stage. Variability is prevalent between the forelimb and hind limb as well as between early and late sub-adults Forelimb elements exhibit characteristics such as faster growing parallel-fibered bone tissue, slightly higher vascularization and a predominance of annuli over Lines of Arrested Growth (LAG) compared to the hind limb which exhibits poorly vascularized, slower growing lamellar-zonal bone interrupted by LAGs. These differences indicate that the forelimb grew more rapidly than the hind limb, possibly due to the method of locomotion seen in terrestrial species. The extensive bone resorption that occurs from the early sub-adult stage destroys much of the primary cortex and results in a significantly different ratio of inner and outer bone diameter (p = 3.59 × 10--5; df = 28.04) as well as compactness (p = 2.91 × 10--5; df = 31.27) between early and late sub-adults. The extensive bone resorption seen also destroys the ecological signal and infers an aquatic lifestyle for this species despite it being clearly terrestrial. This supports the results of other studies that have found that using bone microanatomy to determine lifestyle in testudines does not produce accurate results.

Ngwevu intloko: a new early sauropodomorph dinosaur from the Lower Jurassic Elliot Formation of South Africa and comments on cranial ontogeny in Massospondylus carinatus.

Our knowledge of Early Jurassic palaeobiodiversity in the upper Elliot Formation of South Africa has increased markedly in recent years with the discovery of new fossils, re-assessments of previously collected material and a better understanding of Stormberg Group stratigraphy. Here, Ngwevu intloko, a new genus of upper Elliot basal sauropodomorph is named on the basis of a complete skull and partial skeleton (BP/1/4779) previously assigned to Massospondylus carinatus. It can be distinguished from all other basal sauropodomorphs by a combination of 16 cranial and six postcranial characters. The new species is compared to a small ontogenetic series of M. carinatus as well as to a range of closely related taxa. Taphonomic deformation, sexual dimorphism and ontogeny are rejected as possible explanations for the morphological differences present between BP/1/4779 and other taxa. Osteohistological examination reveals that BP/1/4779 had nearly reached adult size at the time of its death at a minimum age of 10 years.

Abrupt and gradual extinction among Late Permian land vertebrates in the Karoo basin, South Africa.

The Karoo basin of South Africa exposes a succession of Upper Permian to Lower Triassic terrestrial strata containing abundant terrestrial vertebrate fossils. Paleomagnetic/magnetostratigraphic and carbon-isotope data allow sections to be correlated across the basin. With this stratigraphy, the vertebrate fossil data show a gradual extinction in the Upper Permian punctuated by an enhanced extinction pulse at the Permian-Triassic boundary interval, particularly among the dicynodont therapsids, coinciding with negative carbon-isotope anomalies.