Thoughts on paper by D'Emic (2023) regarding evolution of huge body size in sauropods

For generations, sauropod dinosaurs have starred in the popular imagination as the biggest land animals to ever walk the Earth, with interest in giant sauropods going back to the 1970s and 1980s with the discovery of the derived titanosaur Argentinosaurus and the diplodocids Diplodocus (=Seismosaurus) hallorum and Supersaurus (the giant rebbachisaurid Maraapunisaurus was seen in some publications as possibly the biggest-ever sauropod, although the missing nature of the holotype dorsal vertebra made size estimates of 190 feet guesswork, but Carpenter [2018] revised the size estimate of this genus to 105 feet, which makes sense because the initial size estimates of 170 feet for Diplodocus  hallorum was later revised to 110 feet). While children and adults alike marvel at the huge size of sauropods compared to elephants, rhinoceroses, and the extinct paraceratheres, I have not forgotten the fact that some sauropods living on island arcs in southern Europe during the Late Cretaceous which today are part of France, Spain, and Romania exhibited insular dwarfism, and that not all sauropods approached the body sizes attained by Apatosaurus, Brachiosaurus, Brontosaurus, Diplodocus, Galeamopus, Giraffatitan, and Supersaurus. Recently, D'Emic (2023) published a new paper illuminating the evolution of body size among sauropod taxa, relying on measurements of the circumferences of sauropod limb bones to propose that massive body size evolved convergently in multiple sauropod clades, while noting that select taxa of sauropods showed decreasing trends in body size. Having had the chance to read this paper, there are some noteworthy observations from the study that I wish to emphasize in detail. 

As admitted by D'Emic (2023), the patchy sauropod fossil record has constrained the focus on sauropod body size evolution to less than half of the approximately 250 described sauropod taxa, but the fact that Franz Nopcsa's interpretation of Magyarosaurus as a dwarf taxon has been vindicated by several studies (e.g. Benton et al. 2010; Stein et al. 2010) along with the small size of the short-necked dicraeosaurid Brachytrachelopan and the dwarf brachiosaurid Europasaurus shows that diminutive body size was present in more than one eusauropod clade. Although Cope's rule says that tetrapod lineages tend to increase in body size over time, it should be noted that when Edward Drinker Cope and Othniel Charles Marsh described to science the sauropod fauna of the Morrison Formation in western North America, they did not foresee that a few sauropod taxa of diminutive body size would be named in a handful of publications long after their deaths, and Magyarosaurus would be the first sauropod to be described that deviates from Cope's rule when it comes to body size in sauropods. With respect to the argument by D'Emic that the evolutionary cascade hypothesis put forward by Sander (2013) to interpret gigantism in some sauropods as being driven by anatomical and physiological innovations stemming from a nested array of historical prerequisites is best explained by ecological and life-history factors rather than any shared morphological traits, I should emphasize that the co-existence of dwarf and gigantic titanosaurs in the Late Cretaceous of Romania, Spain, and France (Stein et al. 2010; Vila et al. 2022) lends support to D'Emic's conclusion that ecological and life-history factors influenced the degree of dwarfism or gigantism among sauropod clades by showing that the insular nature of the ecosystems of the Ibero-Armorican island and Hațeg Island didn't necessarily translate into uniform dwarfism among titanosaur taxa from the Late Ceretaceous of Europe. For instance, Vila et al. (2022) note that the holotype of Abditosaurus kuehnei is substantially larger than specimens of other titanosaur taxa from the Ibero-Armorican Island as well as titanosaur specimens from the Hațeg Island, indicating that Cope's rule might apply to the evolution of body size in titanosaurs over the course of the Maastrichtian in southern Europe.

Phenogram of sauropod body size evolution over the course of the Mesozoic (from D'Emic 2023). Note that the lineages of the six eusauropod lineages that surpassed the maximum mammalian body mass are denoted by longitudinal lines highlighted in different colors (light green=non-neosauropod eusauropods; dark green=turiasaurians; blue=diplodocoids; orange=basal macronarians and non-titanosaur somphospondyls; purple=brachiosaurids; red=titanosaurs).

According to D'Emic, a total of 36 sauropod lineages independently evolved huge body sizes greater than those of other terrestrial tetrapods from the Mesozoic and Cenozoic, 32 of them belonging to the clade Neosauropoda. The discovery of isolated postcranial remains from the Bajocian-Callovian age Dongdaqiao Formation of Tibet belonging to a eusauropod over 66 feet (20 meters) long (Wei et al. 2023), two gigantic eusauropod cervical vertebrae from the Shishugou Formation of Xinjiang indicating a eusauropod 115 feet (35 meters) in length (which are referred to Mamenchisaurus sinocanadorum by Paul [2019] but considered to be of indeterminate taxonomic placement by Moore et al. [2023]), and a maximum size estimate of 105 feet (32 meters) for the Middle Jurassic mamenchisaurid Xinjiangtitan given by Wu et al. (2013), indicate that gigantic body size evolved in more than one clade of non-turiasaurian, non-neosauropod eusauropods during the Middle Jurassic, although the limited amount of material known for Mamenchisaurus sinocanadorum renders the exact size of this taxon unclear. The gigantic size of Turiasaurus relative to that of other turiasaurs makes me feel tempted to suggest that the rate of body size evolution in Turiasauria is inconsistent with Cope's rule because of the medium body size of the Early Cretaceous turiasaurs Mierasaurus and Moabosaurus and small body size of the Late Jurassic form Amanzia from Switzerland (Schwarz et al. 2020), the minor age difference between  Turiasaurus and the Yellow Cat Member of the Cedar Mountain Formation yielding Mierasaurus and Moabosaurus could suggest large-bodied turiasaurs might survived into the Valanginian-Barremian interval and that the small size of Amanzia can be best explained as a result of insular dwarfism given that much of western and central Europe was covered by seas during the Late Jurassic.

References:

Benton, M.J., Csiki, Z., Grigorescu, D., Redelstorff, R., Sander, P.M., Stein, K., and Weishampel, D.B., 2010. Dinosaurs and the island rule: The dwarfed dinosaurs from Haţeg Island. Palaeogeography, Palaeoclimatology, Palaeoecology 293 (3): 438–454. doi:10.1016/j.palaeo.2010.01.026

Carpenter, K, 2018. Maraapunisaurus fragillimus, N.G. (formerly Amphicoelias fragillimus), a basal Rebbachisaurid from the Morrison Formation (Upper Jurassic) of Colorado. Geology of the Intermountain West 5: 227–244.

D'Emic, M. D., 2023. The evolution of maximum terrestrial body mass in sauropod dinosaurs. Current Biology 33 (9): R349–R350. doi:10.1016/j.cub.2023.02.067

Paul, G.S., 2019. Determining the largest known land animal: A critical comparison of differing methods for restoring the volume and mass of extinct animals. Annals of the Carnegie Museum 85 (4): 335–358. doi:10.2992/007.085.0403

Sander, P.M., 2013. An Evolutionary Cascade Model for Sauropod Dinosaur Gigantism - Overview, Update and Tests. PLoS ONE 8(10): e78573. https://doi.org/10.1371/journal.pone.0078573

Schwarz, D., Mannion, P.D., Wings, O., and Meyer, C.A., 2020. Re-description of the sauropod dinosaur Amanzia (‘Ornithopsis/Cetiosauriscus’) greppini n. gen. and other vertebrate remains from the Kimmeridgian (Late Jurassic) Reuchenette Formation of Moutier, Switzerland. Swiss Journal of Geosciences 113: 2. https://doi.org/10.1186/s00015-020-00355-5

Stein, K., Csiki, Z., Curry Rogers, K., Weishampel, D.B., Redelstorff, R., Carballidoa, J.L., and Sander, P.M., 2010. Small body size and extreme cortical bone remodeling indicate phyletic dwarfism in Magyarosaurus dacus (Sauropoda: Titanosauria). Proceedings of the National Academy of Sciences of the United States of America 107 (20): 9258–9263. doi:10.1073/pnas.1000781107

Vila, B., Sellés, A., Moreno-Azanza, M., Razzolini, N.L., Gil-Delgado, A., Canudo, J.I., and Galobart, A., 2022. A titanosaurian sauropod with Gondwanan affinities in the latest Cretaceous of Europe. Nature Ecology & Evolution 6: 288-296. doi:10.1038/s41559-021-01651-5.

Wei, X.-F.; Wang, Q.-Y., An, X.-Y., Wang, B.-D., Zhang, Y.-J., Mou, C.-L., Li, Y., Wang, D.-B., Ma, W., and Kundrát, M., 2023. New sauropod remains from the Middle Jurassic Dongdaqiao Formation of Qamdo, eastern Tibet. Palaeoworld: in press. doi:10.1016/j.palwor.2023.02.002

Wu, W.H., Zhou, C.F., Wings, O., Sekiya, T., and Dong, Z.M., 2013. A new gigantic sauropod dinosaur from the Middle Jurassic of Shanshan, Xinjiang. Global Geology 32: 437–446.

Did early titanosaurs have non-procoelous anterior caudals and broad-crowned teeth? My thoughts on Poropat et al. 2023 paper

I remember that the description of  Rapetosaurus from Madagascar in the early 2000s demonstrated that the supposed late-surviving diplodocoids Nemegtosaurus and Quaesitosaurus are derived titanosaurs, the morphological similarities of the skulls of these taxa to diplodocids stemming from convergent evolution. Ironically, very few non-lithostrotian somphospondyl taxa preserve cranial remains, namely Diamantinasaurus, Euhelopus, Liaoningotitan, Ligabuesaurus, Mongolosaurus,  Phuwiangosaurus, Sarmientosaurus, and Tambatitanis, and the dearth of cranial remains for both basal titanosaurs and basal somphospondyls has been an obstacle to better understanding the ancestral cranial Bauplan of the most primitive titanosaurs, although Sarmientosaurus has a skull morphologically intermediate between that of basal titanosauriforms and derived titanosaurs. Recently, Poropat et al. (2023) have described a new specimen of Diamantinasaurus matildae (recovered by Poropat et al. [2021] as the sister taxon of Sarmientosaurus and Savannasaurus in the new titanosaur clade Diamantinasauria) preserving a nearly complete skull, AODF 906, illuminating aspects of the skull anatomy of this genus not preserved in referred Diamantinasaurus matildae specimen AODF 836 (described in detail by Poropat et al. 2021). Since AODF 906 reveals that Diamantinasaurus had a Sarmientosaurus-like skull and non-procoelous anterior caudal vertebrae, I have an opportunity to investigate whether the most primitive titanosaurs had broad, spatulate teeth and non-procoelous anterior caudals.

Equal-weights cladistic analysis of Diamantinasaurus matildae based on new morphological information from referred specimen AODF 906 (after Poropat et al. 2023). The figure drawings of Diamantinasaurus and Sarmientosaurus in the cladogram highlight the greater height of the rear skull relative to the snout distinguishing diamantinasaurians from lithrostrotian taxa for which skull material is known.  

In their paper erecting the name Diamantinasauria for the non-lithostrotian titanosaur clade formed by Diamantinasaurus, Sarmientosaurus, and Savannasaurus, Poropat et al. (2021) listed amphicoelous anterior caudal vertebrae as one of the distinguishing features of Diamantinasauria, but stressed that amphicoelous anterior caudals could only be assessed in Savannasaurus in contrast to the holotypes of Diamantinasaurus matildae and Sarmientosaurus musacchioi as well as referred D. matildae specimen AODF 836 lacking caudal remains even though Andesaurus has been consistently recovered as a basal titanosaur, raising the question of whether the presence of slight procoely in the anterior caudals of Andesaurus represents an independent morphological acquisition from lithostrotian titanosaurs. As Carballido et al. (2022) point out, Andesaurus has been consistently recovered as a basal titanosaur in nearly all titanosaur phylogenies, but its phylogenetic instability in some recent cladistic studies renders its role as a phylogenetic exemplar for basal Titanosauria labile, and it should be noted that the holotype of Andesaurus delgadoi is incomplete, which raises the possibility that future discoveries could render Andesaurus less basal within Titanosauria but still outside Lithostrotia. Indeed, the cladistic analysis of the titanosaur Ruixinia by Mo et al. (2023) places Andesaurus in a basal titanosaur clade that also includes Dongyangosaurus, Huabeisaurus, and Tambatitanis in a basal clade of Titan, and because Baotianmansaurus, Dongyangosaurus, Huabeisaurus and Tambatitanis share with Diamantinasaurus and Savannasaurus the presence of amphicoelous anterior caudals, it is possible that slightly procoelous in the anterior caudals of Andesaurus constitutes an autapomorphy among non-lithostrotian titanosaurs, since Poropat et al. (2023) recover Baotianmansaurus, Dongyangosaurus, and Huabeisaurus basally within Titanosauria outside Lithostrotia, like the clade Diamantinasauria. Although Hamititan from the Early Cretaceous of Xinjiang (Wang et al. 2021) is much older than Andesaurus and Diamantinasaurus, it differs from diamantinasaurians in having strongly procoelous caudal vertebrae, suggesting that some early titanosaurs had strongly procoelous anterior caudals and that others had either amphicoelous or opisthocoelous anterior caudal vertebrae because the anterior caudal vertebrae of Ninjatitan from the earliest Cretaceous of Argentina is slightly procoelous like Andesaurus (Gallina at al. 2021).

As noted by Poropat et al. (2021), the cranial material of the Diamantinasaurus matildae specimen AODF 836 is similar to the holotype of Sarmientosaurus musacchioi in having a quadratojugal with a posterior tongue-like process, a braincase with more than one ossified exit for cranial nerve V, and compressed and conical chisel-shaped teeth, but the new D. matildae specimen described by Poropat et al. (2023) demonstrates that the skull of diamantinasaurian titanosaurs was taller and acutely elevated relative to the snout, and that members of Diamantinasauria have robust dentigerous elements. I earlier mentioned that Euhelopus, Liaoningotitan, Mongolosaurus, Phuwiangosaurus, and Tambatitanis are the only non-lithostrotian somphospondyls besides diamantinasaurians that preserve extensive cranial remains, but the skulls of Diamantinasaurus and Sarmientosaurus are similar in every respect to those of brachiosaurids and differ from Euhelopus in having narrower tooth crowns, although they are not as slender as that of the basal somphospondylan Phuwiangosaurus (for which one referred specimen containing cranial and dental elements is known) or derived titanosaurs (Poropat et al. 2022, 2023). The occurrence of a relatively broad-crowned titanosauriform tooth in Santonian-age deposits in Hungary (Ősi et al. 2017) and the presence of broad-crowned teeth in the lithostrotian titanosaur Ampelosaurus (Le Loeuff 2005), in tandem with the spatulate teeth of Euhelopus and the fairly narrow tooth crowns of Diamantinasaurus, Huabeisaurus, Sarmientosaurus, and Tambatitanis, could indicate that the tooth crowns of the earliest and most primitive titanosaurs were more similar to those of Camarasaurus and Euhelopus, especially considering that the teeth of Diamantinasaurus, Huabeisaurus, Sarmientosaurus, and Tambatitanis are not as slender as those of lithostrotians such as Nemegtosaurus, Quaesitosaurus, Rapetosaurus, and Tapuiasaurus. Although the holotype of the basal somphospondyl Yongjinglong datangi does not preserve any cranial remains, it does include three teeth, all of which are somewhat similar to Euhelopus, and the basal somphospondyl Sibirotitan also had broad tooth crowns (Poropat et al. 2022). Therefore, broad-crowned teeth are most probably symplesiomorphic for the most primitive titanosaurs and a few derived titanosaurs, with conical chisel-shaped teeth and slender pencil-shaped teeth being derived states for Titanosauria. 

References:

Carballido, J.L., Otero, A., Mannion, P.D., Salgado, L., and Moreno, A.P., 2022. Titanosauria: A Critical Reappraisal of Its Systematics and the Relevance of the South American Record. pp. 269–298. In: Otero, A., Carballido, J.L., and Pol, D. (eds.). South American Sauropodomorph Dinosaurs. Record, Diversity and Evolution. Cham, Switzerland: Springer. ISBN 978-3-030-95958-6

Gallina, P. A., Canale, J. I., and Carballido, J. L., 2021. The Earliest Known Titanosaur Sauropod Dinosaur. Ameghiniana 58 (1): 35–51. doi:10.5710/AMGH.20.08.2020.3376.

Le Loeuff, J., 2005. Osteology of Ampelosaurus atacis (Titanosauria) from Southern France. pp. 115–137. In: Tidwell, V., and Carpenter, K. (eds.). Thunder-Lizards: The Sauropodomorph Dinosaurs. Bloomington: Indiana University Press. ISBN 978-0-253-34542-4.

Mo, J., Ma, F., Yu, Y., and Xu, X., 2023. A new titanosauriform sauropod with an unusual tail from the Lower Cretaceous of northeastern China. Cretaceous Research 144: 105449.  doi:10.1016/j.cretres.2022.105449.

Ősi, A., Csiki-Sava, Z., and Prondvai, E., 2017. A sauropod tooth from the Santonian of Hungary and the European Late Cretaceous 'Sauropod Hiatus.' Scientific Reports 7: 3261. https://doi.org/10.1038/s41598-017-03602-2 

Poropat, S. F., Kundrát, M., Mannion, P. D., Upchurch, P., Tischler, T. R., and Elliott, D. A., 2021. Second specimen of the Late Cretaceous Australian sauropod dinosaur Diamantinasaurus matildae  provides new anatomical information on the skull and neck of early titanosaurs. Zoological Journal of the Linnean Society 192 (2): 610-674. doi:10.1093/zoolinnean/zlaa173 

Poropat, S.F., Frauenfelder, T.G., Mannion, P.D., Rigby, S.L., Pentland, A.H., Sloan, T. and Elliott, D.A., 2022. Sauropod dinosaur teeth from the lower Upper Cretaceous Winton Formation of Queensland, Australia and the global record of early titanosauriforms. Royal Society Open Science 9: 220381.

Poropat, S. F., Mannion, P. D., Rigby, S. L., Duncan, R. J., Pentland, A. H., Bevitt, J. J., Sloan, T., and Elliott, D. A., 2023. A nearly complete skull of the sauropod dinosaur Diamantinasaurus matildae from the Upper Cretaceous Winton Formation of Australia and implications for the early evolution of titanosaurs. Royal Society Open Science 10(4): 221618. https://doi.org/10.1098/rsos.221618   

Wang, X., Bandeira, K. L. N., Qiu, R., Jiang, S., Cheng, X., Ma, Y., and Kellner, A.W.A., 2021. The first dinosaurs from the Early Cretaceous Hami Pterosaur Fauna, China. Scientific Reports 11:14962. doi:10.1038/s41598-021-94273-7.