Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-18T01:20:21.189Z Has data issue: false hasContentIssue false
  • English
  • Français

A test of Bergmann's rule in the Early Triassic: latitude, body size, and sampling in Lystrosaurus

Published online by Cambridge University Press:  21 September 2022

Zoe T. Kulik Open the ORCID record for Zoe T. Kulik [Opens in a new window]  and
Christian A. Sidor
Zoe T. Kulik*
Affiliation:
Department of Biology and Burke Museum, University of Washington, Seattle, Washington 98195, U.S.A. E-mail: zkulik@uw.edu, casidor@uw.edu
Christian A. Sidor
Affiliation:
Department of Biology and Burke Museum, University of Washington, Seattle, Washington 98195, U.S.A. E-mail: zkulik@uw.edu, casidor@uw.edu
*
*Corresponding author.
Rights & Permissions [Opens in a new window]

Abstract

The ecogeographic rule known as Bergmann's rule suggests that there is a positive relationship between body size and latitude when comparing closely related taxa. The underlying mechanism or mechanisms to explain this pattern vary as widely as the taxa that seem to follow it, which has led to skepticism over whether Bergmann's rule should be considered a rule at all. Despite this, Bergmann's rule is widespread among modern birds, mammals, beetles, and some amphibians, but far fewer extinct taxa have been subjected to tests of Bergmann's rule. To examine whether Bergmann's rule is detected in extinct taxa, we compared body-size proxies in Lystrosaurus recovered from Early Triassic–aged strata in Antarctica, South Africa, India, and China. Our results reveal that average body size is largest at mid-northern paleolatitudes (~45°N) instead of the highest southern paleolatitudes (~70°S). Additionally, maximum body size is consistent across the Northern and Southern Hemispheres, indicating that Bergmann's rule did not apply for Lystrosaurus during the Early Triassic. To test potential sample size biases in our results, we used rarefaction and subsampling to show that only the Karoo Basin is well sampled and that large individuals are exceedingly rare, except in the Turpan-Junggar Basin of Xinjiang, China. Taken together, our results suggest that Lystrosaurus had the potential to reach large body sizes in each of the latitudinally widespread geologic basins studied here, but that local conditions may have allowed individuals at mid-northern paleolatitudes a greater chance of reaching a large size compared with southern congeners that suffered increased mortality when young or at a small size.

Type
Articles
Information
Paleobiology , Volume 49 , Issue 1 , February 2023 , pp. 53 - 67
Check for updates
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of The Paleontological Society

Introduction

Macroecological patterns in body size are well documented for a wide variety of extant taxa, including endotherms and ectotherms in terrestrial, freshwater, and marine habitats worldwide (Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Ashton Reference Ashton2002; Belk and Houston Reference Belk and Houston2002; Ashton and Feldman Reference Ashton and Feldman2003; Chown and Gaston Reference Chown and Gaston2010; Berke et al. Reference Berke, Jablonski, Krug, Roy and Tomasovych2013; Angielczyk et al. Reference Angielczyk, Burroughs and Feldman2015; Gohli and Voje Reference Gohli and Voje2016; Blackburn et al. Reference Blackburn, Redding and Dyer2019). Of these, the most commonly observed pattern conforms to Bergmann's rule, after Carl Bergmann, who described a relationship where larger body sizes are seen in species that live in colder climates compared with their smaller-bodied relatives that live in warmer climates (Reference Bergmann1847; see translation by James Reference James1970). Because the definition of the rule is itself a reformulated translation that has since been reinterpreted by various authors (e.g., Rensch Reference Rensch1938; Mayr Reference Mayr1963; James Reference James1970; Blackburn et al. Reference Blackburn, Gaston and Loder1999; Salewski and Watt Reference Salewski and Watt2017) and because no underlying mechanism is as widespread as the taxa that seem to follow it, the validity of Bergmann's rule has long been debated (Mayr Reference Mayr1956; McNab Reference McNab1971, Reference McNab2010; Blackburn et al. Reference Blackburn, Gaston and Loder1999; Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Meiri and Dayan Reference Meiri and Dayan2003; Meiri et al. Reference Meiri, Yom-Tov and Geffen2007; Watt et al. Reference Watt, Mitchell and Salewski2010; Salewski and Watt Reference Salewski and Watt2017). The classical interpretation of Bergmann's rule is that larger endothermic animals withstand cold temperatures better by having a reduced surface to volume ratio (James Reference James1970). However, many studies have used definitions of Bergmann's rule that do not include a specific physiological mechanism or indeed any explicit underlying process: namely, that body size is positively correlated with latitude (Blackburn and Gaston Reference Blackburn and Gaston1996; Blackburn and Ruggiero Reference Blackburn and Ruggiero2001; Ashton Reference Ashton2002; Montgomery et al. Reference Montgomery, Mackessy and Moore2003; Meiri et al. Reference Meiri, Dayan and Simberloff2004).

Size–latitude relationships are a common test of Bergmann's rule, as climate is assumed to be colder at higher latitudes, although this correlation may be weak at small scales (Mayr Reference Mayr1963; Blackburn et al. Reference Blackburn, Gaston and Loder1999) or absent during times in Earth history with reduced temperature gradients from equator to poles. Importantly, latitude does not affect body size directly but is likely to correlate with body-size clines, because it encompasses more precise predictive variables that fluctuate over temporal and spatial scales to affect body size (reviewed in Yom-Tov and Geffen Reference Yom-Tov and Geffen2011). Indeed, body size has been shown to vary in response to precipitation (Nwaogu et al. Reference Nwaogu, Tieleman, Bitrus and Cresswell2018), elevation (Feder et al. Reference Feder, Papenfuss and Wake1982; Yu et al. Reference Yu, Wang, Busam and Deng2019), water depth (Timofeev Reference Timofeev2001), seasonality (James Reference James1970; Murphy Reference Murphy1985; Wells et al. Reference Wells, Saunders, Lea, Cortina-Borja and Shirley2019), geographic-range size (Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Rodríguez et al. Reference Rodríguez, Olalla-Tárraga and Hawkins2008), resource availability (McNab Reference McNab2010; Correll et al. Reference Correll, Prowse and Prideaux2016; Brown et al. Reference Brown, Kotler and Porter2017; Kelly et al. Reference Kelly, Friedman and Santana2018), functional traits (Briscoe et al. Reference Briscoe, Krockenberger, Handasyde and Kearney2015), or predation risk and prey size (McNab Reference McNab1971), with only some correlations supporting a Bergmann-like pattern (e.g., Murphy Reference Murphy1985; Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Timofeev Reference Timofeev2001; Rodríguez et al. Reference Rodríguez, Olalla-Tárraga and Hawkins2008; Briscoe et al. Reference Briscoe, Krockenberger, Handasyde and Kearney2015; Correll et al. Reference Correll, Prowse and Prideaux2016; Nwaogu et al. Reference Nwaogu, Tieleman, Bitrus and Cresswell2018; Yu et al. Reference Yu, Wang, Busam and Deng2019).

Tests for Bergmann's rule at different taxonomic scales can also give different results, with interspecific analyses obscuring intraspecific patterns that may be better explained by the specific variables mentioned previously, rather than latitude alone (e.g., Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Freckleton et al. Reference Freckleton, Harvey and Pagel2003; Gohli and Voje Reference Gohli and Voje2016; Pallarés et al. Reference Pallarés, Lai, Abellán, Ribera and Sánchez-Fernández2019; Romano et al. Reference Romano, Séchaud and Roulin2021). Nonetheless, modern birds, mammals, and salamanders generally show support for Bergmann's rule when average body sizes of numerous species are compared across a wide latitudinal range (mammals: Ashton et al. Reference Ashton, Tracy and de Queiroz2000; Meiri et al. Reference Meiri, Dayan and Simberloff2004; birds: Blackburn and Gaston Reference Blackburn and Gaston1996; salamanders: Ashton Reference Ashton2002). Modern turtles and frogs also follow a Bergmann-like pattern, although species sampling is comparatively scarce (Ashton Reference Ashton2002; Ashton and Feldman Reference Ashton and Feldman2003). Extant squamates tend to show the converse of Bergmann's rule, that body size decreases in colder climates (Ashton and Feldman Reference Ashton and Feldman2003); however, others argue that no spatial pattern in body size is seen (Pincheira-Donoso and Meiri Reference Pincheira-Donoso and Meiri2013; Slavenko et al. Reference Slavenko, Feldman, Allison, Bauer, Böhm, Chirio and Colli2019). Interestingly, many more taxa should follow Bergmann's rule, according to estimates using ancestral-state reconstructions among major tetrapod groups (de Queiroz and Ashton Reference Queiroz and Ashton2004). This provocative result may imply that the tendency to develop Bergmann-like clines is a shared pattern that is deeply nested in the evolutionary history of endothermic and ectothermic tetrapods (de Queiroz and Ashton Reference Queiroz and Ashton2004).

Bergmann's Rule in the Fossil Record

While Bergmann's rule is certainly widespread among extant taxa, comparatively few investigations have looked for similar results in the fossil record. Pterosaurs show the converse of Bergmann's rule during the Cretaceous and do not follow size–latitude clines during the Triassic–Jurassic (Villabolos et al. Reference Villabolos, Olalla-Tarraga, Vieira, Mazzei and Bini2017). Bivalve size distributions remain remarkably consistent across a global latitudinal distribution during the Miocene–Recent (Roy et al. Reference Roy, Jablonski and Martien2000). Similar investigations that focus on comparisons between extant and extinct members of the same clade within the same latitudinal region approximate tests for Bergmann's rule from a climatically driven standpoint but do not test for size–latitude patterns outright. For example, comparisons between Eocene–Recent Antarctic penguins, Pleistocene–Recent coyotes across North America, and equids, canids, and sciurids from the Oligo-Miocene of the northwest United States test for climate-driven patterns in body size (Jadwiszczak Reference Jadwiszczak2001; Orcutt and Hopkins Reference Orcutt and Hopkins2013; Meachen et al. Reference Meachen, Janowicz, Avery and Sadleir2014). These studies, while not a direct comparison of latitudinally driven changes in body size, indicate that penguin average body size tends to be larger in extinct taxa but that the underlying mechanism may be due to an adaptive radiation rather than warmer climates (Jadwiszczak Reference Jadwiszczak2001). Body-size trends are highly variable among North American mammals studied thus far, with coyotes showing a decrease from larger than Recent average size across the Pleistocene/Holocene boundary, perhaps due to species interactions and niche partitioning (Meachen et al. Reference Meachen, Janowicz, Avery and Sadleir2014). Equid, canid, and sciurid body-size variation during the Oligo-Miocene shows no consistent relationship with climate variables, nor were trends similar between orders (Orcutt and Hopkins Reference Orcutt and Hopkins2013). Taken together, investigations into the potential drivers of body-size patterns in the fossil record have yielded highly variable results. For the few taxa that have been studied during the Cenozoic, inferred climate variables do not have significant relationships to body-size variation, counter to what has been shown in modern ecosystems. Indeed, times in Earth history with a decreased temperature gradient from equator-to-pole may have removed key factors underlying Bergmann's rule. One extreme example of this is the earliest Triassic, where elevated CO2 levels, globally high sea level, and ice-free polar regions intensified global climate extremes across the supercontinent of Pangea (Kidder and Worsley Reference Kidder and Worsley2004; Winguth et al. Reference Winguth, Shields and Winguth2015; Mancuso et al. Reference Mancuso, Horn, Benavente, Schultz and Irmis2021).

A prime candidate for a test of Bergmann's rule in the fossil record is Lystrosaurus, a non-mammalian synapsid that survived the end-Permian mass extinction and rose to remarkable abundance across much of Pangea during the Early Triassic (King Reference King1990; Grine et al. Reference Grine, Forster, Cluver, Georgi, Carrano, Gaudin, Blob and Wible2006). Indeed, Lystrosaurus is exceptional among fossil tetrapods, because it is a globally distributed genus known from a relatively short time interval (~3 Myr). Fossils of Lystrosaurus have been recovered in Early Triassic–aged strata in South Africa, Antarctica, Mongolia, Russia, China, India, and possibly Australia and Mozambique (e.g., Tripathi and Puri Reference Tripathi and Puri1961; Colbert Reference Colbert1974; Sun Reference Sun1980; Thulborn Reference Thulborn1990; Gubin and Sinitza Reference Gubin, Sinitza, Lucas and Morales1993; Liu et al. Reference Liu, Li and Cheng2002; Ray Reference Ray2005; Botha and Smith Reference Botha and Smith2007; Araújo et al. Reference Araújo, Smith, Tolan, Angielczyk, Crowley, Milisse and Mugabe2020; Viglietti et al. Reference Viglietti, Benson, Smith, Botha, Kammerer, Skosan and Butler2021) (Fig. 1). Besides having a near-global distribution, Lystrosaurus is also remarkably abundant, especially in South Africa, where more than 2500 specimens are cataloged into museum collections (Smith et al. Reference Smith, Rubidge, van der Walt and Chinsamy-Turan2012).

Figure 1. Geographic distribution of Lystrosaurus fossils sampled. Paleogeographic map of the Early Triassic with estimated locations of geologic basins denoted by stars; sampled localities are labeled and filled in orange; unsampled localities are open. Paleomap modified from Scotese (Reference Scotese2016). Lystrosaurus silhouette from Phylopic.org.

Here, we examine whether body-size proxies vary predictably with paleolatitude in Triassic species of Lystrosaurus. Our sample includes nearly 500 specimens recovered from four basins that span a range of paleolatitudes from approximately 73°S–55°S and ~45°N (van Hinsbergen et al. Reference Hinsbergen, de Groot, van Schaik, Spakman, Bijl, Sluijs, Langereis and Brinkhuis2015; Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021) (Fig. 1). This sample spans the entirety of all known Early Triassic–aged deposits, but unfortunately, Lystrosaurus-bearing strata from equatorial regions are lacking. If Lystrosaurus followed a size–latitude pattern consistent with Bergmann's rule, the largest specimens would be expected from the highest southern paleolatitudes (i.e., the Transantarctic Basin of Antarctica). If some other body-size cline is detected, this could indicate that Lystrosaurus is an exception to the rule, along with modern lizards and snakes. If, however, no size–latitude pattern is detected, sampling inconsistencies between Early Triassic basins could play a role in overprinting potential patterns. Finally, a failure to detect body-size clines in Lystrosaurus could also imply a previously unrecognized macroevolutionary consequence of climatic warming.

Data Collection and Analysis

Distribution of Lystrosaurus Species across Pangea

Lystrosaurus is found in Early Triassic–aged strata on every continent except North and South America (Tripathi and Puri Reference Tripathi and Puri1961; Colbert Reference Colbert1974; Sun Reference Sun1980; Thulborn Reference Thulborn1990; Gubin and Sinitza Reference Gubin, Sinitza, Lucas and Morales1993; Liu et al. Reference Liu, Li and Cheng2002; Ray Reference Ray2005; Botha and Smith Reference Botha and Smith2007; Araújo et al. Reference Araújo, Smith, Tolan, Angielczyk, Crowley, Milisse and Mugabe2020; Viglietti et al. Reference Viglietti, Benson, Smith, Botha, Kammerer, Skosan and Butler2021). Species-specific distributions are more clearly defined from southern Pangean deposits, where the most recent systematic appraisal of Lystrosaurus recognized four valid species in South Africa: Lystrosaurus maccaigi, Lystrosaurus curvatus, Lystrosaurus murrayi, and Lystrosaurus declivis (Grine et al. Reference Grine, Forster, Cluver, Georgi, Carrano, Gaudin, Blob and Wible2006). These four species have been used in numerous studies since (e.g., Botha and Smith Reference Botha and Smith2007; Botha-Brink et al. Reference Botha-Brink, Codron, Huttenlocker, Angielczyk and Ruta2016; Botha Reference Botha2020). All four species occur in varying abundances across southern Pangea, except for L. maccaigi, which is only found in South Africa and Antarctica (Colbert Reference Colbert1974; Peecook et al. Reference Peecook, Smith and Sidor2019), and L. declivis, which is currently only recognized from South Africa and India (Gupta and Das Reference Gupta and Das2011).

Within the Karoo Basin of South Africa, L. curvatus is the rarest species followed by L. maccaigi. These species are locally considered Permian taxa but likely survived during the extinction interval based on in situ specimens found in strata within the lithologic boundary of the vertebrate-defined Permo-Triassic boundary (Botha-Brink et al. Reference Botha-Brink, Huttenlocker, Modesto, Kammerer, Angielczyk and Fröbisch2014; Viglietti et al. Reference Viglietti, Benson, Smith, Botha, Kammerer, Skosan and Butler2021). Additionally, L. maccaigi and L. curvatus are found in the lower Fremouw Formation of Antarctica, indicating that these species persisted at higher latitudes in the Early Triassic (Colbert Reference Colbert1974; Collinson et al. Reference Collinson, Hammer, Askin and Elliot2006; Peecook et al. Reference Peecook, Smith and Sidor2019).

In contrast to the sparse occurrences of L. maccaigi and L. curvatus, thousands of specimens of L. murrayi and L. declivis have been recovered from the lowermost Triassic of the Karoo Basin, the more abundant L. declivis giving its name to the assemblage zone that typifies the faunal assemblage immediately after the end-Permian mass extinction (Botha and Smith Reference Botha and Smith2020). Lystrosaurus murrayi is also known in Antarctica and India (Colbert Reference Colbert1974; Ray Reference Ray2005; Peecook et al. Reference Peecook, Smith and Sidor2019). Two specimens referred to L. curvatus and one to L. declivis have also been recovered from the Panchet Formation in the Damodar Basin of India, further suggesting the cosmopolitan distribution of all four species across southern Pangea (Gupta and Das Reference Gupta and Das2011).

In the greater Turpan-Junggar Basin of Xinjiang, China, numerous species of Lystrosaurus have been described, including Lystrosaurus youngi, Lystrosaurus robustus, Lystrosaurus latifrons, and Lystrosaurus hedini, which has also been found in Mongolia (Yuan and Young Reference Yuan and Young1934; Young Reference Young1939; Sun Reference Sun1964, Reference Sun1973; Gubin and Sinitza Reference Gubin, Sinitza, Lucas and Morales1993; Liu et al. Reference Liu, Li and Cheng2002). Cosgriff et al. (Reference Cosgriff, Hammer and Ryan1982) suggested that some of the northern Pangean forms were likely synonymous with L. murrayi. More recently, work by Camp and Liu (Reference Camp and Liu2011) and Kulik et al. (Reference Kulik, Lungmus, Angielczyk and Sidor2021), has shown that Chinese specimens have significantly different cranial morphologies compared with South African specimens. Therefore, it is unlikely that northern Pangean species are synonymous with southern species. Furthermore, is it not currently possible to provide a reliable taxonomic assignment to Chinese specimens, as additional work is needed to clarify the number of valid taxa there, as well as in Russia (Surkov et al. Reference Surkov, Kalandadze and Benton2005). For our analysis, we refer to all species recovered from China as Lystrosaurus sp.

Body-Size Proxies

We gathered cranial measurements from 482 skulls to compare body-size proxies from Early Triassic specimens of Lystrosaurus. Nine specimens were from the Transantarctic Basin of Antarctica, 411 were from the Karoo Basin of South Africa, 27 were from the Damodar Basin of India, and 35 were from the Turpan-Junggar Basin of China (see Supplementary Material for associated data). Specimens were selected to best represent the maximum distribution of Lystrosaurus skull size from all known Early Triassic localities. Paleolatitude was estimated from tectonic plate reconstructions made available through the online calculator developed by van Hinsbergen et al. (Reference Hinsbergen, de Groot, van Schaik, Spakman, Bijl, Sluijs, Langereis and Brinkhuis2015) and range from approximately 73°S–55°S and ~45°N (van Hinsbergen et al. Reference Hinsbergen, de Groot, van Schaik, Spakman, Bijl, Sluijs, Langereis and Brinkhuis2015; Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). These ranges were reconstructed from the basins preserving Early Triassic Lystrosaurus, but importantly lack records from low paleolatitudes (Romano et al. Reference Romano, Bernardi, Petti, Rubidge, Hancox and Benton2020). Indeed, the Triassic terrestrial fossil record is exceedingly sparse from low paleolatitudes, which complicates our understanding of Pangean species’ distributions but does not preclude an assessment of body sizes at high-southern and mid-northern paleolatitudes.

We selected cranial measurements that were easily identifiable, reproducible, and most often free of encasing matrix (i.e., the interorbital region and snout are often prepared, because they provide taxonomically informative details for species-level identification). As shown in Figure 2, these include: (1) basal skull length, as measured from the anterior extremity of the snout to the occipital condyle; (2) minimum interorbital width; and (3) tusk diameter at its point of eruption from the maxilla (averaged when both tusks could be measured). When skulls were not sufficiently prepared or were incomplete, we measured the dorsal snout length, as a midline horizontal line from the anteriormost point of the parietal foramen to the anterior extent of the premaxilla, and/or dorsal skull length, as a midline horizontal line from the anterior extent of the premaxilla to the posterior end of the parietal. Linear regressions were computed based on complete and prepared specimens of the four southern Pangean species to estimate basal skull length in specimens that were incomplete or not completely prepared. Skulls that were crushed, distorted, or too fragmentary were excluded from our analysis.

Figure 2. Cranial measurements used to estimate body size in Lystrosaurus. A, Minimum interorbital width, B, basal skull length, C, tusk diameter at eruption, and D, dorsal snout length and dorsal skull length were measured from incompletely prepared or broken specimens. Abbreviations: f, frontal; p, premaxilla. Skull drawings adapted from King (Reference King1990).

Measurements were taken using Mitutoyo digital calipers (±0.02 mm) at the following institutions: Burke Museum of Natural History and Culture, Washington, U.S.A.; American Museum of Natural History, New York, U.S.A.; Evolutionary Studies Institute (formerly Bernard Price Institute for Paleontological Research), University of the Witwatersrand, Johannesburg, South Africa; the Field Museum of Natural History, Chicago, Illinois, U.S.A.; Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China; National Museum, Bloemfontein, South Africa; and Iziko, the South African Museum, Cape Town, South Africa. Measurement data were also compiled from a survey of the literature (Ray Reference Ray2005; Gupta and Das Reference Gupta and Das2011; Botha Reference Botha2020; see Supplementary Material). All subsequent data manipulations and visualizations were carried out in R (v. 2022.02.0).

Testing for Bergmann's Rule

We assessed whether Lystrosaurus body-size proxies varied with paleolatitude by comparing average basal skull length and average tusk diameter between interspecific samples binned into the four basins included in our study (Fig. 3). Interspecific averages could be influenced by species-specific body-size distributions in Lystrosaurus, particularly because each species overlaps in its body-size range with at least one other species. For example, L. murrayi has a maximum known size of 21.3 cm (BP/1/ 3236), whereas L. curvatus has a maximum known size of 20 cm (BP/1/ 3976). To account for species-specific differences in body size, we standardized basal skull length and tusk diameter as a proportion of the maximum known size per species. We treated the unidentified southern Pangean specimens as a unique species (Lystrosaurus sp. indet.), which corresponds to a grouping of small skulls that are most likely unidentifiable to the species level because they lack developed diagnostic features. Similarly, we treated Chinese Lystrosaurus sp. as a separate species and computed proportional skull and tusk size accordingly.

Figure 3. Plots comparing Lystrosaurus size and geographic position using: A, basal skull length; B, standardized basal skull length as a percent of maximum size; C, tusk diameter; and D, standardized tusk diameter. Lystrosaurus does not follow a pattern that is consistent with Bergmann's rule. Skull size is significantly larger in the midlatitude Turpan-Junggar Basin and greater in the Karoo Basin than in the Damodar Basin. Red diamonds and gray bars indicate the mean and median values, respectively.

Results

Considering both raw and standardized body size across geologic basins, Lystrosaurus body-size proxies do not vary with paleolatitude in a pattern that is consistent with Bergmann's rule (Fig. 3). The largest average skull and tusk sizes are from Lystrosaurus specimens from the Turpan-Junggar Basin, which have an estimated paleolatitude of ~45°N (Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). Indeed, average basal skull length and tusk diameter are between 16% and 17% larger in the Turpan-Junggar Basin compared with southern congeners. However, when only the basins in the Southern Hemisphere are considered, average skull and tusk size increase toward the pole (Fig. 3). These results, however, are not statistically significant at high paleolatitudes between the Karoo (~55°S–65°S) and Transantarctic Basins (~65°S–70°S) (t = 0.87124, df = 8.0759, p = 0.4088). Interestingly, mean tusk diameter and basal skull length are significantly smaller in the Damodar Basin when compared with the Karoo dataset (tusk: t = −8.4281, df = 37.01, p < 0.05; skull: t = −7.0031, df = 37.384, p < 0.05).

Based on these results, it is possible that intraspecific differences in maximum size could be driving the pattern of large specimens (i.e., large species) in high southern paleolatitudes. To address this, we compared species-specific average body size across southern Pangean basins and show that Bergmann's rule is not detected (Fig. 4). Median body size remains constant across southern Pangean species, except for large Lystrosaurus maccaigi from the Transantarctic Basin, which are much larger than the median size from the Karoo Basin. However, maximum size is remarkably similar across both basins. Indeed, interspecific maximum size is comparable across the Transantarctic, Karoo, and Turpan-Junggar Basins (between 22 and 28 cm), indicating that Lystrosaurus species in both the Northern and Southern Hemispheres could reach similar large sizes (Figs. 3, 5). However, the frequency of large Lystrosaurus specimens is highest in the Northern Hemisphere, as most sampled individuals are larger than ~50% maximum known size (Fig. 5). This is in contrast to the Karoo Basin, where the highest frequency of skulls is less than 50% maximum known size. Importantly, the Karoo Basin dataset is an order of magnitude larger than those of the other basins, which prompts us to consider the effects that different sample sizes have on average body size in Lystrosaurus.

Figure 4. Plots comparing skull length in four species of Lystrosaurus against geographic position. At the species level, median body size remains constant between Triassic basins, except for Lystrosaurus maccaigi; note that the outlier from the Karoo Basin is approximately the same size as the individuals from the Transantarctic Basin.

Figure 5. Distributions of skull size of Lystrosaurus collected from four geographic areas. A, interspecific Lystrosaurus basal skull length (BSL) and proportional skull size (%BSL max) in the Transantarctic Basin, B, normally distributed skull size in the Karoo Basin, C, right-skewed distribution in the Damodar Basin, and D, left-skewed distribution in the Turpan-Junggar Basin when skull length is standardized as a proportion of the maximum known size per species.

Assessing Sampling Bias through Resampling

Despite Lystrosaurus being one of the most abundant terrestrial fossils found in Early Triassic–aged strata, substantial differences exist in the number of specimens recovered outside the Karoo Basin. To assess how different sample sizes could be affecting our results, we subsampled the Karoo Basin dataset to the size of the other basins, respectively. We then tested for statistically significant differences between the downsampled Karoo dataset and the remaining datasets from the other basins. In addition, we also calculated the probability of recovering the largest known skull when the Karoo dataset was downsampled to further demonstrate the rarity of large sizes known from the Karoo Basin. We found that there is a 7% probability of recovering the maximum known skull size when the Karoo Basin dataset is reduced to the sample size of the Damodar or Turpan-Junggar Basin and only a 2% probability of recovering the largest individual when the Karoo is downsampled to the size of the Transantarctic Basin. We then tested whether average body-size proxies (i.e., basal skull length and tusk diameter) were significantly different between the downsampled Karoo dataset and the datasets from other basins using Welch's t-test of unequal variance. Average skull and tusk size were similarly not significantly larger between the Transantarctic Basin and downsampled Karoo Basin (t = −0.89094, df = 8.0035, p = 0.399), consistent with the raw and standardized results reported earlier. In addition, body-size proxies from the Damodar Basin remained significantly smaller when compared with the downsampled Karoo dataset (t = 7.5418, df = 26.176, p > 0.05). These results indicate a significant difference in body size between basins at relatively high southern paleolatitudes (~50°S–65°S) but not between these basins and the most poleward sample in our dataset, which is not consistent with the predictions of Bergmann's rule. However, comparisons between downsampled results remove much of the available data. Therefore, we employed rarefaction methods to extrapolate body-size abundance at larger sample sizes.

Assessing Sampling Bias Using Rarefaction

To test the effects that different sample sizes had on body-size distributions without reducing sample sizes to the smallest dataset in our results, we employed rarefaction methods originally developed to assess species diversity from unequal sample sizes. This provides a new approach to estimate whether body sizes are likely to remain large if more specimens were recovered from the Turpan-Junggar Basin, or conversely, specimens are likely to remain small if more were recovered from the Damodar Basin. To investigate whether body-size distributions are likely to remain consistent when sample sizes are increased, diversity metrics (i.e., richness, Shannon diversity, and Simpson diversity) were used to calculate rarefaction curves using the R package iNEXT (Hsieh et al. Reference Hsieh, Ma and Chao2016). This method is preferred over traditional rarefaction methods, because it does not reduce sample sizes. Importantly, diversity metric calculations are iterated over numerous sample sizes and are typically reliable to twice that of the reference sample (Chao and Jost Reference Chao and Jost2012). Unfortunately, this does not allow comparisons between equal sample sizes in our dataset, as the doubled Transantarctic Basin sample size is less than the reference sample size of the remaining datasets.

In our application of these rarefaction metrics, rather than thinking of richness as a measure of the number of species within a population, we treat it as the number of individuals at a given size class within a population. With this in mind, we made the following adjustments to our data. First, we binned Lystrosaurus skull sizes into 25 size classes using 10 mm increments, from 21 to 270 mm. Next, we calculated the interspecific abundances of each size class within each basin. This allowed us to compare body-size abundance between basins, analogous to traditional diversity metrics that compare species abundances between sites. Our goal was to be able to determine whether each basin had reached its asymptote in the number of body-size classes filled.

Our results indicate that skull sizes do not readily span the full range of sizes known for Lystrosaurus in any of the four basins studied here (Fig. 6). Of the 25 size classes generated by Lystrosaurus skull size, none of the richness estimates reach the expected asymptote (Fig. 6). The Karoo Basin comes closest to the asymptote, with 21 size classes filled in the reference sample. In the remaining basins, only a small portion of size classes are filled in the reference and extrapolated sample, indicating that sampling is sparse overall. The wide confidence intervals in the rarefaction curves for the Damodar and Transantarctic Basins further indicate that small sample size is skewing the distribution of body sizes in those basins (Fig. 6). The current sample also makes it impossible to extrapolate what sample size is needed for the asymptotes to be reached.

Figure 6. Plots comparing rarefaction curves estimating the number of body-size categories that are filled by fossil specimens in each basin studied here. A, summary of rarefaction curves for each basin, scaled to extrapolate twice that of the reference sample. B–E, rarefaction curves for each basin. Sample size–based rarefaction curves indicate that all Lystrosaurus specimens collected from Early Triassic basins fail to capture the total expected diversity of Lystrosaurus body sizes. In A–E, the solid lines represent the total number of size classes that are filled by at least one individual in the reference sample, and the extrapolated dotted line shows how many additional size classes would be filled at larger sample sizes with 95% confidence intervals. Note that extrapolated sample sizes are scaled based on the size of the reference sample.

With so many size classes left empty in our data, we cannot reliably estimate body-size distributions at larger sample sizes. Instead, we can compare the frequency and skew of body sizes from the four basins (Fig. 5) and rarefaction curves (Fig. 6) to see that specimens recovered from the Transantarctic Basin are either large or quite small, whereas specimens from the Damodar Basin tend to be small, and specimens from the Turpan-Junggar Basin are quite large. Taken together, our results indicate that additional sampling efforts outside the Karoo Basin will improve the accuracy of average body-size estimates within each basin as well as the accuracy of what sample size is needed to reach rarefied asymptotes of body-size abundances. Furthermore, our resampling and rarefaction results indicate that average body-size estimates are likely to change with the addition of new specimens outside the Karoo Basin, but that maximum body-size estimates are less likely to change, as maximum known skull size is comparable across northern and southern basins, regardless of paleolatitude. These results imply that Bergmann's rule did not apply for Lystrosaurus during the Early Triassic.

Discussion

The myriad drivers suggested as underlying Bergmann's rule in modern ecosystems make it difficult to narrow down mechanisms that could have affected body-size distributions and body-size clines in Lystrosaurus in the fossil record. In addition to sample size differences, local environmental differences within each basin could explain why body-size distributions are left or right skewed, which can influence body-size clines more broadly. Furthermore, physiological interpretations and thermal tolerances inferred for Lystrosaurus could also help to explain the potential trend of large body size in southern polar regions. As outlined in this section, we consider these potential drivers of Lystrosaurus body-size clines and discuss some of the unique considerations of size–latitude assessments in the fossil record.

There is considerable debate on the environmental conditions inferred during the Permian–Triassic (Thomas et al. Reference Thomas, Tabor, Yang, Myers, Yang and Wang2011; Li et al. Reference Li, Gastaldo, Neveling and Geissman2017; Tabor et al. Reference Tabor, Sidor, Smith, Nesbitt and Angielczyk2017; Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). This complicates tests for Bergmann's rule using specific environmental indicators. Seasonally dry, subhumid to semiarid conditions have been inferred for the mid-Induan lower Olenekian Jiucaiyuan Formation in the Turpan-Junngar Basin (Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). Seasonally dry conditions are inferred during the extinction interval in the Karoo Basin; however, aridity estimates are highly variable (e.g., Smith and Botha-Brink Reference Smith and Botha-Brink2014; Li et al. Reference Li, Gastaldo, Neveling and Geissman2017; Tabor et al. Reference Tabor, Sidor, Smith, Nesbitt and Angielczyk2017). Despite differing reports for environmental conditions in the Karoo Basin, ecosystem instability is widespread across Pangea and began in the latest Permian and continued into the Early Triassic. For example, macrofloral fossils indicate increased environmental stress in the Glossopteris forests of Antarctica (Gulbranson et al. Reference Gulbranson, Mellum, Corti, Dahlseid, Atkinson, Ryberg and Cornamusini2021) and fossilized charcoal shows evidence of wildfires in northwestern China (Wan et al. Reference Wan, Yang, Wan and Wang2021).

Considering the disturbed and highly turbulent ecosystems of the earliest Triassic, local environmental conditions within each basin could have provided different resources for Lystrosaurus to exploit. Resource availability could explain why similar maximum sizes are observed across assemblages in the Northern and Southern Hemispheres, and why the highest frequency of large individuals are recovered in the Turpan-Junggar Basin, where the inferred subhumid to semiarid environment likely supported more vegetation compared with the Karoo Basin (Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). This interpretation is consistent with McNab's (2010) resource rule, which predicts that the quality and availability of resources will have a stronger effect on body-size clines than latitude or temperature. It follows that temperature and climate dictate resource availability and primary productivity (McNab Reference McNab2010). Because paleoclimates are inferred to be more favorable and therefore could have provided increased food availability for Lystrosaurus in the Turpan-Junggar Basin, we might expect to find additional large individuals with renewed sampling in this area. The presence of large individuals in Antarctica during the Early Triassic might also be explained by more favorable environments outside the Karoo and Damodar Basins, but specific climate estimates are limited.

An important consideration in climate and resource-related influences on body size is the physiology inferred for Lystrosaurus. A heterothermic endothermic physiology has been suggested based on histological analyses of hard tissues (Botha Reference Botha2020; Whitney and Sidor Reference Whitney and Sidor2020; Han et al. Reference Han, Zhao and Liu2021; Kulik et al. Reference Kulik, Lungmus, Angielczyk and Sidor2021). This flexible physiology, combined with its broad habitat and thermal tolerances (Retallack et al. Reference Retallack, Smith and Ward2003; Liu et al. Reference Liu, Abdala, Angielczyk and Sidor2021), burrowing lifestyle (Botha-Brink Reference Botha-Brink2017), and inferred generalist diet of tough plant material (e.g., Jasinoski et al. Reference Jasinoski, Rayfield and Chinsamy2009, Reference Jasinoski, Cluver, Chinsamy, Reddy, Kammerer, Angielczyk and Fröbisch2014) could have allowed Lystrosaurus to weather extreme ecosystem instability. Histological evidence from the long bones of specimens from South Africa, India, and China indicate that none of the sampled individuals had reached skeletal maturity at death (Ray et al. Reference Ray, Chinsamy and Bandyopadhyay2005; Botha Reference Botha2020; Kulik et al. Reference Kulik, Lungmus, Angielczyk and Sidor2021). Further, the intrinsically high rate of growth inferred from the bone tissue composition indicates that Lystrosaurus had the ability to reach large size and did so in the Turpan-Junggar Basin (Kulik et al. Reference Kulik, Lungmus, Angielczyk and Sidor2021), but that Southern Hemisphere assemblages suffered increased mortality when young or at small sizes in the Karoo and Damodar Basins (Ray et al. Reference Ray, Chinsamy and Bandyopadhyay2005; Botha Reference Botha2020).

As demonstrated in our results, differences in sample size also affect estimates of average body size between basins. The relative abundance of large-bodied Lystrosaurus from China could reflect more favorable environmental conditions in the Turpan-Junggar Basin during the Early Triassic. However, we might expect the right-skewed body-size distribution to change to a normal distribution when more specimens are recovered (Fig. 5). This is also true for the Transantarctic Basin, which is so sparsely sampled that no pattern is evident in the body-size distribution (Fig. 5). Overall, it is rare to record extremes of extant taxa, so it is likely even rarer to find fossils that are extremely small or large (Blackburn and Gaston Reference Blackburn and Gaston1994). Indeed, from our results, it is rare to find a wide distribution of body sizes at all, as the number of missing size classes from our rarefaction analyses indicates that the true shape of basin-specific body-size distributions is largely unknown outside the Karoo Basin.

From the classical interpretation of Bergmann's rule with respect to cold climates, it is possible that the heterothermic endothermic physiology reconstructed for Lystrosaurus (based on the interpretation of hard tissues), could have allowed natural selection to act on individuals to impact growth rate, life history, and life span at different paleolatitudes, leading to variation in body size (Botha Reference Botha2020; Whitney and Sidor Reference Whitney and Sidor2020; Grigg et al. Reference Grigg, Nowack, Bicudo, Bal, Woodward and Seymour2021; Han et al. Reference Han, Zhao and Liu2021; Kulik et al. Reference Kulik, Lungmus, Angielczyk and Sidor2021). However, cold climates, akin to current Antarctic conditions, were not present at the poles during the Early Triassic (Boucot et al. Reference Boucot, Xu, Scotese and Morley2013), so any potential body-size trend in southern Pangea is not directly comparable to the energetic benefit of large body size at cold, high-latitude climates as classically interpreted for Bergmann's rule. Indeed, global warming caused severe dampening of the latitudinal temperature gradient and is thought to have permitted the migration of terrestrial tetrapods into southern polar regions during the Early Triassic (Collinson and Hammer Reference Collinson, Hammer, Cooper and Raymond2007; Fröbisch et al. Reference Fröbisch, Angielczyk and Sidor2010). In the absence of polar ice caps, it is possible that the comparatively cooler climate conditions in the highest southern regions could have allowed individuals to reach larger body sizes, as large archosauriforms are also known from the Early Triassic of Antarctica (Smith et al. Reference Smith, Crandall, Hellert, Hammer and Makovicky2011). The characteristic of large-bodied Triassic taxa in present-day Antarctica could have resulted from a release of constraints operating in mid-southern paleolatitudes to reduce body size (i.e., high mortality at small size), possibly due to increased resource quality and availability in temperate polar regions (Fröbisch et al. Reference Fröbisch, Angielczyk and Sidor2010; Romano et al. Reference Romano, Bernardi, Petti, Rubidge, Hancox and Benton2020).

A similar migration in the Northern Hemisphere may not have been necessary, as paleoclimate estimates indicate warm, subhumid to semiarid environments for the mid-paleolatitudes (Boucot et al. Reference Boucot, Xu, Scotese and Morley2013; Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). The possibility that Bergmann's rule could operate across different latitudinal regions within each hemisphere cannot be ruled out, nor can it be tested, as the scarcity of terrestrial fossils from paleoequatorial regions makes it impossible to assess Bergmann's rule in the Northern Hemisphere alone (Romano et al. Reference Romano, Bernardi, Petti, Rubidge, Hancox and Benton2020).

A unique consideration when testing Bergmann's rule in the fossil record is the temporal scale that the sampled assemblages encompass. Age estimates for the terrestrial Permian/Triassic boundary are highly debated, especially in the Karoo Basin (e.g., Botha et al. Reference Botha, Huttenlocker, Smith, Prevec, Viglietti and Modesto2020; Gastaldo et al. Reference Gastaldo, Kamo, Neveling, Geissman, Looy and Martini2020), which raises the possibility that samples of Lystrosaurus within each basin represent different—and potentially non-overlapping—intervals of geologic time. Geochemical age estimates generated by independent working groups reveal that the terrestrial extinction event is decoupled from the end-Permian marine extinction event in the Karoo (Botha et al. Reference Botha, Huttenlocker, Smith, Prevec, Viglietti and Modesto2020; Gastaldo et al. Reference Gastaldo, Kamo, Neveling, Geissman, Looy and Martini2020; Viglietti et al. Reference Viglietti, Benson, Smith, Botha, Kammerer, Skosan and Butler2021). Further, U-Pb age estimates from the same localities in the Karoo Basin have recovered different dates, either placing the base of the Lystrosaurus declivis Assemblage Zone in the latest Permian (Gastaldo et al. Reference Gastaldo, Kamo, Neveling, Geissman, Looy and Martini2020) or in the Early Triassic after the lithological change taken to signify the Permian/Triassic boundary (Botha et al. Reference Botha, Huttenlocker, Smith, Prevec, Viglietti and Modesto2020). Age assessments for the Permian/Triassic boundary in China place specimens recovered from the Jiucaiyuan Formation as upper Induan–lower Olenekian (Yang et al. Reference Yang, Wan, Crowley, Wang, Luo, Tabor and Angielczyk2021). However, the remaining historical collection from the wider Turpan-Junggar Basin has not been correlated to this datum. In Antarctica and India, vertebrate biochronology suggests that both the lower Fremouw and Panchet Formations are Early Triassic in age, but age dates are not available (Collinson et al. Reference Collinson, Hammer, Askin and Elliot2006; Elliot et al. Reference Elliot, Fanning, Isbell and Hulett2017). Taken together, the possibility that our results include body-size data from Permian specimens cannot be entirely ruled out.

Although our results do not recognize a Bergmann's rule body-size distribution in Lystrosaurus, other geographically widespread tetrapods, such as Diictodon and Dicynodon during the Permian, might be more amenable to this type of analysis (Kammerer et al. Reference Kammerer, Angielczyk and Fröbisch2011). If body size varies predictably with paleolatitude for other Permian or Triassic taxa, this might suggest that our results are hampered by latitudinal range or small sample sizes in some geographic areas. Alternatively, repeated failures to detect Bergmann-like patterns during times in Earth history with drastically different global temperature regimes could indicate that Bergmann's rule is only valid for the icehouse conditions of the late Cenozoic. This has been suggested by neontologists who noticed a phenotypic change in body size of modern vertebrates due to anthropogenic climate change (Yom-Tov and Geffen Reference Yom-Tov and Geffen2011; McCoy Reference McCoy2012; Goldenberg et al. Reference Goldenberg, Bisschop, D'Alba and Shawkey2022). In sum, additional investigations of Bergmann's rule in the fossil record are critical for understanding how well patterns in the past can inform our understanding of the present.

Data Availability Statement

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.j3tx95xhk.

Acknowledgments

We thank the following curators, collections managers, and colleagues for their help in providing museum collection access and support: Z. Skosan, C. Browning, C. Kammerer, R. Smith, J. Botha, E. Butler, B. Zipfel, B. Rubidge, S. Jirah, V. Radermacher, C. Mehling, M. Norell, K. Angielczyk, J. Liu, and A. Bailleul. We thank Neil Brocklehurst and one anonymous reviewer for their helpful suggestions on this manuscript. We acknowledge research funding from National Science Foundation EAR 1713787 and ANT 1341304 (to C.A.S.) and University of Washington Department of Biology Iuvo, Walker, and Snyder awards (to Z.T.K.).

References

Literature Cited

Angielczyk, K. D., Burroughs, R. W., and Feldman, C. R.. 2015. Do turtles follow the rules? Latitudinal gradients in species richness, body size, and geographic range area of the world's turtles. Journal of Experimental Zoology B 324:270–294.CrossRefGoogle ScholarPubMed
Araújo, R., Smith, R. M. H., Tolan, S., Angielczyk, K. D., Crowley, J. L., Milisse, D., and Mugabe, J.. 2020. Biostratigraphic refinement of tetrapod-bearing beds from the Metangula graben (Niassa Province, Mozambique). New radiometric dating and the first Lower Triassic tetrapod fossils from Mozambique. Palaeontologia Africana 54:56–58.Google Scholar
Ashton, K. G. 2002. Do amphibians follow Bergmann's rule? Canadian Journal of Zoology 80:708–716.CrossRefGoogle Scholar
Ashton, K. G., and Feldman, C. R.. 2003. Bergmann's rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution 57:1151–1163.Google Scholar
Ashton, K. G., Tracy, M. C., and de Queiroz, A.. 2000. Is Bergmann's rule valid for mammals? American Naturalist 156:390–415.CrossRefGoogle ScholarPubMed
Belk, M. C., and Houston, D. D. 2002. Bergmann's rule in ectotherms: a test using freshwater fishes. American Naturalist 160:803–808.CrossRefGoogle ScholarPubMed
Bergmann, C. 1847. Uber die verhaltnisse der warmeokonomie der thiere zu uber grosso. Göttinger studien, Vol. 3. Vandenhoeck and Ruprecht, Göttingen.Google Scholar
Berke, S. K., Jablonski, D., Krug, A. Z., Roy, K., and Tomasovych, A.. 2013. Beyond Bergmann's rule: size–latitude relationships in marine Bivalvia world-wide. Global Ecology and Biogeography 22:173–183.CrossRefGoogle Scholar
Blackburn, T. M., and Gaston, K. J.. 1994. Animal body size distributions: patterns, mechanisms and implications. Trends in Ecology and Evolution 9:471–474.CrossRefGoogle ScholarPubMed
Blackburn, T. M., and Gaston, K. J.. 1996. Spatial patterns in the body sizes of bird species in the new world. Oikos 77:436–446.CrossRefGoogle Scholar
Blackburn, T. M., and Ruggiero, A.. 2001. Latitude, elevation and body mass variation in Andean passerine birds. Global Ecology and Biogeography 10:245–259.CrossRefGoogle Scholar
Blackburn, T. M., Gaston, K. J., and Loder, N.. 1999. Geographic gradients in body size: a clarification of Bergmann's rule. Diversity and Distributions 5:165–174.CrossRefGoogle Scholar
Blackburn, T. M., Redding, D. W., and Dyer, E. E.. 2019. Bergmann's rule in alien birds. Ecography 42:102–110.CrossRefGoogle Scholar
Botha, J. 2020. The paleobiology and paleoecology of South African Lystrosaurus. PeerJ 8:e10408.CrossRefGoogle ScholarPubMed
Botha, J., and Smith, R. M. H.. 2007. Lystrosaurus species composition across the Permo–Triassic boundary in the Karoo Basin of South Africa. Lethaia 40:125–137.CrossRefGoogle Scholar
Botha, J., and Smith, R. M. H.. 2020. Biostratigraphy of the Lystrosaurus declivis Assemblage Zone (Beaufort Group, Karoo Supergroup), South Africa. South African Journal of Geology 123:207–216.CrossRefGoogle Scholar
Botha, J., Huttenlocker, A. K., Smith, R. M.H., Prevec, R., Viglietti, P., and Modesto, S. P.. 2020. New geochemical and palaeontological data from the Permian–Triassic boundary in the South African Karoo Basin test the synchronicity of terrestrial and marine extinctions. Palaeogeography, Palaeoclimatology, Palaeoecology 540:109467.CrossRefGoogle Scholar
Botha-Brink, J. 2017. Burrowing in Lystrosaurus: preadaptation to a postextinction environment? Journal of Vertebrate Paleontology 37:e1365080.CrossRefGoogle Scholar
Botha-Brink, J., Huttenlocker, A. K., and Modesto, S. P.. 2014. Vertebrate paleontology of Nooitgedacht 68: a Lystrosaurus maccaigi-rich Permo-Triassic boundary locality in South Africa. Pp. 289–304 in Kammerer, C. F., Angielczyk, K. D., and Fröbisch, J., eds. Early evolutionary history of the Synapsida. Vertebrate Paleobiology and Paleoanthropology. Dordrecht, Netherlands: Springer.CrossRefGoogle Scholar
Botha-Brink, J., Codron, D., Huttenlocker, A. K., Angielczyk, K. D., and Ruta, M.. 2016. Breeding young as a survival strategy during Earth's greatest mass extinction. Scientific Reports 6(1). https://doi.org/10.1038/srep24053.CrossRefGoogle Scholar
Boucot, A. J., Xu, C., Scotese, C. R., and Morley, R. J.. 2013. Phanerozoic paleoclimate: an atlas of lithologic indicators of climate. Tulsa, Okla.: SEPM.CrossRefGoogle Scholar
Briscoe, N. J., Krockenberger, A., Handasyde, K. A., and Kearney, M. R.. 2015. Bergmann meets Scholander: geographical variation in body size and insulation in the koala is related to climate. Journal of Biogeography 42:791–802.CrossRefGoogle Scholar
Brown, J. S., Kotler, B. P., and Porter, W. P.. 2017. How foraging allometries and resource dynamics could explain Bergmann's rule and the body-size diet relationship in mammals. Oikos 126(2). https://doi.org/10.1111/oik.03468.CrossRefGoogle Scholar
Camp, J., and Liu, J.. 2011. The taxonomy and cranial morphology of Chinese Lystrosaurus [Abstract]. In 71st Annual Meeting of the Society of Vertebrate Paleontology. Journal of Vertebrate Paleontology 31(Suppl. 2):82.Google Scholar
Chao, A., and Jost, L.. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547.CrossRefGoogle ScholarPubMed
Chown, S. L., and Gaston, K. J.. 2010. Body size variation in insects: a macroecological perspective. Biological Reviews 85:139–169.CrossRefGoogle ScholarPubMed
Colbert, E. H. 1974. Lystrosaurus from Antarctica. American Museum Novitates 2535:1–44.Google Scholar
Collinson, J. W., and Hammer, W. R.. 2007. Migration of Triassic tetrapods to Antarctica. P. 3 in Cooper, A. K. and Raymond, C. R., eds. Antarctica: a keystone in a changing world. Online proceedings of the 10th International Symposium on Antarctic Earth Sciences.Google Scholar
Collinson, J. W., Hammer, W. R., Askin, R. A., and Elliot, D. H.. 2006. Permian–Triassic boundary in the central Transantarctic Mountains, Antarctica. GSA Bulletin 118:747–763.CrossRefGoogle Scholar
Correll, R. A., Prowse, T. A. A., and Prideaux, G. J.. 2016. Lean-season primary productivity and heat dissipation as key drivers of geographic body-size variation in a widespread marsupial. Ecography 39:77–86.CrossRefGoogle Scholar
Cosgriff, J. W., Hammer, W. R., and Ryan, W. J.. 1982. The Pangaean reptile, Lystrosaurus maccaigi, in the Lower Triassic of Antarctica. Journal of Paleontology 56:371–385.Google Scholar
Elliot, D. H., Fanning, C. M., Isbell, J. L., and Hulett, S. R.W.. 2017. The Permo-Triassic Gondwana sequence, central Transantarctic Mountains, Antarctica: zircon geochronology, provenance, and basin evolution. Geosphere 13:155–178.CrossRefGoogle Scholar
Feder, M. E., Papenfuss, T. J., and Wake, D. B.. 1982. Body size and elevation in neotropical salamanders. Copeia 1982:186–188.CrossRefGoogle Scholar
Freckleton, R. P., Harvey, P. H., and Pagel, M.. 2003. Bergmann's rule and body size in mammals. American Naturalist 161:821–825.CrossRefGoogle ScholarPubMed
Fröbisch, J., Angielczyk, K. D., and Sidor, C. A.. 2010. The Triassic dicynodont Kombuisia (Synapsida, Anomodontia) from Antarctica, a refuge from the terrestrial Permo-Triassic mass extinction. Naturwissenschaften 97:187–196.CrossRefGoogle Scholar
Gastaldo, R. A., Kamo, S. L., Neveling, J., Geissman, J. W., Looy, C. V., and Martini, A. M.. 2020. The base of the Lystrosaurus Assemblage Zone, Karoo Basin, predates the end-Permian marine extinction. Nature Communications 11:1428.CrossRefGoogle ScholarPubMed
Gohli, J., and Voje, K. L.. 2016. An interspecific assessment of Bergmann's rule in 22 mammalian families. BMC Evolutionary Biology 16(1). https://doi.org/10.1186/s12862-016-0778-x.CrossRefGoogle ScholarPubMed
Goldenberg, J., Bisschop, K., D'Alba, L., and Shawkey, M. D.. 2022. The link between body size, colouration and thermoregulation and their integration into ecogeographical rules: a critical appraisal in light of climate change. Oikos. https://doi.org/10.1111/oik.09152.CrossRefGoogle Scholar
Grigg, G., Nowack, J., Bicudo, J. E. P. W., Bal, N. C., Woodward, H. N., and Seymour, R. S.. 2021. Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians. Biological Reviews 97:766–801.CrossRefGoogle ScholarPubMed
Grine, F. E., Forster, C. A., Cluver, M. A., and Georgi, J. A.. 2006. Cranial variability, ontogeny and taxonomy of Lystrosaurus from the Karoo Basin of South Africa. Pp. 432–503 in Carrano, M. T., Gaudin, T., Blob, R., and Wible, J., eds. Amniote paleobiology: perspectives on the evolution of mammals, birds, and reptiles. University of Chicago Press, Chicago.Google Scholar
Gubin, Y. M., and Sinitza, S. M.. 1993. Triassic terrestrial tetrapods of Mongolia and the geological structure of the Sain-Sar-Bulak locality. In Lucas, S. G. and Morales, Michael, eds. The nonmarine Triassic. New Mexico Museum of Natural History and Science Bulletin 3:169–70.Google Scholar
Gulbranson, E., Mellum, M., Corti, V., Dahlseid, A., Atkinson, B., Ryberg, P., and Cornamusini, G.. 2021. Paleoclimate-induced stress on polar forested ecosystems prior to the Permian–Triassic mass extinction. Preprint. https://doi.org/10.21203/rs.3.rs-1108556/v1.Google Scholar
Gupta, A., and Das, D. P.. 2011. Report of Lystrosaurus cf. curvatus and L. cf. declivis from the Early Triassic Panchet Formation, Damodar Valley, West Bengal, India and its implications. Indian Journal of Geosciences 65:119–130.Google Scholar
Han, F., Zhao, Q., and Liu, J.. 2021. Preliminary bone histological analysis of Lystrosaurus (Therapsida: Dicynodontia) from the Lower Triassic of North China, and its implication for lifestyle and environments after the end-Permian extinction. PLoS ONE 16:e0248681.CrossRefGoogle ScholarPubMed
Hinsbergen, D. J. J. van, de Groot, L. V., van Schaik, S. J., Spakman, W., Bijl, P. K., Sluijs, A., Langereis, C. G., and Brinkhuis, H.. 2015. A paleolatitude calculator for paleoclimate studies. PLoS ONE 10:e0126946.CrossRefGoogle ScholarPubMed
Hsieh, T. C., Ma, K. H., and Chao, A.. 2016. INEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution 7(12):1451–1456.CrossRefGoogle Scholar
Jadwiszczak, P. 2001. Body size in Eocene Antarctic penguins. Polish Polar Research 22:147–158.Google Scholar
James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology 51:365–390.CrossRefGoogle Scholar
Jasinoski, S. C., Rayfield, E. J., and Chinsamy, A.. 2009. Comparative feeding biomechanics of Lystrosaurus and the generalized dicynodont Oudenodon. Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology 292:862–874.CrossRefGoogle ScholarPubMed
Jasinoski, S. C., Cluver, M. A., Chinsamy, A., and Reddy, B. D.. 2014. Anatomical plasticity in the snout of Lystrosaurus. Pp. 139–149 in Kammerer, C. F., Angielczyk, K. D., and Fröbisch, J., eds. Early evolutionary history of the Synapsida. Vertebrate Paleobiology and Paleoanthropology. Dordrecht, Netherlands: Springer.CrossRefGoogle Scholar
Kammerer, C. F., Angielczyk, K. D., and Fröbisch, J.. 2011. A comprehensive taxonomic revision of Dicynodon (Therapsida, Anomodontia) and its implications for dicynodont phylogeny, biogeography, and biostratigraphy. Journal of Vertebrate Paleontology 31:1–158.CrossRefGoogle Scholar
Kelly, R. M., Friedman, R., and Santana, S. E.. 2018. Primary productivity explains size variation across the pallid bat's western geographic range. Functional Ecology 32:1520–1530.CrossRefGoogle Scholar
Kidder, D. L., and Worsley, T. R.. 2004. Causes and consequences of extreme Permo-Triassic warming to globally equable climate and relation to the Permo-Triassic extinction and recovery. Palaeogeography, Palaeoclimatology, Palaeoecology 203:207–237.CrossRefGoogle Scholar
King, G. 1990. The dicynodonts: a study in palaeobiology. Chapman and Hall, New York.Google Scholar
Kulik, Z. T., Lungmus, J. K., Angielczyk, K. D., and Sidor, C. A.. 2021. Living fast in the Triassic: new data on life history in Lystrosaurus (Therapsida: Dicynodontia) from northeastern Pangea. PLoS ONE 16:e0259369.CrossRefGoogle ScholarPubMed
Li, J., Gastaldo, R. A., Neveling, J., and Geissman, J. W.. 2017. Siltstones across the Daptocephalus (Dicynodon) and Lystrosaurus Assemblage Zones, Karoo Basin, South Africa, show no evidence for aridification. Journal of Sedimentary Research 87:653–671.CrossRefGoogle Scholar
Liu, J., Li, J. L., and Cheng, Z. W.. 2002. The Lystrosaurus fossils from Xinjiang and their bearing on the terrestrial Permian Triassic boundary. Vertebrata Pal Asiatica 40:267–275.Google Scholar
Liu, J., Abdala, F., Angielczyk, K. D., and Sidor, C. A.. 2021. Tetrapod turnover during the Permo-Triassic transition explained by temperature change. Earth-Science Reviews 224:103886.CrossRefGoogle Scholar
Mancuso, A. C., Horn, B. L. D., Benavente, C. A., Schultz, C. L., and Irmis, R. B.. 2021. The paleoclimatic context for South American Triassic vertebrate evolution. Journal of South American Earth Sciences 110:103321.CrossRefGoogle Scholar
Mayr, E. 1956. Geographical character gradients and climatic adaptation. Evolution 10:105–108.CrossRefGoogle Scholar
Mayr, E. 1963. Animal species and evolution. Harvard University Press, Cambridge, Mass.CrossRefGoogle Scholar
McCoy, D. E. 2012. Connecticut birds and climate change: Bergmann's rule in the fourth dimension. Northeastern Naturalist 19:323–334.CrossRefGoogle Scholar
McNab, B. K. 1971. On the ecological significance of Bergmann's rule. Ecology 52:845–854.CrossRefGoogle Scholar
McNab, B. K. 2010. Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23.CrossRefGoogle ScholarPubMed
Meachen, J. A., Janowicz, A. C., Avery, J. E., and Sadleir, R. W.. 2014. Ecological changes in coyotes (Canis latrans) in response to the ice age megafaunal extinctions. PLoS ONE 9:e116041.CrossRefGoogle Scholar
Meiri, S., and Dayan, T.. 2003. On the validity of Bergmann's rule. Journal of Biogeography 30:331–351.CrossRefGoogle Scholar
Meiri, S., Dayan, T., and Simberloff, D.. 2004. Carnivores, biases and Bergmann's rule. Biological Journal of the Linnean Society 81:579–588.CrossRefGoogle Scholar
Meiri, S., Yom-Tov, Y., and Geffen, E.. 2007. What determines conformity to Bergmann's rule? Global Ecology and Biogeography 16:788–794.CrossRefGoogle Scholar
Montgomery, C. E., Mackessy, S. P., and Moore, J. C.. 2003. Body size variation in the Texas horned lizard, Phrynosoma cornutum, from central Mexico to Colorado. Journal of Herpetology 37:550–553.CrossRefGoogle Scholar
Murphy, E. C. 1985. Bergmann's rule, seasonality, and geographic variation in body size of house sparrows. Evolution 39:1327–1334.CrossRefGoogle ScholarPubMed
Nwaogu, C. J., Tieleman, B. I., Bitrus, K., and Cresswell, W.. 2018. Temperature and aridity determine body size conformity to Bergmann's rule independent of latitudinal differences in a tropical environment. Journal of Ornithology 159:1053–1062.CrossRefGoogle Scholar
Orcutt, J. D., and Hopkins, S. S. B.. 2013. Oligo-Miocene climate change and mammal body-size evolution in the northwest United States: a test of Bergmann's rule. Paleobiology 39:648–661.CrossRefGoogle Scholar
Pallarés, S., Lai, M., Abellán, P., Ribera, I., and Sánchez-Fernández, D.. 2019. An interspecific test of Bergmann's rule reveals inconsistent body size patterns across several lineages of water beetles (Coleoptera: Dytiscidae). Ecological Entomology 44:249–254.CrossRefGoogle Scholar
Peecook, B. R., Smith, R. M. H., and Sidor, C. A.. 2019. A novel archosauromorph from Antarctica and an updated review of a high-latitude vertebrate assemblage in the wake of the end-Permian mass extinction. Journal of Vertebrate Paleontology 38:e1536664.CrossRefGoogle Scholar
Pincheira-Donoso, D., and Meiri, S.. 2013. An intercontinental analysis of climate-driven body size clines in reptiles: no support for patterns, no signals of processes. Evolutionary Biology 40:562–578.CrossRefGoogle Scholar
Queiroz, A. de, and Ashton, K. G.. 2004. The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann's rule in tetrapods. Evolution 58:1674–1684.Google ScholarPubMed
Ray, S. 2005. Lystrosaurus (Therapsida, Dicynodontia) from India: taxonomy, relative growth and cranial dimorphism. Journal of Systematic Palaeontology 3:203–221.CrossRefGoogle Scholar
Ray, S., Chinsamy, A., and Bandyopadhyay, S.. 2005. Lystrosaurus murrayi (Therapsida, Dicynodontia): Bone histology, growth and lifestyle adaptations. Palaeontology 48:1169–1185.CrossRefGoogle Scholar
Rensch, B. 1938. Some problems of geographical variation and species-formation. Proceedings of the Linnean Society of London 150:275–285.CrossRefGoogle Scholar
Retallack, G. J., Smith, R. M.H., and Ward, P. D.. 2003. Vertebrate extinction across Permian–Triassic boundary in Karoo Basin, South Africa. Geological Society of America Bulletin 115:1133–1152.CrossRefGoogle Scholar
Rodríguez, M. Á., Olalla-Tárraga, M. Á., and Hawkins, B. A.. 2008. Bergmann's rule and the geography of mammal body size in the western hemisphere. Global Ecology and Biogeography 17:274–283.CrossRefGoogle Scholar
Romano, M., Bernardi, M., Petti, F. M., Rubidge, B., Hancox, J., and Benton, M. J.. 2020. Early Triassic terrestrial tetrapod fauna: a review. Earth-Science Reviews 210:1–40.CrossRefGoogle Scholar
Romano, A., Séchaud, R., and Roulin, A.. 2021. Generalized evidence for Bergmann's rule: body size variation in a cosmopolitan owl genus. Journal of Biogeography 48:51–63.CrossRefGoogle Scholar
Roy, K., Jablonski, D., and Martien, K. K.. 2000. Invariant size–frequency distributions along a latitudinal gradient in marine bivalves. Proceedings of the National Academy of Sciences USA 97:13150–13155.CrossRefGoogle ScholarPubMed
Salewski, V., and Watt, C.. 2017. Bergmann's rule: a biophysiological rule examined in birds. Oikos 126(2). https://doi.org/10.1111/oik.03698.CrossRefGoogle Scholar
Scotese, C. R. 2016. PALEOMAP PaleoAtlas for GPlates and the PaleoData Plotter Program, Version 2. PALEOMAP Project. http://www.earthbyte.org/paleomap-paleoatlas-for-gplates.CrossRefGoogle Scholar
Slavenko, A., Feldman, A., Allison, A., Bauer, A. M., Böhm, M., Chirio, L., Colli, G. R., et al. 2019. Global patterns of body size evolution in squamate reptiles are not driven by climate. Global Ecology and Biogeography 28:471–483.CrossRefGoogle Scholar
Smith, N. D., Crandall, J. R., Hellert, S. M., Hammer, W. R., and Makovicky, P. J.. 2011. Anatomy and affinities of large Archosauromorphs from the lower Fremouw Formation (Early Triassic) of Antarctica. Journal of Vertebrate Paleontology 31:784–797.CrossRefGoogle Scholar
Smith, R. M. H., and Botha-Brink, J.. 2014. 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. Palaeogeography, Palaeoclimatology, Palaeoecology 396:99–118.CrossRefGoogle Scholar
Smith, R. M. H., Rubidge, B. S., and van der Walt, M.. 2012. Therapsid biodiversity patterns and paleoenvironments of the Karoo Basin, South Africa. Pp. 31–63 in Chinsamy-Turan, A., ed. Forerunners of mammals: radiation, histology, biology. Indiana University Press, Bloomington.Google Scholar
Sun, A.-L. 1964. Preliminary report on a new species of Lystrosaurus of Sinkiang. Vertebrata Pal Asiatica 8:216–217.Google Scholar
Sun, A.-L. 1973. Permo-Triassic dicynodonts from Turfan, Sinkiang. Reports of Paleontological Expedition to Sinkiang (I): Permo-Triassic Vertebrate Fossils of Turfan Basin. Memoirs of the Institute of Vertebrate Paleontology and Paleoanthropology Academia Sinica 10:53–68.Google Scholar
Sun, A.-L. 1980. Late Permian and Triassic terrestrial tetrapods of North China. Vertebrata PalAsiatica 18:11.Google Scholar
Surkov, M. V., Kalandadze, N. N., and Benton, M. J.. 2005. Lystrosaurus georgi, a dicynodont from the Lower Triassic of Russia. Journal of Vertebrate Paleontology 25:402–413.CrossRefGoogle Scholar
Tabor, N. J., Sidor, C. A., Smith, R. M. H., Nesbitt, S. J., and Angielczyk, K. D.. 2017. Paleosols of the Permian–Triassic: proxies for rainfall, climate change and major changes in terrestrial tetrapod diversity. Journal of Vertebrate Paleontology 37:240–253.CrossRefGoogle Scholar
Thomas, S. G., Tabor, N. J., Yang, W., Myers, T. S., Yang, Y., and Wang, D.. 2011. Palaeosol stratigraphy across the Permian–Triassic Boundary, Bogda Mountains, NW China: implications for palaeoenvironmental transition through Earth's largest mass extinction. Palaeogeography, Palaeoclimatology, Palaeoecology 308:41–64.CrossRefGoogle Scholar
Thulborn, R. A. 1990. Mammal-like reptiles of Australia. Memoirs of the Queensland Museum 28:1–169.Google Scholar
Timofeev, S. F. 2001. Bergmann's principle and deep-water gigantism in marine crustaceans. Biology Bulletin 28:646–650.CrossRefGoogle Scholar
Tripathi, C., and Puri, S. N.. 1961. On the remains of Lystrosaurus from the Panchets of the Raniganj coalfield. Records of the Geological Survey of India 89:407–419.Google Scholar
Viglietti, P. A., Benson, R. B. J., Smith, R. M. H., Botha, J., Kammerer, C. F., Skosan, Z., Butler, E., et al. 2021. Evidence from South Africa for a protracted end-Permian extinction on land. Proceedings of the National Academy of Sciences USA 118:e2017045118.CrossRefGoogle ScholarPubMed
Villabolos, F., Olalla-Tarraga, M. A., Vieira, C. M., Mazzei, N. D., and Bini, L. M.. 2017. Spatial dimension of body size evolution in Pterosauria: Bergmann's rule does not drive Cope's rule. Evolutionary Ecology Research 18:169–186.Google Scholar
Wan, M.-L., Yang, W., Wan, S., and Wang, J.. 2021. Wildfires in the Early Triassic of northeastern Pangaea: evidence from fossil charcoal in the Bogda Mountains, northwestern China. Palaeoworld 30:593–601.CrossRefGoogle Scholar
Watt, C., Mitchell, S., and Salewski, V.. 2010. Bergmann's rule; a concept cluster? Oikos 119:89–100.CrossRefGoogle Scholar
Wells, J. C., Saunders, M. A., Lea, A. S., Cortina-Borja, M., and Shirley, M. K.. 2019. Beyond Bergmann's rule: global variability in human body composition is associated with annual average precipitation and annual temperature volatility. American Journal of Physical Anthropology 170:75–87.CrossRefGoogle ScholarPubMed
Whitney, M. R., and Sidor, C. A.. 2020. Evidence of torpor in the tusks of Lystrosaurus from the Early Triassic of Antarctica. Communications Biology 3:1–6.CrossRefGoogle ScholarPubMed
Winguth, A. M. E., Shields, C. A., and Winguth, C.. 2015. Transition into a hothouse world at the Permian–Triassic boundary—a model study. Palaeogeography, Palaeoclimatology, Palaeoecology 440:316–327.CrossRefGoogle Scholar
Yang, W., Wan, M., Crowley, J. L., Wang, J., Luo, X., Tabor, N., Angielczyk, K. D., et al. 2021. Paleoenvironmental and paleoclimatic evolution and cyclo- and chrono-stratigraphy of upper Permian–Lower Triassic fluvial-lacustrine deposits in Bogda mountains, NW China—implications for diachronous plant evolution across the Permian–Triassic boundary. Earth-Science Reviews 222:103741.CrossRefGoogle Scholar
Yom-Tov, Y., and Geffen, E.. 2011. Recent spatial and temporal changes in body size of terrestrial vertebrates: Probable causes and pitfalls. Biological Reviews 86:531–541.CrossRefGoogle ScholarPubMed
Young, C. C. 1939. Additional Dicynodontia remains from Sinkiang. Bulletin of the Geological Society of China 19:111–36.CrossRefGoogle Scholar
Yu, T. L., Wang, D. L., Busam, M., and Deng, T. H.. 2019. Altitudinal variation in body size in Bufo minshanicus supports Bergmann's rule. Evolutionary Ecology 33:449–460.CrossRefGoogle Scholar
Yuan, P. L., and Young, C. C.. 1934. On the occurrence of Lystrosaurus in Sinkiang. Bulletin of the Geological Society of China 13:575–580.CrossRefGoogle Scholar
Figure 0

Figure 1. Geographic distribution of Lystrosaurus fossils sampled. Paleogeographic map of the Early Triassic with estimated locations of geologic basins denoted by stars; sampled localities are labeled and filled in orange; unsampled localities are open. Paleomap modified from Scotese (2016). Lystrosaurus silhouette from Phylopic.org.

Figure 1

Figure 2. Cranial measurements used to estimate body size in Lystrosaurus. A, Minimum interorbital width, B, basal skull length, C, tusk diameter at eruption, and D, dorsal snout length and dorsal skull length were measured from incompletely prepared or broken specimens. Abbreviations: f, frontal; p, premaxilla. Skull drawings adapted from King (1990).

Figure 2

Figure 3. Plots comparing Lystrosaurus size and geographic position using: A, basal skull length; B, standardized basal skull length as a percent of maximum size; C, tusk diameter; and D, standardized tusk diameter. Lystrosaurus does not follow a pattern that is consistent with Bergmann's rule. Skull size is significantly larger in the midlatitude Turpan-Junggar Basin and greater in the Karoo Basin than in the Damodar Basin. Red diamonds and gray bars indicate the mean and median values, respectively.

Figure 3

Figure 4. Plots comparing skull length in four species of Lystrosaurus against geographic position. At the species level, median body size remains constant between Triassic basins, except for Lystrosaurus maccaigi; note that the outlier from the Karoo Basin is approximately the same size as the individuals from the Transantarctic Basin.

Figure 4

Figure 5. Distributions of skull size of Lystrosaurus collected from four geographic areas. A, interspecific Lystrosaurus basal skull length (BSL) and proportional skull size (%BSL max) in the Transantarctic Basin, B, normally distributed skull size in the Karoo Basin, C, right-skewed distribution in the Damodar Basin, and D, left-skewed distribution in the Turpan-Junggar Basin when skull length is standardized as a proportion of the maximum known size per species.

Figure 5

Figure 6. Plots comparing rarefaction curves estimating the number of body-size categories that are filled by fossil specimens in each basin studied here. A, summary of rarefaction curves for each basin, scaled to extrapolate twice that of the reference sample. B–E, rarefaction curves for each basin. Sample size–based rarefaction curves indicate that all Lystrosaurus specimens collected from Early Triassic basins fail to capture the total expected diversity of Lystrosaurus body sizes. In A–E, the solid lines represent the total number of size classes that are filled by at least one individual in the reference sample, and the extrapolated dotted line shows how many additional size classes would be filled at larger sample sizes with 95% confidence intervals. Note that extrapolated sample sizes are scaled based on the size of the reference sample.