Anatomy of a Mass Extinction

Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

Contents lists available at ScienceDirect

Palaeogeography, Palaeoclimatology, Palaeoecology

journal homepage: www.elsevier.com/locate/palaeo

Anatomy of a mass extinction: Sedimentological and taphonomic evidence for drought-induced die-offs at the Permo-Triassic boundary in the main Karoo Basin, South Africa

Roger M.H. Smith a,b,e,⁎, Jennifer Botha-Brink c,d,e a Iziko South African Museum, PO Box 61, Cape Town 8000, South Africa b Department of Geological Sciences, University of Cape Town, Rondebosch, 7701 Cape Town, South Africa c National Museum, PO Box 266, Bloemfontein 9300 South Africa d Department of Zoology and Entomology, University of the Free State, Bloemfontein 9300, South Africa e Centre of Excellence in Palaeosciences, Hosted by the University of the Witwatersrand, Private Bag 3, Wits, 2050, South Africa article info abstract

Article history: The southern part of the Karoo Basin of South Africa contains a near complete stratigraphic record of the Permo- Received 28 August 2013 Triassic boundary (PTB). Isotope- and magneto-stratigraphy confirm that these predominantly fluvial strata are Received in revised form 23 December 2013 approximately the same age as zircon-dated marine PTB sections (252 Mya). By August 2013, our team had Accepted 3 January 2014 found 579 in situ vertebrate fossils, mostly of the clade Therapsida, in PTB exposures at three widely separated Available online 15 January 2014 locations in the southern Karoo Basin. Biostratigraphic ranges of the various taxa found in each of the sections reveal three separate phases of die-off within the same roughly 75 metre-thick stratigraphic interval displaying Keywords: Permo-Triassic mass extinction the same sequence of sedimentary facies interpreted as indicative of climatic drying, increased seasonality and Karoo Basin the onset of an unpredictable monsoon-type rainfall regime. The three phases of an inferred ecologically- Fluvial facies stepped mass extinction are: Phase 1 (45 m–30 m below PTB datum) brought on by lowered watertables, Vertebrate taphonomy which led to loss of shallow rooting groundcover in the more elevated proximal floodplain areas and the Drought disappearance of the smaller groundcover-grazing herbivorous dicynodonts and their attendant small carni- Therapsids vores. Phase 2 (20–0 m below PTB datum), is the main extinction that occurs in massive maroon/grey mudrock culminating in an event bed of laminated reddish-brown siltstone/mudstone couplets. This facies reflects progressively unreliable rainfall leading to vegetation loss in proximal and distal floodplain areas. The larger tree-browsing herbivores and their attendant carnivores are confined to watercourses before finally disappearing. Phase 3 (25–30 m above PTB datum) occurs in massive maroon siltstone facies with evidence of climatic aridity including the accumulation of mummified carcasses buried by windblown dust. All of the surviving Permian taxa disappear within 30 m of the PTB. Temporal resolution based on accretion rates and pedogenic maturity of each stratigraphic section reveals that Phase 1 and Phase 2 die-offs lasted 21 000 and 33 000 years separated by a short period of 7000 years where no disappearances are recorded and this was followed by 50 000 years of stasis for the final extinction phase, lasting only 8000 years, that removed all the Permian survivor taxa,. We propose that the recorded disappearances are real (rather than preferential preservation failure) and that they represent drought-induced die-offs moving progressively up the food chain as the terrestrial ecosystem collapsed; the latter mostly likely caused by volcanogenic greenhouse gas emissions and rapid global warming. © 2014 Elsevier B.V. All rights reserved.

1. Introduction from both marine and terrestrial realms. The extinction occurred over a geologically short time variously estimated as 200 000 (Bowring The Permo-Triassic mass extinction (PTME) is considered to be the et al., 1998) to as little as 10 000 years (Ward et al., 2005). The latest largest ecological catastrophe that life has endured with an estimated SHRIMP analysis of zircons recovered from marine PTB strata in China 90–95% loss of species (Erwin, 1994; Looy et al., 2001; Benton and dates the peak of extinction at 252.3 million years ago (Mya) (Shen Twitchett, 2003; Benton and Newell, 2013) of plant and animal life et al., 2011). Suggested causes of the extinction include extraterrestrial impact (Becker et al., 2001; Tovher et al., 2012), volcanism (Renne et al., 1995), oceanic anoxia (Wignall and Twitchett, 1996; ⁎ Corresponding author at: Iziko South African Museum, 25 Queen Victoria St. Gardens, Isozaki, 1997; Hotinski et al., 2001), oceanic overturn (Knoll et al., Cape Town 8000, South Africa. Tel.: +27 214813879. E-mail addresses: [email protected] (R.M.H. Smith), [email protected] 1996), excessive methane release (Krull et al., 2000; Sheldon and (J. Botha-Brink). Retallack, 2002), CO2-induced global warming (Ward et al., 2000;

0031-0182/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.palaeo.2014.01.002 100 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

Smith and Ward, 2001; Schaller et al., 2011; Benton and Newell, 2013) multi-tiered Dicynodon Assemblage Zone trophic network to a simple andashinducedcooling(Tabor et al., 2007), ecosystem collapse (Wang food chain in the earliest Triassic Lystrosaurus assemblage which is at- et al., 1994; Ward et al., 2000, 2005), oxygen stress (Retallack et al., tributed to a 69–87% loss of surface vegetation and the consequent 2003; Huey and Ward, 2005) and climatic extremes exacerbated by straightening of river channels (Ward et al., 2000; Roopnarine et al., the shear size of the Pangean continent and its interference with 2007; Roopnarine and Angielczyk, 2012). Previous palaeopedogenic ocean/atmosphere circulation (Erwin, 1994). analyses used the ped textures and nodule morphology (Smith, 1995), Conclusive evidence for any of these suggested causes has yet to be depth to calcic horizons Retallack et al. (2003), and petrography and found although there is growing consensus that the extinction event soil chemistry (Tabor et al., 2007) as proxies for interpreting palaeo- was globally synchronous, geologically fast, but not instantaneous, and climate. Despite a lack of consensus, they do accept an overall trend of that it involved a temporary breakdown of the ocean/atmosphere equi- aridification, but differ in the interpreted wetness of the early Triassic librium leading to oceanic anoxia and rapid climate change (Erwin, floodplains. The sedimentological facies sequence through the PTB in 1994; Sephton et al., 2005). Recently Sidor et al. (2013) analysed the the southern Karoo Basin re flects a change from humid temperate distribution of vertebrates before and after the PTME and found that high sinuosity to semi-arid low sinuosity fluvial environments, which climatic isolation of the Pangean faunas led to a dramatic decrease in Ward et al. (2000) attributed to runaway greenhouse conditions overall diversity, but also caused provincialisation of the separate popu- resulting from the basaltic eruptions in northern Pangea and perhaps lations. Hancox et al. (2013) reached similar conclusions by demon- CH4-clathrate releases (Renne et al., 1995; Benton and Twitchett, strating provinciality amongst the Triassic anomodonts of southern 2003). An estimation of the sedimentation rates of the 5 m-thick Africa. However, recent studies have found that various vertebrate event beds that coincide with the final disappearance of many Late clades reacted differently to the PTME. For example, dicynodont therap- Permian taxa in the southern Karoo Basin has been estimated to be as sids passed through a bottleneck and experienced a temporary decrease little as 10 000 years (Ward et al., 2005), however, the accuracy of this in diversity, but declining morphological disparity was found to reflect a estimate has been questioned (Gastaldo et al., 2009). They disagreed steady long-term trend and was not due to the event itself (Ruta et al., with the Ward et al. (2005) use of the term “event bed” in reference 2013a). In contrast, archosauromorphs and cynodont therapsids appear to the red laminated mudrocks that occur at the palaeontologically de- to have thrived in the aftermath of the PTME, increasing in both diversi- fined extinction. Based on their own field measurements and predicted ty and disparity through the Triassic (Nesbitt et al., 2012; Ruta et al., sedimentation rates they calculated the time represented by this facies 2013b). to be longer than what is generally regarded as a geological event. How- The South African Karoo Basin contains the most complete terrestrial ever, for clarity, we reiterate that Ward et al. (2005) used the term sequence of the PTME, and as such, is able to provide the unique oppor- “event bed” not as a time interval, but to describe a rapid and wide- tunity of studying changing tetrapod populations combined with finely spread environmental change, which they correlated, using bio-, detailed stratigraphic data. The aim of this study is to provide detailed magneto- and chemostratigraphy, with the global Permo-Triassic field documentation of the progressive disappearance of the tetrapod boundary (Ward et al., 2012). fauna through the PTB sequence to determine the mechanisms of this The appearance of new Early Triassic taxa in the terrestrial ecosys- mass extinction and which of the possible causes best fittheevidence. tem of the southern Karoo Basin occurred shortly after the PTME The Karoo Basin covers an area of about 600 000 km2 some three (Smith and Botha, 2005; Botha and Smith, 2006), but pre-extinction di- fifths of the total surface area of South Africa, and is modelled as a versity levels only returned around 5 My later during the Middle Triassic retro-arc foreland basin that developed behind an inferred magmatic Cynognathus B Assemblage Zone (Roopnarine et al., 2007; Chen and arc and fold-thrust belt (e.g. Catuneanu et al., 1998; Johnson et al., Benton, 2012; Irmis and Whiteside, 2012; Irmis et al., 2013). The current 2006) between 300 and 200 Mya. However, there is a lack of tight syn- study collected palaeontological and sedimentological field data from chronisation of the infill with the timing of the orogenic thrusting, and three separate PTB outcrop areas in the southern Karoo Basin (Fig. 1) some stratigraphic relationships that are atypical of a flexural foreland to test the hypothesis that rapid global warming caused the PTME in basin. This has been in part explained by a reciprocal flexure model the terrestrial realm. It further documents the progressive stages of (Catuneanu and Elango, 2001) triggered by orogenic thrusting but an collapse of the terrestrial ecosystem and how these changes affected alternative interpretation is that the large scale sag resulted from litho- the resident tetrapod populations. spheric deflection caused by mantle flow from a distant subduction zone (Pysklywec and Mitrovica, 1999; Tankard et al., 2009). 2. Field techniques and procedures The Karoo Supergroup in the main Karoo Basin consists of up to 8500 m of clastic sediments and lavas, but pre-erosional thickness of over Google Earth satellite imagery was used to target extensive clean ex- 10 000 m are thought to have been deposited in the deeper southern posures of measurable and potentially fossiliferous PTB strata extending part of the basin. From the time of the final breakup of Gondwana at least 100 stratigraphic metres below the distinctive basal sandstones around 110 Mya the strata of the Karoo Supergroup have been eroded of the Katberg Formation. Special care was taken to search for structural and today the flanks of numerous sandstone-capped mesas have features (mainly faults, folds and dykes) that could complicate the mudrock exposures that have become arguably the world's best lithostratigraphic correlation of exposures between adjacent gulleys. collecting grounds for therapsid fossils. In the southern Karoo Basin Targeted exposures were systematically surveyed by a team of five well-exposed strata spanning the PTB have been shown to be experienced fossil finders who walked back and forth along strike of stratigraphically continuous (Smith, 1995) and contain an abundance the exposed mudrock intervals taking care to apply equal “collecting of tetrapod fossils, which facilitates the documentation of details of pressure” on every bed. All in-situ (i.e. still embedded) vertebrate fossils the PTME in this part of western Gondwana, from before onset, through found were flagged, their positions logged into a handheld GPS the early to late phases of ecosystem collapse, into the early recovery then carefully uncovered for further identification and taphonomic phase, and finally to a fully-developed Triassic ecosystem. assessment. After field data had been recorded a decision was made Previous palaeontological studies of the PTB sequences in South whether to excavate and transport the specimen to the Iziko prepara- Africa have highlighted an extinction event amongst the tetrapods tion laboratory in Cape Town or leave it behind. The considerations (Smith, 1995; Smith and MacLeod, 1998; Smith and Ward, 2001; favouring fossil recovery are numerous including all specimens that Ward et al., 2005), which is coincident with a floral extinction are relatively complete and unaffected by recent weathering, specimens (Gastaldo et al., 2005)anda“spike” in the abundance of fungal spores that are taphonomically interesting (i.e. bones inside burrow casts, (Steiner et al., 2003). Trophic network modelling (Angielzyk et al., skin impressions, skeletons associated with coprolites, bite marks 2005; Smith et al., 2012) shows a dramatic transformation from the etc.), rare specimens and unidentifiable specimens that had potential R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 101

PTB Johannesburg

Be Durban Nb PTB

Cape Town

Main Karoo Basin

Fig. 1. Location and stratigraphic position of the logged PTB sequences included in this study. The measured sections are grouped into three separate study areas Lo, Lootsberg (Tweefontein, Lootsberg Pass and Old Wapadsberg Pass) Be, Bethulie (Fairydale/Bethel) and Nb, Nieu Bethesda (Krugerskraal and Ripplemead). for identification after preparation. A final, but important consideration stratigraphic distance in metres above or below the PTB datum at the lo- was to ensure that we collected the stratigraphically highest and lowest cality (see supplementary Table 1). Detailed sedimentological logs were specimen of each taxon found to date, regardless of the state of preser- recorded at every outcrop that yielded more than 10 fossils within the vation. Trace fossils such as coprolites, invertebrate and vertebrate bur- three study areas situated +/−350 km apart (for convenience named row casts and trackways were also logged and collected. A 1.5 m × 2 m Bethulie, Lootsberg and Nieu Bethesda, see Fig. 1). The length of individ- Plaster of Paris cast was made of multiple tetrapod trackways on a sand- ual logs is limited by the extent of clean rock exposures, however, wher- stone palaeosurface just above the PTB in the Bethel section (see ever possible, clusters of accurately correlated outcrops within a few Fig. 8B). A total of 80 days (approximately 3200 man hours) were hundred metres of each other were selected to cover the stratigraphic in- spent in the field resulting in a total of 579 potentially identifiable in terval from roughly 100 m below to 100 m above the palaeontologically- situ specimens from 100 m below to 100 m above the PTB, most of defined extinction event. In logging the sedimentological sections special which required many hours of mechanical preparation to expose the emphasis was given to climate sensitive features such as channel sand- taxonomically diagnostic characters. The locality, identification to at stone architecture, overbank splay sequences, palaeopedogenic modifica- least generic level, and stratigraphic position relative to the PTB datum tion and evidence for vertical and horizontal movement of groundwater of each specimen have been entered into the PTB database (see Supple- in the floodplain facies. The latter is interpreted from the distribution mentary Table 1), plotted onto the sedimentological sections (Figs.2,3 and morphology of pedogenic calcareous nodules, root moulds and and 4) and collated onto a biostratigraphic range chart to an accuracy of rhizoliths, and the colour mottling indicative of seasonally saturated 0.5 m (Fig. 11). Supplementary Table 1 also includes in situ specimens gley soil horizons. Taphonomic data were recorded for all in situ verte- that could be confidently identified, but were not collected due to ex- brate fossils including field identification of taxa (commonly to generic tensive weathering (labeled “not collected” in notes column). Addition- level), degree of skeletal disarticulation, skull position (i.e. dorsal-up, ally numerous specimens were collected and prepared to the point of ventral-up etc.). The degree of pre-burial bone-weathering and other identification, but were not accessioned into the South African Museum evidence of bone modification (e.g. tooth marks, trampling fracture (SAM) collections as they were not of sufficient quality. These are stored patterns) as well as post-burial perimineralisation and compaction in the collections under their RS field number (RS numbers in first col- were also noted. umn). Most of the specimens were collected and prepared and have Facies analysis allows for an estimation of the frequency and hydro- been accessioned into the collections of the SAM (SAM-PK-K) and a dynamics of overbank flows and the rates of deposition of each event. few into the Karoo Palaeontology Collection at the National Museum, Palaeosol analysis gives estimates of the duration of non-depositional Bloemfontein (NMQR). periods and groundwater movements. Taphonomic analysis qualifies The PTB datum in this study is taken as the top of the laminated both analyses with estimates of the duration of sub-aerial exposure of reddish-brown siltstone/mudstone couplets facies (red laminites skeletons. Estimates of floodplain accretion rates were gained from “event bed” of Ward et al., 2005), which in most of the sections is also studies of modern fluvial environments that have been shown to accu- marked by a horizon of large brown-weathering smooth-surfaced mulate similar sedimentological facies sequences and pedogenic pro- calcareous nodules. Every logged in situ fossil has been allocated a files. Additional time estimates were gained from taphonomic studies 102

Facies A

E ...Sih .BtaBik/Plegorpy aaolmtlg,Pleeooy36(04 99 (2014) 396 Palaeoecology Palaeoclimatology, Palaeogeography, / Botha-Brink J. Smith, R.M.H.

1cm D C

B – 118

C B R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 103

floodplain between large Mississippi-sized meanderbelt ridges (Smith, 1987b). Floodwaters periodically overtopped the meanderbelt channel banks and inundated the proximal floodplain depositing a layer of silt that buried the soil profile deeply enough to temporarily curtail pedogenesis and at the same time raise the water table. The horizons of oblate smooth-surfaced carbonate nodules are interpreted as having been precipitated in pond margin environments on semi-arid floodplains (Alonso-Zarza, 2003). The immature calcic vertisols (Smith, 1990) and poorly developed horizonation suggest high floodplain accretion rates resulting from regular, possibly seasonal, overbank flooding and seasonal temperature and moisture fluctua- tions. Thus, the palaeoclimatic interpretation of the massive grey mudrock facies is of a long relatively cool wet season and a short warm dry season with watertables remaining relatively high throughout the year resulting in surface seepage and evaporation around shallow wet depressions, ponds and lakes especially along the axis of the interchannel belt (distal floodplain). B. Massive mottled maroon/grey mudrock (uppermost Permian) interbedded with thin tabular sandstone bodies displaying distinctively “gullied” basal contacts and climbing ripple cross stratification both of which are indicative of rapid scour-and-fill sedimentation (Fig. 6A, B). The mottled siltstones contain isolated brown- weathering calcareous nodules some of which contain fossil bone (Fig. 6C, D) along with claystone-lined root moulds, and the first Fig. 2. Sedimentological log with facies and in situ fossils from the Ripplemead PTB expo- occurrence of distinctive metre-long Katbergia burrow casts sures in the Nieu Bethesda study area. (A) Oblique satellite image of section locality cour- (Fig. 7A). These burrow casts are straight and dip at a consistent tesy of Google Earth. Short vertical arrows indicate the base of the arenaceous Katberg 45° but are randomly orientated. They are assigned to an inverte- Formation. (B) View from the embedded new large cynodont specimen next to hammer brate scratch-digging decapod (Gastaldo and Rolerson, 2008) (RS 439 on log) up-section through the PTB outcrops. (C) New large cynodont skull after excavation from the uppermost Permian approximately 22 m below the PTB. Skull is possibly a callianassid-like shrimp (Smith and Botha, 2005). The 16 cm long. (D) Dorsal view of the dicynodont Lystrosaurus murrayi from lowermost sandstone bodies are composed of two or three vertically stacked Triassic rocks approximately 10 m above the PTB. units structured by horizontal lamination grading upwards into climbing ripple cross-lamination. Some of the elongated basal of modern bone burial that show comparable disarticulation ratios and scours contain lenses of reworked mudrock pebbles and flakes, degree of bone weathering as the numerous tetrapod fossils recovered but with few pedogenic glaebules. in this study. All these sources of information are used to test the hy- Three sedimentological features distinguish this facies from the pothesis that rapid climate change was the main reason for the global underlying massive grey mudrock. They are characterized by die-off known as the PTME. the first occurrence of patchy rubification of the mudrocks, the first occurrence of vertically stacked sheet sandstones with fluted 3. Description and interpretation of PTB facies sequence (Fig. 7C) and gullied basal surfaces and the first occurrence of Katbergia burrows. Collectively these new features are interpreted A series of 150 m-thick stratigraphic sections through the PTB as indicative of a relatively rapid change in fluvial style from a few interval were logged and systematically searched for in situ fossils at large meandering channel belts to a network of more numerous three separate localities namely Bethulie, Lootsberg Pass (Type locality smaller low sinuosity channels. At the same time there was a switch of the Lootsbergian faunachron of Lucas, 2002) and Nieu Bethesda, from seasonally fluctuating perennial flow to more ephemeral-type (see Figs. 1–4). At all the study sections the predominant channel “flash flood” hydrodynamics along with progressive lowering of the palaeocurrent direction is today's north to north east. The Lootsberg floodplain watertables. As these changes affected the entire basin and Nieu Bethesda sections lie approximately 800 km from the former synchronously within a relatively short time interval a climatic margin of the basin and some 200 km closer to the original catchment rather than tectonic control is considered more plausible. We there- area than Bethulie. Despite differences in thickness, the sequence of fore interpret these sedimentological features as reflecting an sedimentary facies across the PTB in all these sections is comparable increase in the expression of climatic seasonality and intensity of (i.e. A–EofFig. 5). From the lowest (A) to the highest (E) the sequence rainstorms such that might result from the onset of a monsoonal is as follows: rainfall regime similar in many respects to the Late Triassic “megamonsoon” of Dubeil et al. (1991). A. Massive grey mudrock (Upper Permian) interbedded with stacked C. Laminated reddish-brown siltstone/mudstone couplets (PTB metre-thick tabular beds of structureless bluish-grey and greenish- “event” beds) occur at the same position in the facies sequence in grey siltstone and rare, thicker (up to 6 m-thick) erosionally- all measured sections (Fig. 5). Ranging between 3–5 m thick, this based, fine-grained sandstone bodies. The latter are structured by facies provides a distinctive marker bed (see Fig. 2 of Gastaldo trough-cross beds at the base, grading upwards into ripple cross- et al., 2009)thatissufficiently different from those above and laminated sandstone stringers with low-angle (10–15°) lateral below to be used as a mappable unit (corroborated independently, accretion surfaces typical of large sand-dominated point bars Botha-Brink et al., 2014) and a datum in the measured sections (Jackson, 1981; Labrecque et al., 2011). The siltstone beds commonly (see Figs. 2–4andFig. 5A). The main sedimentological feature host metre-thick horizons of oblate smooth-surfaced brown- of this facies is the presence of distinctive thickly-laminated weathering nodules from 5–20 cm in diameter containing brecciated siltstone-mudstone couplets, each 1–3 cm thick, with a sharp flat siltstone clasts floating in micritic cement. basal surface and an upward fining texture. Where the coarser The interpreted depositional setting for the massive grey mudrock fraction contains more fine sand-sized particles it gains a pale grey facies is an expansive flat generally dry, but seasonally wet colour whereas the mudstone portion is always dark reddish 104

Facies A

E ...Sih .BtaBik/Plegorpy aaolmtlg,Pleeooy36(04 99 (2014) 396 Palaeoecology Palaeoclimatology, Palaeogeography, / Botha-Brink J. Smith, R.M.H.

D 2cm

B – 118

n A C

B R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 105

brown (Munsell 2.5YR 2.5/4). Individual 2 cm thick couplets sequence in the Karoo Basin is evidence of incremental overbank can be traced along strike for 20 m with no visible bioturbation, sedimentation episodes with irregular periodicity, interspersed pedogenisis or desiccation features; in fact it is the anomalous with episodes of sheetwash erosion and rill formation that resulted absence of these features that makes this facies so distinctive. from rapid loss of vegetation, lowering of watertables and the Earlier field parties (Smith and Ward, 2001) could not find any body suspension of soil-forming processes. Interestingly, Newell et al. fossils in this facies, but increasing the prospecting intensity has (2010) record a similar laminated mudrock facies at the top of recovered an impoverished Upper Permian tetrapod fauna in this in- the Permian succession in Russia, which they interpret as fluvial/ terval (Ward et al., 2005). This was corroborated by an independent playa deposits that were disrupted by braided stream channels in study on a recently re-discovered PTB site that records a complete the earliest Triassic as a result of devegetation of the upland source sequence from uppermost Permian to Lower Triassic rocks, ap- areas. We record a similar landscape evolution in the southern proximately 40 km north of the Bethulie site (Botha-Brink et al., Karoo Basin, albeit with more transitional facies, such that a linked 2014). Retallack et al. (2003) also found evidence of incipient pe- cause such as rapid global warming, is a compelling explanation. dogenesis and root traces similar to those in uppermost Permian D. Massive maroon siltstone facies (lowermost Triassic) consisting of strata in Antarctica. At Bethulie this facies interval coincides with a massively-bedded maroon and olive-grey siltstone interbedded negative stable carbon isotope anomaly (McLeod et al., 2000) and with minor thin sandstone sheets with sharp flat basal and upper a magnetostratigraphic reversal (Steiner et al., 2003; Ward et al., contacts (Fig. 8A), the latter preserving rippled palaeosurfaces, 2005) both of which have been correlated with radiometrically- which in some places display trackways with digit impressions dated Permo-Triassic boundary sections in China. We interpret the (Fig. 8B,C) of interpreted dicynodonts and cynodont therapsids. occurrence of this facies in this stratigraphic position throughout Rough-surfaced irregularly shaped calcareous nodules, scattered the southern Karoo Basin as indicative of a basin-wide environmen- small spherical peloids with internal shrinkage cracks and isolated tal disturbance or climatic event associated with the PTME. The use Katbergia burrow casts occur in broad horizons within the rubified of the term climatic event refers to a climate induced perturbation siltstones beds. Articulated Lystrosaurus skeletons (Fig. 9A), some lasting 10 000–100 000 years rather than an instantaneous event in tubular burrow cast structures (Modesto and Botha-Brink, such as might result from bolide impacts or catastrophic volcanic 2010) are relatively abundant in this interval and are commonly ash falls. We regard the common, but not ubiquitous, occurrence thickly enveloped in dark reddish-brown nodular material. of a horizon of large oblate micrite nodules at the top of this facies A first occurrence in this facies is that of distinctive medium-sized as a workable lithological marker (“golden spike”) of the End- sand-filled decline burrow casts ascribed to the burrowing activity Permian in the southern Karoo Basin (Ward et al., 2012). of therapsids in particular the scratch digging cynodonts Galesaurus Ward et al. (2000) compared the PTB facies sequence in the and Thrinaxodon (Fig 8A + insert). southern Karoo to modern fluvial systems that have been subjected The distinguishing sedimentological features of this facies is the re- to increased sediment load resulting from rapid devegetation of version to massive siltstone dominated overbank facies, but by this their floodplains and source areas. They also drew comparisons time the mudrocks are entirely and uniformally reddened to a ligh- with pre-Silurian floodplain deposits that accumulated before land ter maroon or dark red (2.5 YR 3/6) compared to the dark reddish plants had evolved and in the absence of true pedogenesis. We brown (2.5 YR 2.5/4) of the lower facies and they contain evidence generally agree with these findings and would add that the most of desiccation and aeolian sedimentation. The loessic origin is evi- plausible cause for the loss of vegetation in the floodplains (and denced by the thick beds of red uniform textured silt with planar probably an equally severe reduction in diversity and density or gently undulating contacts that are commonly veneered with along the channel belts) was a rapid basin-wide drop in watertable dark red clay (Giles et al., 2013) indicative of episodic rapid sedi- brought about by rainfall in the basin and hinterland becoming un- mentation. Weakly developed palaeosols with textural BCa horizons reliable and concentrated into short duration monsoon-type down- showing claystone-lined shrink/swell planes and small peloidal pours. The evident loss of vegetation would have lowered the carbonate nodules are also characteristic of rapid sedimentation cohesive strength of the channel banks making them more easily events that bury the soils and curtail pedogenesis (Chan, 1999). erodible and unable to maintain a highly sinuous course. Thus, the The palaeoenvironmental significance of rubification in these sedimentological evidence suggests that the main rivers evolved mudrocks very much depends on whether the oxidation of iron straighter, wider and shallower channel profiles as an ephemeral compounds is primary (pedogenic or early diagenetic) or secondary flash-flood hydrological regime became the norm. Away from the (late diagenetic, metamorphic). In this case, the baking effects along channel belts on devegetated floodplains torrential downpours the margins of dolerite intrusions locally change the mudrock colour resulted in excessive surface run-off. Rills and gulleys scoured the in this facies to light grey (5Y7/2). We are confident that the redden- floodplain surface and filled the lowland depressions with tempo- ing is primary and because it is distinctively massive compared to rary water bodies. Sediment laden run-off flowed down the gulleys, the underlying facies we attribute this to an increase in loessic entered the playas and spread across the lake bed as turbidite flows dust settling on the dry floodplain surface containing iron oxide par- depositing the sand-sized load as a turbid sand sheet. Soon after the ticles that were then remobilized and distributed throughout the flow ceased the sand was blanketed by a layer of suspension fall-out solum. Previous workers have interpreted the onset of reddening silt and clay. It is proposed that these turbidites are preserved in the in the PTB sequences of the southern Karoo variously as indicative PTB sequence as the laminated siltstone/mudstone couplets facies. of warmer mean annual temperatures with generally wetter soil Similar laminated couplets resulting from successive sheetwash conditions (Retallack et al., 2003) or as cooler temperatures with events are found in terminal fandeltas issuing into playas of the generally wetter soil conditions (Tabor et al., 2007). We take the hyper-arid Lake Eyre Basin of Australia (Croke et al., 1998). We view that this massive maroon siltstone facies is partially loessic in conclude that the ubiquitous red laminated bed of the PTB facies origin and thus could only have been generated by cyclones moving

Fig. 3. Sedimentological log with facies and in situ fossils from Old Wapadsberg Pass in the Lootsberg Pass study area. Legend as in Fig. 2. (A) Oblique satellite image of the section locality courtesy of Google Earth. Short vertical arrows mark the base of the Katberg Formation sandstones. (B) Embedded dorsal-up skull of the large Late Permian dicynodont Dinanomodon (RS 168 on log) approximately 25 m below the PTB in massive grey mudrock facies. (C) View up-section from the PTB boundary which is commonly marked by a layer of brown-weathering micritic nodules (n). Note the change in mudrock colour and texture from blue-grey blocky weathering siltstone to dark red laminites across the PTB. (D) Two juvenile cynodont skeletons (Thrinaxodon lihorhinus, SAM-PK-K 10017 = RS 167 on log) from the red mudrocks of the Lower Triassic basal Katberg Formation at 32 m above the PTB. The head-to-head juxtapositionof identical skeletons is interpreted as members of the same brood having died whilst aestivating or hibernating. 106

Facies A

E ...Sih .BtaBik/Plegorpy aaolmtlg,Pleeooy36(04 99 (2014) 396 Palaeoecology Palaeoclimatology, Palaeogeography, / Botha-Brink J. Smith, R.M.H.

D D

B – 118

C B R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 107

Facies mudstone beds. The thicker (3–5 m) multistoried channel sandstones commonly display elongate basal scours or gulleys (Fig. 9B) eroded into the underlying mudrocks and filled with lenses of glaebule conglomerate (Fig. 9C). The sandstone body contains several (2–5) irregular disconformity surfaces that are commonly lined with lenses and stringers of mudstone clast conglomerate. E The basal conglomerates are a distinctive feature of this facies in that they are composed of mud pebbles, reworked bone fragments and numerous spheroidal pedogenic pisoliths many with internal septarian shrinkage cracks (Fig. 9C). Mudrock dominated inter- B vals comprise metre-thick alternating beds of massive olive D grey (5Y5/2) siltstone and dark-red fissile mudstone interbedded with sporadic thin (0.25–0.5 m thick), olive-grey, fine-grained single- PTB storied sheet sandstone bodies that commonly display sand-filled C downward tapering desiccationcracksatthebasalcontact(Fig. 9D). The vertically accreted multi-storied conglomeratic sandstone bodies are interpreted as the preserved in-channel deposits of wide, shallow low-sinuosity rivers with a highly fluctuating discharge regime and pe- B riods when flow ceased altogether similar in many aspects to the sandy ephemeral stream channel fills described from the Mid-Devonian of southern England by Tunbridge (1984). The intraformationally- derived conglomerates contain an interesting first appearance- abundant spherical pea-sized calcareous pisoliths (or glaebules) A many containing outwardly tapering star-shaped septarian shrinkage C cracks. Their inclusion within a clast-supported melange of red mudrock pebbles, rolled bone fragments and other pedogenic calcar- A eous nodules (Fig. 9C) indicates that they too have been reworked from the alluvium into which the channel has incised. The Katberg Fig. 5. Facies sequence A–E through the PTB on Bethel in the Bethulie study area illustrates Formation pisoliths are comparable to those described from Quater- the sequence encountered at this stratigraphic level in all three study areas. (A) General nary calcretes of western Australia occurring scattered within sandy view of the PTB exposures on Bethel. (B) Closer view of the maroon laminated “event parent material (Arakel, 1982)aswellasthosedescribedaspedogen- bed” of Smith and Ward (2001) at the top of Facies C. (C) General view of outcrop style of the Upper Permian massive grey mudrock facies lower down in the succession. Facies ic peloids from the semi-arid Indo-Gangetic alluvial plains of India A, Massive grey mudrock; B, Massive mottled maroon/grey mudrock; C, Laminated (Khadkikar et al., 2000). On the Indus floodplain they form shallow reddish-brown siltstone/mudstone couplets; D, Massive maroon siltstone; E, Conglomer- B/Ca horizons some 0.25 m below surface in silt-dominated alluvium atic sandstone. around springs and playa lakes. They are the result of an evapora- tive pump driven by the rapid alternation between saturated and dry soil moisture conditions under a warm climate monsoonal across dry floodplain surfaces suggesting that the palaeoclimate at rainfall regime. The appearance of similar septarian glaebules in the time was semi-arid, dry for most of the year with a short, but the PTB stratigraphic record in the main Karoo Basin serves to intensive wet season. Structural (i.e. non-geochemical) evidence of strengthen the sedimentological facies interpretation for warm mean annual temperature is difficult to find in the rock record, how- climatic conditions with highly seasonal rainfall in this part of ever the combination of loessic palaeosols with vertic shrink/swell western Gondwana in the earliest Triassic. The sudden appear- structures, iron rich pedogenic carbonate horizons and calcareous ance of pisolith-rich intraformational conglomerate at the onset perimineralisation of freshly buried bone, suggests that an evapora- of the Katberg braidplain progradation suggests that a certain tive capillary-pump was seasonally operative within the B horizon amount of floodplain degradation (incision) was taking place up- of the soils some 1.5 m below the surface. From this it can be inferred stream, possibly reworking a mature piedmont surface at the that the mean annual temperatures were probably higher (26–30 °C base of the Gondwanide mountain chain. of Smith, 1990) rather than lower (18–20 °C of Tabor et al., 2007). Interestingly very similar massive to laminated to massive siltstone 4. Vertebrate taphonomy of the PTB facies sequence facies transitions occur in Mid-Late Triassic rift bound red beds of southern England, which have been attributed to loessic sedimen- 4.1. Degree of disarticulation and fragmentation tation on distal alluvial playas (Tucker, 1978) or alternatively sheetwash deposits of reworked pedogenically modified mud ag- The degree of disarticulation of fossil skeletons changes through the gregates (Talbot et al., 1994) by the same process as that described PTB facies sequence from the massive grey mudrock facies that contain from Lake Eyre Basin by Magee et al. (2004). mainly isolated postcranial elements (mostly humeri), lower jaws E. Conglomeratic sandstone facies (Lower Triassic) comprises the and rare skulls through the onset of pedogenic rubification within lower strata of the Katberg Formation; composed of vertically the grey/maroon mudrocks where mainly skulls and isolated lower stacked tabular olive-grey medium-grained sandstone bodies jaws of the larger dicynodonts are found without any associated separated by upwardly thinning intervals of blocky weathering postcrania. This facies gives way to an interval of maroon laminated light olive grey (5Y 6/2) siltstone, and fissile dark red (2.5YR 3/6) mudrocks that was initially thought to be barren of vertebrate

Fig. 4. Sedimentological log with facies and in situ fossils from the Bethulie study area. Legend as in Fig. 2. (A) Oblique satellite image courtesy of Google Earth of the “Bethel Canyon” showing the outcrops logged in this study. The Caledon River is in the foreground eroding Upper Permian strata and the more resistant sandstones of the Triassic Katberg Formation form the upper plateau. Vertical arrow denotes base of Katberg Formation (B) Late Permian massive grey mudrock with ventral-up skull of Dicynodon lacerticeps (RS 51 = SAM-PK-K 9949). (C) View of lowermost Triassic massive maroon siltstone facies. (D) Prepared specimen of an articulated Lystrosaurus declivis that was re-embedded for a photoshoot at the place it was found in the “Bethel Canyon”. 108 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

15 cm 1 cm AB

CD30 cm 10 cm

Fig. 6. Sedimentology of PTB massive mottled maroon/grey mudrock facies. (A) View of a low-sinuosity channel sandstone in the mottled siltstone facies on Bethel showing two vertically stacked storeys: the lower dominantly structured with ripple cross-stratification and the upper with horizontal lamination. (B) Close up of climbing ripples outlined in A showing a 30° angle of climb indicative of rapid dumping of fine sand from sediment laden-flow. (C) View of massive mottled maroon/grey siltstone with an embedded Dicynodon skull (RS 60, arrowed) approximately 7 m below the PTB. (D) Vertical view of the embedded Dicynodon skull shown in C.

remains, but systematic searches have succeeded in locating a few in transportation, but low burial potential for all but the smallest therapsid situ specimens that indicate the remnants of the Dicynodon Assem- bones and bone fragments. Above the PTB this gives way to a semi-arid blage Zone (A.Z.) fauna. All of these specimens provide evidence of monsoonal floodplain environment where drought induced die-off, increased pre-burial breakage with preferential preservation of the shelter-sharing (Abdala et al., 2006; Fernandez et al., 2013), and more robust portions of dicynodont and therocephalian skulls, in- group-huddling (Viglietti et al., 2013)weremorecommon,andani- cluding the basioccipitals, caniniform processes and isolated cervical mals that died within depressions were buried en-mass by wind- vertebrae and phalanges. The overlying massive maroon siltstone blowndustwithinayearorso,somewiththeirmummified skin facies of the lowermost Triassic contains a relatively abundant still intact (see below). assemblage of articulated, semi-articulated as well as completely disarticulated, but still associated skeletons of 1–2 m length dicyno- 4.2. Description of taphonomically important PTB vertebrate fossils donts and archosauromorphs. We interpret the overall change in taphonomic style through 4.2.1. Submerged Lystrosaurus maccaigi the PTB to generally reflect the changing floodplain conditions. The In the middle of the massive maroon/grey mudrock facies in the disarticulated and scattered skeletons have been exposed on the flood- Bethulie section, approximately 11 m below the PTB a nearly complete plain surface for much longer than articulated specimens. On semi-arid Lystrosaurus maccaigi skeleton (RS 74/SAM-PK-K9958) was excavated. floodplains this residence time is mainly determined by the frequency Preparation revealed a ventral-up pose with a skull lying left lateral- and volume of sedimentation events. As most of these events emanate up and limbs still articulated, but slightly displaced from their life po- from overtopping of the channel banks the residence time on the flood- sition (Fig. 10A, B). This specimen is lying in a shallow depression plain (Rogers and Kidwell, 2010) decreases the closer the death site is to within the massive grey siltstone and was buried with slightly a major channel. Taking this into account we interpret the increasing more clay rich grey thickly laminated siltstone that still retained disarticulation ratios and fragmentation of skulls leading up to the some of the original bedding planes. Articulated skeletons are anom- PTB as an indication of decreased flood frequency. The anomalous alous in this facies, which contain mainly isolated skulls and postcra- occurrence of isolated skull fragments in the red laminites facies is nial elements and we interpret this specimen as having been buried interpreted as an indication of very low floodplain accretion rates, beneath standing water in a pond or lake bed. The lack of pedogenic with increased pre-burial weathering exacerbated by lack of vegetation carbonate perimineralization and the downward flexure of the strata and the dominance of sheetwash type sedimentation that has high beneath the carcass suggest that it came to rest on a wet substrate. R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 109

10 cm 1 cm AB

1 cm CD5 cm

Fig. 7. Massive maroon siltstone facies: (A) a single Katbergia arthropod burrow cast in massive siltstone. Note the outer surface of the fine sandstone burrow cast is coated with claystone veneer and displays a pustular texture. (B) Invertebrate burrow casts on a crevasse splay sandstone palaeosurface in the massive maroon siltstone facies. Note the meniscate backfilling of the unlined Taenidium burrow indicative of scratch diggers such as beetles and shrimps. (C) Distinctive flute casts preserved as sole marks on the base of a thin tabular crevasse-splay sandstone in Facies E. (D) Close up of backfilled Taenidium burrow showing meniscae of thin arcuate mudstone/sandstone alternations.

The ventral-up attitude is a possible indication that the putrifying in juxtaposition to the Lystrosaurus skull suggests that they were carcass was floating with its bloated belly up and that after the gasses es- attempting to feed on the dicynodont carcass and that they too became caped it sank to the bed in that position. A similar scenario is interpreted trapped in the thixotropic silt. A similar death trap scenario is for the articulated Lower Cretaceous iguanadontid dinosaurs in the interpreted for the Pleistocene Rancho La Brea bonebeds (Spencer Belgian Bernissart bonebeds (Baele et al., 2012). et al., 2003) where patches of numerous disarticulated mammalian long bones and skulls occur in bone-on-bone contact within a structure- 4.2.2. Mired Moschorhinus less fine-sand matrix. They too are orientated at high angles and there is Approximately 1 km away from the submerged Lystrosaurus maccaigi, an anomalous over representation of carnivores. in the same massive maroon grey mudrock facies, we excavated a rare co-occurrence of carnivorous therocephalian and herbivorous 4.2.3. Mummified Promoscorhynchus dicynodont taxa together that are clearly not associated with a Approximately 5 stratigraphic metres above the PTB on Bethel an in- burrow structure yet they suggest more than a chance association teresting disarticulated, but still associated skeleton of the therocephalian (Fig. 10C). The juxtaposition of two carnivorous Moschorhinus Promoscorhynchus platyrhinus (RS 129/SAM-PK-K10014) displays tex- kitchingi skulls and their semi-articulated skeletons alongside a tured surfaces in the surrounding siltstone that suggest the former pres- skull and scattered postcranial elements of a large herbivorous ence of mummified skin (Fig. 11A). Before the fossil was prepared a L. maccaigi (RS 137/SAM-PK-K0015) is worth consideration as a silicon mould was made of the possible skin impression which is now possible miring scenario. The anomalous anterior-up attitude of the stored with the specimen. After preparation (Fig. 11B) it was confirmed large L. maccaigi skull (Fig. 10C) and the chaotic three-dimensional that this was the most completely preserved and youngest documented contortion of the skeletons suggest that the animals became bogged occurrence of this genus (Huttenlocker et al., 2011). down in waterlogged silt possibly at a seep or pond margin. The channel A recently described specimen from 24 m above the PTB in the facies in this stratigraphic interval are conglomeratic sandstone with Bethel study area is of two articulated specimens of different taxa appar- gullied bases and structured with discontinuity surfaces that reflect an ently sharing a burrow (Abdala et al., 2006). The relatively high degree increasingly ephemeral hydrological regime. Such a regime would of articulation of elements that normally fall away during decomposi- have resulted in standing water pools in the main channels, and tion (i.e. ribs) is attributed to the carcasses of the cynodont Galesaurus temporary ponds and lakes out on the floodplains. It is likely that the planiceps and procolophonoid ‘Owenetta’ kitchingorum (possibly a latter is where the therapsids congregated during the dry season and junior synonym of Saurodektes, S. P. Modesto, Pers. Comm., 2006) is where miring is most likely to have taken place. The presence of having desiccated in the open burrow after death and before burial. two juvenile therocephalians, which are normally rare carnivore taxa, The effectiveness of desiccated skin in holding together parareptile 110 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

25cm A

C 10cm B

Fig. 8. Ichnology of the PTB sequence in the Bethulie study area. (A) Partially excavated cynodont burrow cast in massive maroon siltstone facies on the farm Bethel. Similar casts excavated in the same area have been shown to contain articulated remains of Thrinaxodon and Galesaurus. Note the thin tabular horizontally-laminated crevasse splay sandstone that most probably provided the burrow ﬁll sediment. (B) A rare palaeosurface exposure in the massive maroon siltstone facies on Bethel (see log in Fig. 4) displays a range of trackways attributed to dicynodonts and cynodonts. LP, left pes; LM, left manus; RP, right pes; RM, right manus. (C) Reconstruction of the size and step cycle of the dicynodont trace maker. Metre-rule for scale.

and therapsid carcasses exposed in semi-arid floodplains has been red laminites facies at the PTB as a third datum. A summary of the strat- poorly documented yet is well illustrated by carcasses in the present igraphic ranges of all 579 identifiable in situ fossils found in the sections day Karoo (Fig. 11C). Here we propose that the increased incidence of studied is shown in Fig. 12. The ranges of the individual taxa have been such mummified remains in the PTB sequence is corroborative evidence positioned in order of disappearance of pre-existing taxa and ap- for drought induced die-off. pearance of new taxa to highlight the faunal die-offs recorded by the vertebrate fossils in the strata of the upper Elandsberg and 5. Biostratigraphically-defined phases of the Permo-Triassic Palingkloof members. mass extinction The following is a descriptive summary of the environmental changes and observed faunal turnover in the southern Karoo Basin based on Figs.2,3and4show the three outcrop areas studied with the sedi- the identification and stratigraphic distribution of 579 in situ fossils mentological logs and fossils found in each study section. Before each found in this study. fossil was excavated, its position was recorded using a GPS, it was man- Extinction Phase 1 (45 m–30 m below PTB datum – Massive grey ually plotted onto a 1:50 000 topo-cadastral map and its stratigraphic mudrock – upper Elandsberg Member). The rainfall regime became position plotted onto a measured sedimentological section. Supplemen- more seasonal (+/−1000 mm/year), watertables were lowered for tary Table 1 includes all the relevant biostratigraphic data compiled much of the year leading to a loss of pond environments in distal from the logs and field books. The separate sections are correlated flood basins leaving evaporitic gypsum rosettes, and shallow rooting using the base of the Katberg Formation and the top of the Barberskrans groundcover in the more elevated proximal floodplain areas disap- Member (where it was exposed) as rough correlation and the top of the peared. With the loss of pond environments Uranocentrodon, the last R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 111

AB5 cm

30 cm CD2 cm

Fig. 9. Conglomeratic sandstone facies: (A) Embedded curled-up articulated skeleton of Lystrosaurus murrayi in the massive maroon siltstone facies approximately 30 m above the PTB on Tweefontein in the Lootsberg study area (B) View of distinctive gulleys at the base of a vertically-aggraded channel sandstone in the Bethulie area. Gulleying ﬁrst appears in the facies sequence in the maroon/grey mottled siltstone facies approximately 10 m below the PTB. (C) Close up of micrite-cemented intraformational pedogenic glaebule conglomerate from the base of a Lower Triassic channel sandstone in Facies E. Note the septarian shrinkage cracks in the reworked spherical calcareous glaebules and the limb bone of a juvenile dicynodont (arrowed). (D) Successive layers of overbank splay sandstone ﬁlling desiccation cracks in maroon massive siltstones of the Lower Triassic Katberg Formation.

of the rhinesuchid amphibians, disappeared. As the groundcover dimin- 25 and 30 m above the PTB including the dicynodont Lystrosaurus ished the small herbivorous dicynodonts including the previously curvatus, and the therocephalians Moschorhinus and Promoschorhynchus. successful and at times very abundant taxon Diictodon disappeared The latter taxa can be termed ‘dead clade walking’ (Jablonski, 2002)asal- as well as their cohabitant medium-sized gorgonopsian carnivore though they survived the extinction event itself, they soon disappeared Sycosaurus. in the aftermath. Extinction Phase 2 (20–0 m below PTB datum – Massive maroon/ Early Recovery Phase (5– 25 m above PTB datum – Conglomeratic grey mudrock and laminated reddish-brown siltstone/mudstone sandstone facies – lower Katberg Formation). The appearance of new couplets – lower Palingkloof Member). Rainfall became progressively Triassic taxa began during continued arid conditions. Frequent droughts more unreliable leading to die-off of vegetation in the proximal and restricted the range of the herbivorous dicynodonts, Lystrosaurus distal floodplain areas, Glossopteris trees and sphenopsid horsetails murrayi and L. declivis as well as the predators and scavengers to stands continued to grow alongside and within ephemeral watercourses. At of vegetation (mainly horsetails) along ephemeral watercourses. This the boundary, torrential monsoon driven rainstorms led to sheet flows resulted in a distinctive taphonomic style dominated by mummified that scoured the devegetated floodplains. The small (maximum skull carcasses of L. murrayi and bonebeds of multiple disarticulated juvenile length 15 cm) herbivorous dicynodont Dicynodontoides and the rela- Lystrosaurus declivis buried by loessic dust (Smith and Botha, 2005; tively large dicynodonts (skull lengths 30–55 cm) such as Dinanomodon, Viglietti et al., 2013). Aulacephalodon, Daptocephalus, Oudenodon, Pelanomodon, Dicynodon At least half of the Lystrosaurus AZ taxa made their first appearance and Lystrosaurus maccaigi became confined to watercourses before within the lowermost strata of the Triassic portion of the Palingkloof disappearing completely. Similarly, the larger carnivorous taxa such as Member, including amphibians, parareptiles, archosauromorphs, the gorgonopsian Rubidgea, and a new, as yet unnamed, large-bodied and a variety of therapsids. The presence of the archosauromorph cynodont also disappeared. This interval also heralded the end of the Proterosuchus fergusi is of special note as it is the first new genus to armoured pareiasaurians with the disappearance of Pareiasaurus appear above the PTB in both the Karoo and South Urals Basins and is serridens. The only taxa found to have survived this phase are the thus important in Pangean-scale palaeobiogeography. As far as we can herbivorous dicynodont Lystrosaurus curvatus and the carnivorous ascertain from our field data the stratigraphic range of Proterosuchus therocephalians Moschorhinus and Promoschorhynchus. at two widely separated sections appears to be very short, confined Extinction Phase 3 (25–30 m above PTB datum – Massive maroon to the lower Palingkloof Member between 5–14 m above the PTB. siltstone facies – upper Palingkloof Member). Arid conditions prevailed The biostratigraphic range of the therocephalian Tetracynodon darti in this part of Gondwana as a sparcely-vegetated braidplain prograded is also noteworthy as it was previously considered to be a survivor northwards to cover most of the basin. of the PTME. However, a revision of the genus has revealed that Windblown dust buried mummified carcasses along the ephemeral Tetracynodon tenuis is known only from a single specimen and is limited water courses and all of the surviving Permian taxa disappeared between to the Permian (Sigurdsen et al., 2012)whereasT. darti is limited to 112 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

A B

15cm

C tusk

orbit 10cm

Fig. 10. Taphonomy of PTB vertebrate skeletons. (A) Overhead view of an articulated Lystrosaurus maccaigi skeleton (RS 74 = SAM-PK-K 9958) excavated from massive grey siltstone facies approximately 30 m below the PTB on Bethel. (B) Artist's reconstruction of the ventral-up partially disassociated L. maccaigi carcass shown in A, interpreted as having been buried on the bed of a ﬂoodplain pond or lake. (C) L. maccaigi bonebed. Partially prepared block containing two Moschorhinus kitchingi skulls (arrowed) with partial skeletons in association with a large L. maccaigi skull preserved in an unusual anterior-up attitude within in massive mottled maroon/grey siltstone facies on Bethel. This chaotic 3-dimensional mix of carnivore and herbivore skeletons buried in a structureless silt substrate is interpreted as a miring scenario.

Triassic strata. The appearance of most of the taxa from the Lystrosaurus of 2–2.5 mm/year (Pickup, 1991; Knighton and Nanson, 2000). How- AZ within 30 m of the PTB indicates a rapid radiation into niches left ever, the observation that therapsid skulls were being completely vacant by Permian taxa. This rapid expansion so close to the boundary buried by overbank silt without significant weathering under semi- suggests that the lineages of many of these taxa originated during the arid conditions indicates a minimum sedimentation rate of at least Permian. 4.5 mm/year for the fossil-bearing intervals (Behrensmeyer, 1991; Smith, 1993). Calculating the temporal resolution of the 75 metre- 5.1. Temporal resolution of the extinction phases thick interval of rock strata that contains the palaeontologically- defined PTME on Ripplemead (Fig. 2, Table 1), using a compaction cor- The temporal resolution of each phase of extinction is difficult to rection of three for the channel sandstones and five for silt-dominated determine accurately because fluvial systems are an interconnected pedogenically modified floodplain facies (Baldwin and Butler, 1985; network of several depositional environments, each with different sed- Shelden and Retallack, 2001), an accretion rate of 10.5 mm/y for the imentary processes and long term accretion rates. Floodplain accretion point bar deposits and 4.5 mm/year for the overbank facies, and adding rates are especially difficult to quantify because they are essentially 10 ky years of floodplain stasis (Leeder, 1975) for each Stage I and 15 ky large flat areas of non-deposition that are susceptible to episodic erosion for each of the Stage II nodular horizons (Gile et al., 1965) gives an esti- and sedimentation events. As a guide to the predicted accretion rates, mated total of 141.8.ky (see Table 1). Applying the same calculations to Holocene deposits in the arid continental basin of south central each extinction phase demonstrates that phases 1 and 2 die-offs oc- Australia are considered to be a good modern analogue for the PTB curred over varying time intervals: Phase I lasted 26.6 ky followed by sections in the southern Karoo. Field studies of the modern Cooper a period of stasis lasting roughly 3 k where there were no recorded Creek system have measured normal floodplain aggradation rates disappearences before Phase II which lasted 42.2 ky followed by a R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 113

10mm 2.5cm

5 cm.

Fig. 11. Mummified skin impression. (A) Disarticulated, but still associated skeleton of Promoschorhychus cf. P. platyrhinus (Huttenlocker et al., 2011) from 2.5 m above the PTB on Bethel displaying an interpreted mummified skin impression (see insert). (B) Promoschorynchus skeleton (RS 129 = SAM-PK-K 10014) after preparation showing the taphonomic style of desiccated carcasses that are mostly disarticulated but the bones have been held together with mummified cartilage and skin. (C) Mummified carcass of a modern bat-eared fox collected from its lair beneath a sandstone overhang in the southern Karoo. It displays a passive death pose and shrunken skin with tendons still attached which is typical of an animal that died of malnutrition in a drought-prone environment.

3 Recovery phase 1

Phase 2

Fig. 12. Summary of the biostratigraphic ranges of 579 in situ vertebrate fossils located and logged during the course of this study (see supplementary Table 1). Biostratigraphic ranges supplemented with data from Botha et al. (2007) for Sauropareion anoplus, Proterosuchus and a personal observation of an in situ specimen of Tetracynodon darti from the farm Barendskraal (NMQR 3720). “Owenetta” kitchingorum may represent a junior synonym of Saurodektes rogersorum (S. Modesto personal communication, 2007). Plotting the ranges in the order of their disappearance highlights two phases of die-off in the latest Permian with the third occurring in the earliest Triassic at the same time as the ﬁrst wave of immigration and radiation. Ranges that extend beyond the 120 m PTB interval are indicated with a broken bar. 114 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

Table 1 Temporal resolution of the PTB sequences in the southern Karoo Basin. See text for explanation of how the time intervals were calculated from the sedimentary record.

Measured Phase I extinction Stasis 30–20 m Phase II extinction Stasis 0–25 m Phase III extinction Total years recorded by 70 m section 45–30 m below PTB below PTB 20–0 m below PTB above PTB 25–30 m above PTB thick PTB extinction interval (ky) (ky) (ky) (ky) (ky) (ky)

Ripplemead 26.6 2.9 42.2 54.5 15.6 141.8 Wapadsberg 28.4 7.0 29.0 52.8 7.0 124.2 Bethulie 10.5 11.1 28.0 43.7 3.5 96.8

Mean 21.8 7.0 33.1 50.3 8.7 120.9 longer gap of 54.5 ky years before the final extinction phase lasting only effects of climate change to its ability to excavate underground burrows 15.6 ky. Similar calculations made for the Wapadsberg and Bethulie sec- for body temperature and moisture regulation. The occurrence of sever- tions are summarized in Table 1. We are confident that the vertebrate al individual burrows in close proximity strengthens the comparison in fossil record in the southern Karoo Basin records the PTME as three size, body shape and life habit to modern ground dwellers in semi-arid phases of die-off, the first two lasting some 30 ky years and the last climes such as the ground squirrel and mongoose. However, Diictodon's much shorter at 9 ky years and each was separated by intervals of edentulate jaws and tortoise-like horny beak are adaptations for herbiv- 7 ky and 50 ky years respectively when there were no recorded disap- ory, and as such they would have been the first to be affected by the pro- pearances. We propose that the disappearances are real (rather than gressive loss of low groundcover foliage (clubmosses, ferns and preferential preservation failure or an expression of the Signor-Lipps glossopterid tree leaf litter) as a seasonal source of fodder. It is paradox- effect related to rareness) and because they are coincident with geological that Diictodon's burrowing ability was not able to save the genus ical evidence of climatic drying, they most likely reflect drought induced from extinction at the end-Permian, whereas this same ability may die-offs moving progressively up the food chain as the terrestrial eco- well have been pivotal in the success of the cynodonts in the earliest Tri- system gradually collapsed under the pressure of rapid global warming. assic (Smith and Botha, 2005). We conclude that despite their long his- One of the reasons why we interpret the stepped disappearances as tory of survivorship in the Karoo Basin, the small base herbivores such as indicative of drought-induced ecosystem collapse is that on all the Diictodon and Pristerodon were probably entirely dependent on shallow- sections, the small base herbivores and their attendant carnivores rooted groundcover type vegetation, the disappearance of which was an disappeared before the larger animals. This is contrary to observations important factor in their extinction. of modern drought induced die-offs in savanna ecosystems which affect Botha-Brink and Angielczyk (2010) hypothesized that rapid growth the larger herbivores and their attendant predators first. The difference was a factor that contributed to survivorship amongst dicynodonts at could well be attributed to which of the kill mechanisms of malnutrition the end of the Permian. Many of the latest Permian dicynodonts they and dehydration predominated. Recent studies have shown the main sampled (particularly Dicynodon and Lystrosaurus)revealedhighly kill mechanism in modern savannas to be malnutrition caused by vascularized fibro-lamellar bone, features which are consistent with over-grazing of vegetation in the area surrounding accessible drinking rapid growth rates (Amprino, 1947; Margerie et al., 2002). In contrast, water sources rather than thirst (Behrensmeyer et al., 2012). We the small dicynodonts Diictodon and Dicynodontoides revealed moder- apply a similar kill mechanism to the PTB faunas in the Karoo Basin, ex- ate to poorly vascularised fibro-lamellar bone that became parallel- cept in the absence of grasses, the general lowering of groundwater fibreed later in life, indicating relatively slower growth (Ray and water tables caused by CO2-induced aridification affected the shallow Chinsamy, 2004; Botha-Brink and Angielczyk, 2010). In a later study, rooting “groundcover” of ferns, mosses and horsetails. We propose Huttenlocker and Botha-Brink (2013) found that the relatively large that they became over-grazed by the base herbivores, long before the therocephalian Moschorhinus also grew quickly as shown by the highly deeper rooting glossopterid shrubs and trees. vascularized fibro-lamellar tissues in its' limb bones It is interesting to It has been proposed that the observed biostratigraphic ranges in the note that all Permian therapsids that have undergone bone histological PTB sequences may in fact be an artefact of the Signor Lipps effect (Ward analysis (Ray and Chinsamy, 2004; Botha-Brink and Angielczyk, 2010; et al., 2005) whereby rare taxa are lost from the stratigraphic record Chinsamy-Turan, 2012; Huttenlocker and Botha-Brink, 2013), exhibit before their actual disappearance from the ecosystem. This results multiple growth rings (i.e. annuli or Lines of Arrested Growth indicating in a characteristic convex curve in the biostratigraphic range chart. a temporary decrease or cessation in growth, usually on an annual basis; If this is the reason for the observed ranges then the argument for a Francillon-Vieillot et al., 1990), indicating multi-year growth to somatic much shorter extinction event is valid. However, our more detailed bio- maturity, regardless of body size. stratigraphic ranges presented here do not show a progressive disappearance curve, but rather a distinctive stepped pattern, and one of the first taxa to disappear was the dicynodont Diictodon, which was up 6. Summary and conclusions until that point very well represented in the fossil record. We regard our sample of 579 accurately logged in situ specimens to be sufficient This project adds new field data that documents changes in the de- to be able to make confident statements that the changes in fossil assem- positional environments and faunal populations in the Karoo Basin blages do in fact represent, to a large degree, changes in the once-living leading up to and during the Permo-Triassic mass extinction. It tests populations. the integrity of the fossil record and how, after taphonomic anomalies The disappearance of the small herbivorous dicynodont Diictodon in have been identified, the fossil faunal assemblages may be accepted as Phase 1 of the PTME is an unexpected result because it was up until that a robust indicator of original diversity. On the basis that appearance point a very successful taxon. Diictodon appeared towards the end of the and disappearance of fossil taxa in the PTB stratigraphic sections may Middle Permian (Smith et al., 2012) and maintained a presence in the be interpreted as close approximations to the first and last occurrence Karoo fauna for some 10 Ma, at times becoming very abundant (i.e. in of that taxon in this part of the Karoo Basin we recognize three separate the Tropidostoma Assemblage Zone, Sullivan et al., 2003). There has 10–30 000 year-long intervals when taxon disappearances far outnum- been some speculation as to how many Diictodon species originated ber appearances. Our detailed biostratigraphic range chart shows that over this time period (King, 1993) and currently D. feliceps is proposed the Karoo vertebrate fauna underwent a three-phased or “stepped” as the only valid species (Sullivan and Reisz, 2005; Angielczyk and extinction event that affected different ecotopes at different times Sullivan, 2008). Smith (1987a) attributed some of its resilience to the (Fig. 13). R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 115 Palaeo- Extinction Swartberg m Facies environment phases KATBERG FM.

E .

Early

Palingkl’f m recovery D Phase III BALFOUR FM

C 120 000y . Phase II

Elandsb’g m B .

Phase I

. A Barb’k

Ripplemead Bethel Wapadsberg

Fig. 13. Summary of the PTB facies sequence and phases of vertebrate extinction in the southern Karoo Basin. Modern analogues for the interpreted palaeoenvironments are the Indo- Gangetic alluvial plain for the latest Permian, the Eyre Basin, Australia for the earliest Triassic and a sparcely-vegetated braidplain for the Katberg sandstone. Facies descriptions: A, Massive grey mudrock; B, Massive mottled maroon/grey mudrock; C, Laminated reddish-brown siltstone/mudstone couplets; D, Massive maroon siltstone facies; E, Conglomeratic sandstone facies. Lithostratigraphic members of the upper Balfour Formation: Barb'k, Barberskrans member; Elandsb'g m., Elandsberg member; Palingkl'f m., Palingkloof member.

We conclude that all three phases of vertebrate extinction in the Assemblage Zone. The fossil record shows that this taxon originated Karoo Basin occurred over some 120 000 years and were primarily driv- farther along the Gondwanide foreland in the Antarctic portion of en by progressive climatic drying and increased expression of seasonal- Gondwana in the Early Triassic and only later colonized the Karoo ity causing the groundwater tables to drop and floodplain vegetation to Basin (Fröbisch et al., 2010). Tracing the ancestry of the immigrant progressively disappear. The rapidity of the onset of drought conditions taxa is beyond the scope of this paper, but it suggests that there were led to a breakdown of the terrestrial ecosystem which adversely affect- potentially more survivors of the extinction than are currently known ed the vertebrate communities from the bottom to the top of the food from the fossil record. chain. Interestingly, the radiation of new taxa after the main extinction At this point we can compare the results of our field-based micro- phase was almost as rapid as its loss, and appears most likely to have stratigraphic approach to the recent statistical analyses of specimens been accelerated by waves of immigration of drought-adapted fauna in the various Karoo collections (Irmis and Whiteside, 2012; Fröbisch, from the inter-tropical regions of Pangea (Sidor et al., 2013; Sahney 2013; Irmis et al., 2013). These workers used the numbers of specimens and Benton, 2008). Amongst the immigrant arrivals were the first housed in the various Karoo vertebrate collections, and their allotted archosauromorphs to inhabit the Karoo Basin, suggesting that along biozone, as an indicator of the relative abundance of taxa in the once- with the surviving synapsids, they too were physiologically pre- living population. They were able to confirm that the faunal turnover adapted to coping in a stressful, unpredictable environment (Botha- between the Dicynodon Assemblage Zone and the Lystrosaurus Assem- Brink and Smith, 2011; Botha-Brink et al., 2012). A similar migration blage Zone does indeed reflect an extinction event. However their scenario has been proposed for the first appearance in the Karoo succes- stratigraphic and temporal resolution is at biozone-level, which is sion of the dicynodont Kombuisia in the Middle Triassic Cynognathus considerably lower than the metre-level accuracy of the 579 specimens 116 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 in the 120 metre-thick sections covered by our study. The main advan- Benton, M.J., Newell, A.J., 2013. Impacts of global warming on Permo-Triassic terrestrial ecosystems. Gondwana Research. http://dx.doi.org/10.1016/j.gr.2012.12.010. tage of the collection-based studies is that they are better able to smooth Benton, M.J., Twitchett, R.J., 2003. How to kill (almost) all life: the end-Permian extinction out regional effects caused by climatic and environmental gradients event. Trends in Ecology & Evolution 18 (7), 358–365. within the main Karoo Basin so that the biozones become more useful Botha, J., Smith, R.M.H., 2006. Rapid vertebrate recuperation in the Karoo Basin following the End-Permian extinction. Journal of African Earth Sciences 45, 502–514. for inter-basinal and intercontinental correlation. However, our study Botha, J., Modesto, S., Smith, R.M.H., 2007. Extended procolophonoid survivorship after provides the intricate details of field-based observations that can be the end-Permian extinction. South African Journal of Science 48, 54–56. used to assess the finer complexities of the event, data which tend to Botha-Brink, J., Angielczyk, K.D., 2010. Do extraordinarily high growth rates in Permo- be lacking in collections-based studies. Triassic dicynodonts (Therapsida, Anomodontia) explain their success before and after the end-Permian extinction? Zoological Journal of the Linnean Society 160, Our research continues with documenting the stratigraphic ranges 341–365. and mapping the taphonomic pathways of the earliest Triassic verte- Botha-Brink, J., Smith, R.M.H., 2011. Osteohistology of the Triassic archosauromorphs brates in the southern Karoo Basin with the aim of establishing the timing Prolacerta, Proterosuchus, Euparkeria, and Erythrosuchus from the Karoo Basin of South Africa. Journal of Vertebrate Paleontology 31, 1238– 1254. and rates of adaptive radiation of the survivor taxa and the effects of im- Botha-Brink, J., Abdala, F., Chinsamy-Turan, A., 2012. The radiation and osteohistology of migration and possible ecological displacement by archosauromorphs. nonmammaliaform cynodonts. In: Chinsamy-Turan,A.(Ed.),Forerunnersof We also aim to confirm whether adoption of a fossorial lifestyle was a Mammals. Radiation, Histology, Biology. Indiana University Press, Bloomington, – fi pp. 223 248. signi cant contribution to the success of the Early Triassic cynodonts Botha-Brink, J., Huttenlocker, A.K., Modesto, S.P., 2014. Vertebrate paleontology of (Smith and Botha-Brink, 2009) and their anatomical advancement to- Nooitgedacht 68: a Lystrosaurus maccaigi-rich Permo-Triassic boundary locality in wards a mammalian grade. South Africa. In: Kammerer, C.F., Angielczyk, K.D., Fröbisch, J. (Eds.), Early Evolution- ary History of the Synapsida. Springer, Netherlands, pp. 289–304. Supplementary data to this article can be found online at http:// Bowring, S.A., Erwin, D.H., Jin, Y.G., Martin, M.W., Davidek, K., Wang, W., 1998. U–Pb zir- dx.doi.org/10.1016/j.palaeo.2014.01.002. con geochronology and tempo of the End-Permian mass extinction. Science 280, 1039–1045. Catuneanu, O., Elango, H.N., 2001. Tectonic control on fluvial styles: the Balfour Formation Acknowledgements of the Karoo Basin, South Africa. Sedimentary Geology 140, 291–313. Catuneanu, O., Hancox, P.J., Rubidge, B.S., 1998. Reciprocal flexural behaviour and con- trasting stratigraphies: a new basin development model for the Karoo retroarc fore- We would like to acknowledge members of Iziko South African land system, South Africa. Basin Research 10, 417–439. Museum's Karoo Palaeontology team: Annelise Crean, Georgina Farrell, Chan, M.A., 1999. Triassic loessite of North-Central Utah:stratigraphy, petrophysical char- – Paul October, Hedi Stummer, Zaituna Erasmus, Nolusidiso Mtalana and acter, and paleoclimate implications. Journal of Sedimentary Research 69, 477 485. fi Chen, Z.-Q., Benton, M.J., 2012. The timing and pattern of biotic recovery following the Sibusiso Mtungata, for the many hours of eldwork and for their expert end-Permian mass extinction. Nature Geoscience 5, 375–383. fossil preparation. Also volunteers Dr Mike Strong and Dr Derik Chinsamy-Turan, A. (Ed.), 2012. Forerunners of Mammals: Radiation, Histology, Biology. Wolvaardt for their fossil-finding and company in the field. Fossil Indiana University Press, Bloomington (330 pp.). fi Croke, O., Magee, J.C., Price, D.M., 1998. Stratigraphy and sedimentology of the lower identi cations by Dr Ken Angielczyk, Dr Christian Sidor, Dr Christian Neales River, West Lake Eyre, Central Australia: from Palaeocene to Holocene. Kammerer, Dr Adam Huttenlocker, Prof Claudia Marsicano, Dr Fernando Palaeogeography, Palaeoclimatology, Palaeoecology 144, 331–350. Abdala and Dr Sean Modesto are very much appreciated. We are in- de Margerie, E., Cubo, J., Castanet, J., 2002. Bone typology and growth rate: testing and quantifying ‘Amprino's rule’ in the mallard (Anas platyrhynchos). Les Comptes Rendus debted to the South African National Research Foundation's Incen- de l' Académie des sciences, Série Biologies 325, 221–230. tive funding (RS) and their African Origins Platform (GUN 68944 to Dubiel, R.F., Parrish, J.T., Parrish, J.M., Good, S.C., 1991. The Pangaean Megamonsoon — R.S. and GUN 81168 and 80587 to J. B-B.) for funding this project. evidence from the Upper Triassic Chinle Formation, Colorado Plateau. Palaios 6 (4), – Iziko South African Museum and National Museum provided much 347 370. Erwin, D.H., 1994. The Permo-Triassic extinction. Nature 367, 231–236. appreciated logistical support. Finally, we would like to acknowledge Fernandez, V., Abdala, F., Carlson, K.J., Cook, D.C., Rubidge, B.S., 2013. Synchrotron reveals the comments by Dr Ken Angielczyk and an anonymous reviewer that Early Triassic Odd Couple: injured amphibian and aestivating therapsid share burrow. considerably improved the manuscript. PLoS One 8 (6), e64978. http://dx.doi.org/10.1371/journal.pone.0064978. Francillon-Vieillot, H., de Buffrénil, V., Castanet, J., Geraudie, J., Meunier, F.J., Sire, J.Y., Zylberberg, L., de Ricqlès, A., 1990. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter, J.G. (Ed.), Skeletal Biomineralization: Patterns, Processes References and Evolutionary Trends. Van Nestrand Reinhold, New York, pp. 471–548. Fröbisch, J., 2013. Vertebrate diversity across the end-Permian extinction — separating Abdala, F., Cisneros, J.C., Smith, R.M.H., 2006. Faunal aggregation in the Early Triassic biological and geological signals. Palaeogeography, Palaeoclimatology, Palaeoecology Karoo Basin: earliest evidence of shelter-sharing behaviour among tetrapods. Palaios 372, 50–61. 21, 507–512. Fröbisch, J., Angielczyk, K.D., Sidor, C.A., 2010. The Triassic dicynodont Kombuisia Alonso-Zarza, A.M., 2003. Palaeoenvironmental significance of palustrine carbonates and (Synapsida, Anomodontia) from Antarctica, a refuge from the terrestrial Permian– calcretes in the geological record. Earth-Science Reviews 60, 261–298. Triassic mass extinction. Naturwissenschaften 97, 187–196. Amprino, R., 1947. La structure du tissue osseux envisage comme expression de differ- Gastaldo, R.A., Rolerson, M.W., 2008. Katbergia Gen. Nov., a new trace fossil from ences dans la vitesse de l'accroissement. Archives de Biologie 58, 315–330. Upper Permian and Lower Triassic rocks of the Karoo Basin: implications for Angielczyk, K.D., Sullivan, C., 2008. Diictodon feliceps (Owen, 1876), a dicynodont palaeoenvironmental conditions at the P⁄Tr Extinction event. Palaeontology 51 (Therapsida, Anomodontia) species with a Pangaean distribution. Journal of Verte- (1), 215–229. brate Paleontology 28, 788–802. Gastaldo, R.A., Adendorff, R., Bamford, M., Labandeira, C.C., Neveling, J., Sims, H., 2005. Angielczyk, K.D., Roopmarine, P.D., Wang, S.C., 2005. Modeling the role of primary Taphonomic trends of macrofloral assemblages across the Permian–Triassic bound- productivity disruption in End Permian extinctions, Karoo Basin, South Africa. In: ary, Karoo Basin, South Africa. Palaios 20, 479–497. Lucas, S.G., Ziegler, K.E. (Eds.), The Nonmarine Permian, 30. Museum of Natural Gastaldo, R.A., Neveling, J.C., Kittinger, C., Newbury, S.S., 2009. The terrestrial Permian– History and Science Bulletin, New Mexico, pp. 16–23. Triassic boundary event bed is a nonevent. Geology 37, 199–202. Arakel, A.V., 1982. Genesis of calcrete in Quaternary soil profiles, Hutt and Leeman Gile, L.H., Peterson, F.F., Grossman, R.B., 1965. The K Horizon: A master soil horizon of car- lagoons, Western Australia. Journal of Sedimentary Research 52, 109–125. bonate accumulation. Soil Science 99, 47–52. Baele, J.-M., Godefroit, P., Spagna, P., Dupuis, C., 2012. Geological model and cyclic mass Giles, M.J., Soregham, M.J., Benison, K.C., Soregham, G.S., Hasiotis, S.T., 2013. Lakes, loess mortality scenarios of the Lower Cretaceous Bernissart Iguanodon bonebeds. In: and paleosols in the Permain Wellington Formation of Oklahoma, USA: implications Godefroit, P. (Ed.), Bernissart Dinosaurs and Early Cretaceous Terrestrial Ecosystems. for palaeoclimate and palaeogeography of the mid continent. Journal of Sedimentary Indiana University Press, pp. 155–167. Research 83, 825–846. Baldwin, B., Butler, C.O., 1985. Compaction curves. Bulletin American Association Petro- Hancox, J.P., Angielczyk, K.D., Rubidge, B.S., 2013. Angonisaurus and Shansiodon, leum Geology 69, 622–626. dicynodonts (Therapsida, Anomodontia) from subzone C of the Cynognathus Becker, L., Poreda, R.J., Hunt, A.G., Bunch, T.E., Rampino, M., 2001. Impact event at the assemblage zone (Middle Triassic) of South Africa. Journal of Vertebrate Permian–Triassic boundary: evidence from extraterrestrial noble gases in fullerines. Palaeontology 33, 655–676. Science 291, 1530–1533. Hotinski, R.M., Bice, K.L., Kump, L.R., Najjar, R.G., Arthur, M.A., 2001. Ocean stagnation and Behrensmeyer, A.K., 1991. Terrestrial vertebrate accumulations. In: Allison, P.A., Briggs, end-Permian anoxia. Bulletin Geological Society of America 29, 7–10. D.E.G. (Eds.), Taphonomy: Releasing the Data Locked in the Fossil Record. Topics in Huey, R.B., Ward, P.D., 2005. Hypoxia, global warming, and terrestrial Late Permian ex- Geobiology, 9, pp. 291–335. tinctions. Science 308, 398–401. Behrensmeyer, A.K., Western, D., Badgley, C., Miller, J.H., Odock, F.L., 2012. The impact of Huttenlocker, A.K., Botha-Brink, J., 2013. Body size and growth patterns in the mass mortality on the land surface bone assemblage of Amboseli Park, Kenya. Journal therocephalian Moschorhinus kitchingi (Therapsida: Eutheriodontia) before and of Vertebrate Paleontology 32, 62–63. after the end-Permian extinction in South Africa. Paleobiology 39 (2), 253–277. R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118 117

Huttenlocker, A., Sidor, C., Smith, R.M.H., 2011. A new specimen of Promoschorhynchus Sahney, S., Benton, M.J., 2008. Recovery from the most profound mass extinction of all (Therapsida: Therocephalia: Akidnognathidae) from the Early Triassic of South time. Proceedings of the Royal Society B 275, 759–765.

Africa and its implications fro theriodont survivorship across the Permo-Triassic Schaller, M.F., Wright, J.D., Kent, D.V., 2011. Atmospheric PCO2 perturbations associated boundary. Journal of Vertebrate Palaeontology 31, 405–421. with the Central Atlantic magmatic province. Science 331, 1404–1409. Irmis, R.B., Whiteside, J.H., 2012. Delayed recovery of non-marine tetrapods after the end- Sephton, M.A., Looy, C.V., Brinkhuis, H., Wignall, P.B., de Leeuw, J.W., Visscher, H., Permian mass extinction tracks global carbon cycle. Proceedings of the Royal Society 2005. Catastrophic soil erosion during the end-Permian biotic crisis. Geology B 279, 1310–1318. 33, 941–944. Irmis, R.B., Whiteside, J.H., Kammerer, C.F., 2013. Non-biotic controls of observed diversity Shelden, N.D., Retallack, G.J., 2001. Equation for compaction of paleosols. Geology 29, in the paleontologic record: an example from the Permo-Triassic Karoo Basin of 247–250. South Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 372, 62–77. Sheldon, N.D., Retallack, G.J., 2002. Low oxygen in earliest Triassic soils. Geology 30, 919–922. Isozaki, Y., 1997. Permo-Triassic boundary superanoxia and stratified superocean: records Shen, S.-Z., Crowley, J.L., Wang, Y., Bowring, S.A., Erwin, D.A., Sadler, P.M., Cao, C.-g., from lost deep sea. Science 276, 235–238. Rothman, D.H., Henderson, C.M., Ramezani, J., Zhang, H., Shen, Y., Wang, X.-d., Jablonski, D., 2002. Survival without recovery after mass extinctions. Proceedings of the Wang, W., Lin, Mu., Wen-zhong, Li, Yue-gang, Tang, Xiao-lei, Liu, Lu-jun, Liu, National Academy of Science United States of America 99, 8139–8144. Yong, Zeng, Yao-fa, Jiang, Yu-gan, Jin, 2011. Calibrating the End-Permian mass Jackson II, R.G., 1981. Sedimentology of muddy fine-grained channel deposits in extinction. Science 334, 1367–1372. meandering streams of the American middle west. Journal of Sedimentary Petrology Sidor, C.A., Vilhena, D.A., Angielczyk, K.D., Huttenlocker, A.K., Nesbitt, S.J., Peekook, B.R., 51, 1169–1192. Steyer, J.S., Smith, R.M.H., Tsuji, L.A., 2013. Provincialization of terrestrial faunas Johnson, M.R., van Vuuren, C.J., Visser, J.N.J., Cole, D.I., Wickens, H.de V., Christie, A.D.M., following the end-Permian mass extinction. Proceedings of National Academy of Roberts, D.L., Brandl, G., 2006. Sedimentary rocks of the Karoo Supergroup. In: Science 110, 8129–8133. Johnson, M.R., Anhaeusser, C.R., Thomas, R.J. (Eds.), The Geology of South Africa. Geo- Sigurdsen, T., Huttenlocker, A.K., Modesto, S.P., Rowe, T.B., Damiani, R., 2012. Reassess- logical Society of South Africa and Council for Geoscience, pp. 461–499. ment of the morphology and paleobiology of the therocephalian Tetracynodon Khadkikar, A.S., Chamyal, L.S., Ramesh, R., 2000. The character and genesis of calcrete in darti (Therapsida), and the phylogenetic relationships of Baurioidea. Journal of Verte- Late Quaternary alluvial deposits, Gujarat, western India, and its bearing on the inter- brate Paleontology 32, 1113–1134. pretation of ancient climates. Palaeogeography, Palaeoclimatology, Palaeoecology Smith, R.M.H., 1987a. Helical burrow casts of therapsid origin from the Beaufort Group 162, 239–261. (Permian) of South Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 60, King, G.M., 1993. How many species of Diictodon were there? Annals of the South African 155–170. Museum 102, 303–325. Smith, R.M.H., 1987b. Morphology and depositional history of exhumed Permian Knighton, A.D., Nanson, G.C., 2000. Waterhole form and process in the anastomosing point-bars in the southwestern Karoo, South Africa. Journal of Sedimentary channel system of Cooper Creek, Australia. Geomorphology 35, 101–117. Petrology 57, 19–29. Knoll, A.H., Bambach, R.K., Canfield, D.E., Grotzinger, J.F., 1996. Comparative Earth history Smith, R.M.H., 1990. Alluvial palaeosols and pedofacies sequences in the Permian Lower and the Late Permian mass extinction. Science 273, 452–457. Beaufort of the southwestern Karoo Basin, South Africa. Journal of Sedimentary Krull, E.S., Retallack, G.J., Campbell, H.J., Lyon, G.L., 2000. δ13C org chemostratigraphy of Petrology 60 (2), 258–276. the Permian–Triassic boundary in the Maitai Group, New Zealand: evidence for Smith, R.M.H., 1993. Vertebrate taphonomy of Late Permian floodplain deposits in the high latitude methane release. New Zealand Journal of Geology and Geophysics 43, southwestern Karoo Basin, South Africa. Palaios 8 (1), 45–67. 21–32. Smith, R.M.H., 1995. Changing fluvial environments across the Permian–Triassic boundary in Labrecque, P.A., Hubbard, S.M., Jensen, J.L., Nielsen, H., 2011. Sedimentology and strati- the Karoo Basin, South Africa, and possible causes of the extinctions. Palaeogeography, graphic architecture of a point bar deposit, Lower Cretaceous McMurray Formation, Palaeoclimatology, Palaeoecology 117, 81–104. Alberta, Canada. Bulletin of Canadian Petroleum Geology 59, 147–171. Smith, R.M.H., Botha, J., 2005. The recovery of terrestrial vertebrate diversity in South Leeder, M.R., 1975. Pedogenic carbonates and flood sedimentation rates: a quantitative African Karoo basin after the End-Permian extinction. Comptes Rendus Palevol 4, model for alluvial arid zone lithofacies. Geological Magazine 112, 257–270. 555–568. Looy, C.V., Twitchett, R.J., Dilcher, D.L., van Kojnijnenberg-van Cittert, J.H.A., Visscher, H., Smith, R.M.H., Botha-Brink, J., 2009. Burrowing as a survival strategy in the earliest Triassic 2001. Life in the end-Permian dead zone. Proceedings of the National Academy of Karoo Basin, South Africa. Abs. Society of Vertebrate Palaeontology Annual Meeting, Sciences of the United States of America 98, 7879–7883. Bristol, England. Jounal of Vertebrate Palaeontology 29, 183A. Lucas, S.G., 2002. Tetrapods and the subdivision of Permian time. Carboniferous and Smith, R.M.H., MacLeod, K.G., 1998. Sedimentology and carbon isotope stratigraphy Permian of the World. In: Hills, L.V., Henderson, C.M., Bamber, E.W. (Eds.), Canadian across the Permian–Triassic boundary in the Karoo Basin, South Africa. Abstracts of Society of Petroleum Geologists Memoir, Calgary, 19, pp. 479–491. Society of Vertebrate Palaeontology Annual Meeting, Snowbird, Utah. Journal Verte- Macleod, G.K., Smith, R.M.H., Koch, P.L., Ward, P.D., 2000. Timing of mammal-like rep- brate Palaeontology 18 (3), 79A. tile extinctions across the Permian Triassic boundary in South Africa. Geology 28, Smith, R.M.H., Ward, P.D., 2001. Pattern of vertebrate extinctions across an event bed at 227–230. the Permian–Triassic boundary in the Karoo Basin of South Africa. Geological Society Magee, J.W., Miller, G.H., Spooner, N.A., Questiaux, D., 2004. Continuous150 k.y. monsoon of America Bulletin 29, 1147–1150. record from Lake Eyre, Australia: insolation-forcing implications and unexpected Smith, R.M.H., Rubidge, B.S., Van Der Walt, M., 2012. Therapsid biodiversity patterns and Holocene failure. Geology 32, 885–888. paleoenvironments of the Karoo Basin, South Africa. In: Chinsamy-Turan, A. (Ed.), Modesto, S.P., Botha-Brink, J., 2010. AburrowcastwithLystrosaurus skeletal remains from Forerunners of Mammals: Radiation, Histology. Biology. Indiana University Press, the Lower Triassic of South Africa. Palaios 24, 274–281. Bloomington, U.S., pp. 223–246. Nesbitt, S.J., Barrett, P.M., Werning, S., Sidor, C.A., Charig, A.J., 2012. The oldest dinosaur? A Spencer, L.M., Van Valkenburgh, B., Harris, J.M., 2003. Taphonomic analysis of large mam- Middle Triassic dinosauriform from Tanzania. Biology Letters 9, 201–209. mals recovered from the Pleistocene Rancho La Brea tar seeps. Paleobiology 29, Newell, A.J., Sennikov, A.G., Benton, M.J., Molostovskaya, I.I., Golubev, V.K., Minikh, A.V., 561–575. Minikh, M.G., 2010. Disruption of playa–lacustrine depositional systems at the Steiner, M., Eshet, Y., Rampino, M.R., Schwindt, D.M., 2003. Fungal abundance spike and the Permo-Triassic boundary: evidence from Vyazniki and Gorokhovets on the Russian Permian–Triassic boundary in the Karoo Supergroup (South Africa). Palaeogeography, Platform. Journal of the Geological Society (London) 167, 695–716. Palaeoclimatology, Palaeoecology 194, 405–414. Pickup, G., 1991. Event frequency and landscape stability on the floodplain systems of arid Sullivan, C., Reisz, R.R., 2005. Cranial anatomy and taxonomy of the Late Permian dicyno- central Australia. Quaternary Science Reviews 10, 463–473. dont Diictodon. Annals of the Carnegie Museum 74, 45–75. Pysklywec, R.N., Mitrovica, J.X., 1999. The role of subduction-induced subsidence in the Sullivan, C., Reisz, R., Smith, R.M.H., 2003. The Permian mammal-like herbivore Diictodon, evolution of the Karoo basin. Journal of Geology 107, 155–164. the oldest known example of sexually dimorphic armament. Proceedings of the Royal Ray, S., Chinsamy, A., 2004. Diictodon feliceps (Therapsida, Dicynodontia): bone histology, Society of London B 270, 173–178. growth, and biomechanics. Journal of Vertebrate Paleontology 24, 180–194. Tabor,N.J.,Montañez,I.P.,Steiner,M.B.,Schwindt,D.,2007.δ13Cvaluesofcarbonate Renne, P.R., Zichao, Z., Richards, M.A., Black, M.A., Basu, A.R., 1995. Synchrony and causal nodules across the Permian–Triassic boundary in the Karoo Supergroup (South relations between Permian–Triassic boundary crises and Siberian flood volcanism. Africa) reflect a stinking sulfurous swamp, not atmospheric CO2. Palaeogeography, Science 269, 1413–1416. Palaeoclimatology, Palaeoecology 252, 370–381. Retallack, G.J., Smith, R.M.H., Ward, P.D., 2003. Vertebrate extinction across Permian– Talbot, M.R., Holm, K., Williams, M.A.J., 1994. Sedimentation in low-gradient desert mar- Triassic boundary in Karoo Basin, South Africa. Geological Society of America Bulletin gin systems: A comparison of the Late Triassic of northwest Somerset (England) and 115, 1133–1152. the late Quaternary of east-central Australia. Geological Society America Special Pa- Rogers, R.R., Kidwell, S., 2010. A conceptual framework for the genesis and analysis of pers 289, 97–117. skeletal concentrations. In: Rogers, R.R., Eberth, D.A., Fiorillo, A.R. (Eds.), Bonebeds: Tankard, A., Welsink, H., Aukes, P., Newton, R., Stettler, E., 2009. Tectonic evolution of the Cape Genesis, Analysis, and Paleobiological Significance. Chicago University Press, pp. 1–64. and Karoo basins of South Africa. Marine and Petroleum Geology 26, 1379–1412. Roopnarine, P.D., Angielczyk, K.D., 2012. The evolutionary palaeoecology of species and Tohver, E., Lana, C., Cawood, P.A., Fletcher, I.R., Jourdan, F., Sherlock, S., Rasmussen, B., the tragedy of the commons. Biology Letters 8, 147–150. Trindale, R.I.F., Yokoyama, E., Souza Filho, C.R., Marageni, Y., 2012. Geochronological Roopnarine, P.D., Angielczyk, K.D., Wang, S.C., Hertog, R., 2007. Trophic network models constraints on the age of a Permo-Triassic impact event: U–Pb and 40Ar/39Ar results explain instability of Early Triassic terrestrial communities. Proceedings of the Royal for the 40 km Arguainha structure of central Brazil. Geochimica et Cosmochimica Society B 274, 2077–2086. Acta 86, 214–227. Ruta, M., Angielczyk, K.D., Frobisch, J., Benton, M.J., 2013a. Decoupling of morphological Tucker, M.E., 1978. Triassic lacustrine sediments from South Wales: shore-zone clastics, disparity and taxic diversity during the adaptive radiation of anomodont therapsids. evaporites and carbonates. In: Matter, A., Tucker, M.E. (Eds.), Modern and Ancient Proceedings of the Royal Society B 280. http://dx.doi.org/10.1098/rspb.2013.1071. Lake Sediments. Blackwell, Oxford, pp. 205–224. Ruta, M., Botha-Brink, J., Mitchell, S.A., Benton, M.J., 2013b. The radiation of cynodonts and Tunbridge, I.P., 1984. Facies model for a sandy ephemeral stream and clay playa complex; the ground plan for mammalian morphological diversity. Proceedings of the Royal the Middle Devonian Trentishoe Formation of North Devon, U.K. Sedimentology 31, Society B. http://dx.doi.org/10.1098/rspb.2013.1865. 697–715. 118 R.M.H. Smith, J. Botha-Brink / Palaeogeography, Palaeoclimatology, Palaeoecology 396 (2014) 99–118

Viglietti, P.A., Smith, R.M.H., Compton, J.S., 2013. Lystrosaurus bonebed origins and their Ward, P.D., Botha, J., Buick, R., Dekock, M.O., Erwin, D.H., Garrison, G., Kirschvink, J., Smith, palaeoenvironmental implications for the earliest Triassic Karoo Basin, South Africa. R.H.M., 2005. Abrupt and gradual extinction among Late Permian land vertebrates in Palaeogeography, Palaeoclimatology, Palaeoecology 392, 9–21. the Karoo Basin, South Africa. Science 307, 709–714. Wang, K., Geldsetzer, H.H.J., Krouse, H.R., 1994. Permian–Triassic extinction: organic S13C Ward, P.D., Retallack, G.J., Smith, R.M.H., 2012. The terrestrial Permo-Triassic event bed is evidence from British Columbia, Canada. Geology 22, 580–584. a non-event comment. Geology 40, 256. Ward, P.D., Montgomery, D.R., Smith, R.M.H., 2000. Altered river morphology in South Wignall, P.B., Twitchett, R.J., 1996. Oceanic anoxia and the end-Permian mass extinction. Africa related to the Permian–Triassic Extinction. Science 289, 1740–1743. Science 272, 1155–1158.