PALEONTOLOGY

An elephant-sized Late Triassicsynapsid with erect limbsTomasz Sulej1 and Grzegorz Niedźwiedzki2*

Here, we describe the dicynodont Lisowicia bojani, from the Late Triassic of Poland, agigantic synapsid with seemingly upright subcursorial limbs that reached an estimatedlength of more than 4.5 meters, height of 2.6 meters, and body mass of 9 tons. Lisowicia isthe youngest undisputed dicynodont and the largest nondinosaurian terrestrial tetrapodfrom the Triassic. The lack of lines of arrested growth and the highly remodeled cortexof its limb bones suggest permanently rapid growth and recalls that of dinosaurs andmammals. The discovery of Lisowicia overturns the established picture of the Triassicmegaherbivore radiation as a phenomenon restricted to dinosaurs and shows thatstem-group mammals were capable of reaching body sizes that were not attained againin mammalian evolution until the latest Eocene.

The time interval from the end of thePermian to the beginning of the Jurassic(252 to 201 million years ago) coincidedwith a trophic and taxonomic restructur-ing of terrestrial ecosystems (1). During the

middle Permian, the predominant large herbivoreswere dinocephalians—stem-groupmammals (in theclade Synapsida, “mammal-like reptiles”) such asTapinocephalus, which was up to 3 m in lengthand weighed an estimated 2 tons (2). These ani-mals were associatedwith faunas of nonsynapsidpareiasaurian parareptiles and a rich variety ofother synapsids. In the late Permian, the large-size synapsid herbivores (rhachiocephalid di-cynodonts) and the last pareiasaurians playedthe role of largest terrestrial herbivores (2). Bythe Early Jurassic, no stem-group mammalswere larger than a half meter in length, andmost were much smaller (3, 4), whereas herbiv-orous dinosaurs exceeded 15 m in length and10 tons in weight; virtually all mid-sized to largetetrapods were archosaurs. Until now, this pat-tern has appeared clear-cut, with Triassic syn-apsids approaching the largest Permian formsin size but with no forms reaching sizes of thefirst large sauropodomorphs.Dicynodonts were among the most abundant

and diverse synapsids from the middle Permianto the early Late Triassic (5, 6). There were twoepisodes of body size increase in their evolu-tion: the first in the late Permian, exemplified byRhachiocephalus, and the second in theMiddle toLate Triassic, whendicynodonts such asPlaceriaswere thedominant herbivores in some ecosystems(6). There have been comparatively few rigorousestimates of dicynodont or dinocephalian bodymasses presented in the literature. The largest ofthese dicynodonts (such as kannemeyeriiforms)are estimated previously to have reached lengthsof 3 to 3.5 m and weights of up to 1 to 2 tons

(2, 7), which is very similar to the largest middlePermian dinocephalians, such asTapinocephalusorMoschops (2).Fossils of Triassic dicynodonts are extremely

abundant in African, Asian, andNorth and SouthAmerican deposits but are comparatively poorlyknown from other regions (5, 6). Dicynodontswere seemingly rare in the European Late Triassic,being known only from a single mandible (8)and questionable isolated bones (9). The LateTriassic dicynodont fossils described here, of

Lisowicia bojani, are the first substantial findsfrom Europe (10, 11).Many previous authors have analyzed the

structure of the pelvic girdle of Triassic dicyn-odonts, resulting in the unanimous opinion thatthe posture of the hindlimbs was erect (12). Bycontrast, most authors agree that Triassic dicyn-odonts had sprawling forelimbs with the hori-zontal position of the humerus (13). Lisowicia hasa relatively conventional dicynodont hindlimbconstruction but departs from the standardforelimb posture (Fig. 1). In many respects, itsforelimb position resembles that of large quad-rupedal dinosaurs, but forelimb elements ofLisowicia are morphologically similar to otherdicynodonts (Fig. 2). The result is a subcursorialtetrapod with upright limb posture, unlike anyother known stem-group mammal but compa-rable with that of large crown-group mammalssuch as rhinoceroses and hippopotami, as well asquadrupedal dinosaurs such as sauropodomorphsand ceratopsians.Histological data from limb bones of Lisowicia

provide life history data that complement its dis-tinctness. Like other large dicynodonts, Lisowiciashows a large area of bone resorption in the innercortex. However, unlike in other genera, there isno clear sign of growth-slowing later in life. Thepresence of potential lines of arrested growth inthe studied tibia might be indicative of slower,more episodic growth. However, the lack of char-acteristic slow-growing tissue on the periphery

RESEARCH

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1Institute of Paleobiology, Polish Academy of Sciences (PAS),Twarda 51/55, 00-818 Warsaw, Poland. 2Department ofOrganismal Biology, Uppsala University, Norbyvägen 18A, 75236 Uppsala, Sweden.*Corresponding author. Email: grzegorz.niedzwiedzki@ebc.uu.se

Fig. 1. The skeleton restoration of Lisowicia bojani. (A) Left humerus (ZPAL V.33/96) in ventralview. (B) Left radius (ZPAL V.33/665) in lateral view. (C) Cervical vertebrae (ZPAL V.33/720) inposterior view. (D) Dorsal vertebrae (ZPAL V.33/720) in lateral view. (E) Left pelvis (ZPAL V.33/720;ilium, pubis, and ischium) in lateral view. (F) Left femur (ZPAL V.33/75) in anterior view. (G) Lefttibia (ZPAL V.33/75) in lateral view. (H) Left fibula (ZPAL V.33/75) in medial view. (I) Left ulna (ZPALV.33/470) in lateral view. (J) Left scapulocoracoid (ZPAL V.33/468) in lateral view. (K) Fusedquadrate and quadratojugal (ZPAL V.33/735) in posterior view. Scale bars, 10 cm (A) to (K); 1 m forthe skeleton. (L) Light gray bones represent missing elements. il, ilium; pu, pubis; is, ischium.

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of the largest bones of Lisowicia suggests thatthe studied material represents either a fast-growing taxon or juvenile/subadult individualsof extremely large body size. However, the sec-ond explanation is rather unlikely because of itssize and that these two bones are well ossified.Lisowicia demonstrates that Late Triassic di-

cynodonts became specialized herbivores. It dis-plays several features in the limb skeleton thatsuggest that this group evolved new posturaladaptations. The massive scapula of Lisowicialacks a distinct acromion process for articulationwith the clavicle, the scapula articulates with thehumerus on its posteroventrally (instead of pos-terolaterally) located glenoid, and distal articu-lation surfaces of the humerus are in the sameplane instead of being rotated (formal taxonomicdescription is provided in the supplementarymaterials).On the basis of published scaling relationships

(14), we estimate an adult body mass of 9000 kg,which approaches that of an African elephant[the largest recorded individual stood 4 m atthe shoulders and weighed 10,000 kg (15)]. Thisconfirms that Lisowicia was certainly the largest

Triassic land nondinosaur tetrapod. Gigantismin herbivorous dinosaurs first emerged in theLate Triassic, with the evolution of the firstlarge sauropodomorphs (16, 17) and then theearliest true sauropods (18). Until now, gigan-tism in the Triassic appeared to be entirely adinosaur adaptation (19), and previously knownTriassic dicynodonts were substantially smaller.The discovery of Lisowicia suggests that generalecological factors may have been driving theprocess, rather than clade-specific attributes ofdinosaurs (20).The find of Lisowicia shows that at least

one dicynodont lineage also participated in the“push for gigantism” at the same time as thesauropodomorphs (20) but also suggests thattheir evolutionary history in the Late Triassic ispoorly documented (Fig. 3A). In addition, rec-ognition of Lisowicia as a placeriine dicynodonttogether with the resurrection and recent de-scription of Pentasaurus from South Africa (21)alters our understanding of the Late Triassicfossil record of dicynodonts. Although their rel-atively lower abundance and richness comparedwith those of Middle and early Late Triassic

faunas suggest evolutionary decline, the con-cept of the Late Triassic kannemeyeriiforms ashighly geographically restricted relicts is no longervalid (22). The recognition of dicynodonts inthe late Norian–earliest Rhaetian of Europe (10)and Karoo Basin (21) conflicts with some ideason early Late Triassic dicynodont extinction andsurvival, namely their supposed absence duringthe radiation of early sauropodomorphs (Fig. 3B).Upright posture has been associated with de-

creased joint stress and energetic cost of loco-motion (23). Selection pressures on some aspectsof lifestyle or ecology were likely drivers of theevolution of the distinct posture of Lisowiciaamong dicynodonts. Increase in the body size ofdicynodonts across the Late Triassic may havebeen driven by selection pressure to reach a sizerefuge from large predators (24). It is possiblealso that the gigantism of the latest dicynodontswas a metabolic adaptation that allowed theseanimals to maximize food retention time andconsequently the energy gain (25). It took LateTriassic dicynodonts some 20 million years toproduce giant forms (Fig. 3, B and C), and it wasa rather gradual size increase and a similar pace

Sulej et al., Science 363, 78–80 (2019) 4 January 2019 2 of 3

Fig. 2. Comparison of the reconstructed pectoral girdle of Lisowiciabojani with another dicynodont, dinosaur, and recent mammal.(A) Position of bones of L. bojani in anterior and lateral views. Someproportions of the bones were estimated by means of comparisonwith articulated skeletons of Parakannemeyeria (IVPP V. 979) andSinokannemeyeria (IVPP V.974), but most were inferred from the size

of articulation areas. (B) Reconstruction of large dicynodont Stahleckeria(GPIT/RE/8001) in anterior and lateral views. (C and D) Hypotheticalflexibility of the humerus in protraction-retraction. (E) Reconstructionof rhinoceros Diceros in anterior and lateral views based on MPUWr 502223.(F) Reconstruction of Triceratops in anterior and lateral views based on(27). Scale bars, 10 cm.

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to that observed in the evolution of herbivorousdinosaurs in the Mesozoic and mammalian line-ages in the mid-late Paleogene (26). All suggestthat in the Late Triassic, there was a substantialtemporal overlap in the occurrence of very largeherbivores: the previously dominant dicynodontsand their emerging ecological analogs amongarchosaurs, the sauropodomorph dinosaurs.

REFERENCES AND NOTES

1. H.-D. Sues, N. C. Fraser, Triassic Life on Land: The GreatTransition (Columbia Univ. Press, 2010).

2. G. M. King, Anomodontia, Encyclopedia of Paleoherpetology(Part 17C) (Gutsav Fischer Verlag, 1988).

3. Z. Kielan-Jaworowska, R. L. Cifelli, Z.-X. Luo, Mammals fromthe Age of Dinosaurs: Origins, Evolution, and Structure(Columbia Univ. Press, 2004).

4. T. S. Kemp, The Origin and Evolution of Mammals (Oxford Univ.Press, 2005).

5. J. Fröbisch, Earth Sci. Rev. 95, 119–157 (2009).6. J. Fröbisch, PLOS ONE 3, e3733 (2008).7. A. R. Fiorillo, K. Padian, C. Musikasinthorn, Palaios 15, 373–386

(2000).8. R. R. Schoch, Neues Jahrb. Geol. Palaontol. Abh. 263, 119–123

(2012).9. M. W. Maisch, C. S. Vega, R. R. Schoch, Palaeodiversity 2,

271–278 (2009).10. J. Dzik, T. Sulej, G. Niedźwiedzki, Acta Palaeontol. Pol. 53,

733–738 (2008).

11. T. Sulej, R. Bronowicz, M. Tałanda, G. Niedzwiedzki, Proc. R.Soc. Edinb. 101, 261–269 (2011).

12. J. Fröbisch, Can. J. Earth Sci. 43, 1297–1308 (2006).13. L. R. Walter, in The Beginning of the Age of Dinosaurs

(Cambridge Univ. Press, 1986), pp. 89–97.14. N. E. Campione, D. C. Evans, BMC Biol. 10, 60 (2012).15. D. Macdonald, The New Encyclopedia of Mammals (Oxford

Univ. Press, 2001).16. A. M. Yates, Palaeontology 46, 317–337 (2003).17. P. M. Sander et al., Biol. Rev. Camb. Philos. Soc. 86, 117–155

(2011).18. A. M. Yates, J. W. Kitching, Proc. Biol. Sci. 270, 1753–1758

(2003).19. P. C. Sereno, Science 284, 2137–2147 (1999).20. R. B. Sookias, R. J. Butler, R. B. J. Benson, Proc. Biol. Sci. 279,

2180–2187 (2012).21. Ch. F. Kammerer, Palaeontologia Africana 52, 102–128 (2018).22. C. F. Kammerer, J. Fröbisch, K. D. Angielczyk, PLOS ONE 8,

e64203 (2013).23. A. A. Biewener, Science 245, 45–48 (1989).24. G. Niedźwiedzki, P. Gorzelak, T. Sulej, Lethaia 44, 87–92

(2011).25. P. Bajdek, K. Owocki, G. Niedźwiedzki, Palaeogeogr.

Palaeoclimatol. Palaeoecol. 411, 1–17 (2014).26. D. Prothero, Rhinoceros Giants: The Palaeobiology of

Indricotheres (Indiana Univ. Press, 2013).27. S. Fujiwara, J. Vertebr. Paleontol. 29, 1136–1147 (2009).

ACKNOWLEDGMENTS

We thank J. Dzik (Institute of Paleobiology, PAS) for proposingthis research and support, M. Dec (Institute of Paleobiology,

PAS) for help with preparation of dicynodont shoulder girdlevirtual model, P. E. Ahlberg (Uppsala University) for discussion,D. Snitting (Uppsala University) for help with phylogeneticand computed tomography data, N. Campione (Universityof New England) for his help with body mass estimate, andK. Zaremba-Niedźwiedzka (Uppsala University) for help duringpreparation of the manuscript. We are very thankful toanonymous reviewers whose comments radically improvedthe final version of the paper. Funding: The study was supportedby Polish grant (2012/07/B/NZ8/02707) and SwedishVetenskapsrådet grant (2017-05248). Author contributions:T.S. designed the study. T.S. and G.N. performed thecomparative and analytical work, participated in morphologicalstudies, and wrote the paper. Competing interests: The authorsdeclare no competing interests. Data and materialsavailability: All described specimens are accessioned at theInstitute of Paleobiology, PAS (Poland).

SUPPLEMENTARY MATERIALS

www.sciencemag.org/content/363/6422/78/suppl/DC1Materials and MethodsSupplementary TextFigs. S1 to S16Tables S1 to S7References (28–74)Movies S1 to S4

28 November 2016; resubmitted 4 August 2018Accepted 19 October 2018Published online 22 November 201810.1126/science.aal4853

Sulej et al., Science 363, 78–80 (2019) 4 January 2019 3 of 3

Fig. 3. Phylogeny ofkannemeyeriiformdicynodonts and itsrelationship with thechanges in femurlength of dicynodontsand sauropodomorphs.(A) Time-calibratedphylogeny of the Triassicdicynodonts simplifiedafter (22) (numerical agesfor the base and top ofNorian are based on theChronostratigraphic Chartof the ICS v. 2018/8)with position of L. bojani.(B) Femur length(body size proxy) ofsauropodomorph (blacksquares) and dicynodont(gray circles) taxa from theMiddle to Late Triassicplotted at the stratigraphicrange midpoints for eachtaxon. (C) Comparisonof dicynodont femur bones(1, 2, ZPAL V.33/763,Lisowicia; 3, UCMP 32394,Placerias; 4, MCZ 37858M, Ischigualastia;5, MCN PV 3600,Dinodontosaurus; 6, GPIT/RE/8002, Stahleckeria).

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An elephant-sized Late Triassic synapsid with erect limbsTomasz Sulej and Grzegorz Niedzwiedzki

originally published online November 22, 2018DOI: 10.1126/science.aal4853 (6422), 78-80.363Science 

, this issue p. 78Sciencemegaherbivores in the Triassic were not only dinosaurs.

like modern mammals. Thus,−−that is as large as some coexisting dinosaurs and appears to have had an erect gait nd retained a sprawling gait. Sulej and Niedzwiedzki, however, describe a dicynodont from the Late Triassic of Poland

end-Permian extinction (about 252 million years ago). The few groups that survived into the Triassic were mostly small aand the synapsids, which led to mammals. Synapsids were diverse during the Permian but were greatly reduced after the

Early terrestrial amniotes evolved into two groups: the sauropsids, which led to the bird and dinosaur lineages,A proto-mammalian giant

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