Skip to main content
Log in

The Early Cretaceous frog Genibatrachus from China: Osteology, development, and palaeogeographic relations

  • Original Paper
  • Published:
Palaeobiodiversity and Palaeoenvironments Aims and scope Submit manuscript

Abstract

A thorough anatomical description of the Early Cretaceous frog Genibatrachus is presented, based on 84 fully grown adults and 75 metamorphosing larvae and juveniles. The most distinguishing cranial characters of the adults are premaxillae with a bifurcated facial portion, a pair of frontoparietals contacting one another through a median suture posteriorly but separated by a median fontanelle anteriorly, and free palatines. The postcranial skeleton is characterised by eight amphicoelous presacral vertebrae and an anteriorly convex sacral vertebra, by three pairs of free ribs on V2–V4 (those on V2 small and hook-like, and those on V3 provided with spike-like uncinate processes), by poorly ossified caput humeri even in fully grown adults, praepollex consisting of two segments (the distal one being strongly expanded), and by the tibiale and fibulare fused together at both ends. The development of Genibatrachus is characterised by the same degree of ossification in the forelimbs and hind limbs, no apparent developmental gradient within the vertebral column, and a pelvic girdle arising within the sacral region of the vertebral column, not behind it. The posteromedial processes of the hyoid ossify early, before the end of metamorphosis (when the vestigial tail is still present). The end of metamorphosis is marked by the establishment of a sutural contact between the ilia. The parahyoid is poorly ossified, relatively common among juveniles (from SVL 24 mm), but not reliably discerned in fully grown adults. Genibatrachus seems to be related to coeval Hyogobatrachus and Tambabatrachus from Japan, and to extant Alytoidea, but differs from Liaobatrachus (e.g. by the number of presacral vertebrae). Some skeletal characteristics (e.g. bicondylar sacro-urostylar joint) suggest that Genibatrachus was capable of jumping.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

Fossils that support the conclusions of this study are deposited in the collections of the Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China, under the collection numbers listed in the Material and Methods section.

References

  • Abourachid, A., & Green, D. M. (1999). Origins of the frog-kick? Alternate-leg swimming in primitive frogs, families Leiopelmatidae and Ascaphidae. Journal of Herpetology 33, 657–663.

    Article  Google Scholar 

  • Agnolin, F. A., Carvalho, I. S., Rolando, A. M. A., Novas, F. E., Xavierneto, J., Andrade, J. A. F. G., & Freitas, F. I. (2020). Early Cretaceous neobatrachian frog (Anura) from Brazil sheds light on the origin of modern anurans. Journal of South American Earth Sciences, 101, 102633.

    Article  Google Scholar 

  • Ascarrunz, E., Rage, J.-C., Legreneur, P., & Laurin, M. (2016). Triadobatrachus massinoti, the earliest known lissamphibian (Vertebrata: Tetrapoda) re-examined by μCT scan, and the evolution of trunk length in batrachians. Contributions to Zoology, 85, 201–234.

    Article  Google Scholar 

  • Averianov, A. O., Voronkevich, A. V., Leshchinskiy, S. V., & Fayngertz, A. V. (2006). A Ceratopsian dinosaur Psittacosaurus sibiricus from the Early Cretaceous of West Siberia, Russia and its phylogenetic relationships. Journal of Systematic Palaeontology, 4, 359–395. https://doi.org/10.1017/S1477201906001933.

  • Báez, A. M. (2013). Anurans from the Early Cretaceous Lagerstätte of Las Hoyas, Spain: New evidence on the Mesozoic diversification of crown-clade Anura. Cretaceous Research, 41, 90–106.https://doi.org/10.1016/j.cretres.2012.11.002.

    Article  Google Scholar 

  • Báez, A. M., & Basso, N. G. (1996). The earliest known frogs of the Jurassic of South America: Review and cladistic appraisal of their relationships. Münchner geowissenschaftliche Abhandlungen, A, 30, 131-158.

    Google Scholar 

  • Báez, A. M., & Gómez, R. O. (2016). Revision of the skeletal morphology of Eodiscoglossus santonjae, an Early Cretaceous frog from northeastern Spain, with comments on its phylogenetic placement. Fossil Imprint, 72, 67–77.

    Article  Google Scholar 

  • Báez, A. M., & Gómez, R. O. (2019). Redescription of the overlooked basal frog Wealdenbatrachus reveals increased diversity among Early Cretaceous anurans. Cretaceous Research, 99, 14–29.

    Article  Google Scholar 

  • Báez, A. M., & Nicoli, L. (2004). A new look at an old frog: the Jurassic Notobatrachus Reig from Patagonia. Ameghiniana, 41, 257–270.

    Google Scholar 

  • Báez, A. M., & Sanchiz, B. (2007). A review of Neusibatrachus wilferti, an Early Cretaceous frog from the Montsec Range, northeastern Spain. Acta Palaeontologica Polonica, 52, 477–487.

    Google Scholar 

  • Báez, A. M., Moura, G. J. B., & Gómez, R. O. (2009). Anurans from the Lower Cretaceous Crato Formation of northeastern Brazil: implications for the early divergence of neobatrachians. Cretaceous Research, 30, 829–846. https://doi.org/10.1016/j.cretres.2009.01.002.

    Article  Google Scholar 

  • Baleeva, N. V. (2001). Formation of the scapular part of the pectoral girdle in anuran larvae. Russian Journal of Herpetology, 8, 195–204.

    Google Scholar 

  • Blanco, M. J., & Sanchiz, B. (2000). Evolutionary mechanisms of rib loss in anurans: A comparative developmental approach. Journal of Morphology, 244, 57–67.

    Article  Google Scholar 

  • Bolkay, S. J. (1919). Osnove uporedne osteologije anurskih batrahija. Glasnik Zemaljskog muzeja u Bosni i Hercegovini (1919), 277–356. https://www.scribd.com/doc/56352465/Glasnik-Zemaljskog-Muzeja-1919-Knjiga-3.

  • Chang, M.-M., Chen, P.-J., Wang,Y.-Q., & Wang, Y. (2008). The Jehol Fossils. The emergence of feathered dinosaurs, beaked birds and flowering plants. London and New York: Academic Press.

  • Clarke, B. T. (2007). Comparative morphology and amphibian taxonomy: an example from the osteology of discoglossid frogs. In H. Heatwole & M. Tyler (Eds.), Amphibian Biology. (Systematics, pp. 2465–2612). Chipping Norton: Surrey Beatty & Sons.

  • Dijk, E. van (2002) Longitudinal sliding articulations in pipid frogs. South African Journal of Science, 98, 555–556.

    Google Scholar 

  • Dong, L., Roček, Z., Wang, Y., & Jones, M. E. H. (2013). Anurans from the Lower Cretaceous Jehol Group of Western Liaoning, China. PloS One, 8, e69723.

    Article  Google Scholar 

  • Emerson, S. B. (1979). The ilio-sacral articulation in frogs: form and function. Biological Journal of the Linnean Society, 11, 153–168.

    Article  Google Scholar 

  • Emerson, S. B., & De Jongh, H. J. (1980). Muscle activity at the ilio-sacral articulation of frogs. Journal of Morphology, 166, 129–144.

    Article  Google Scholar 

  • Essner Jr. R. L., Suffian, D. L., Bischop, P. J., & Reilly, S. M. (2010). Landing in basal frogs: evidence of saltational patterns in the evolution of anuran locomotion. Naturwissenschaften, 97, 935–939. https://doi.org/10.1007/s00114-010-0697-4.

    Article  Google Scholar 

  • Estes, R, Špinar, Z. V., & Nevo, E. (1978). Early Cretaceous pipid tadpoles from Israel (Amphibia: Anura). Herpetologica, 34, 374–393.

    Google Scholar 

  • Evans, S. E., & Manabe, M. (1998). Early Cretaceous frog remains from the Okurodani Formation, Tetori Group, Japan. Paleontological Research, 2, 275–278.

    Google Scholar 

  • Fey, B. (1988). Die Anurenfauna aus der Unterkreide von Uña (Ostspanien). Berliner geowissenschaftliche Abhandlungen, 104 (A), 1–125.

  • Fuchs, H. (1929) Über das Os parahyoideum der anuren Amphibien und der Crossopterygier; nebst Bemerkungen über phylogenetische Wanderungen der Haut- und Deckknochen. Gegenbaurs Morphologisches Jahrbuch, 63, 408–453.

    Google Scholar 

  • Gans, C., & Parsons, T. S. (1966). On the origin of the jumping mechanism in frogs. Evolution, 20, 92–99.

    Article  Google Scholar 

  • Gao, K.-Q., & Chen, S. (2004). A new frog (Amphibia: Anura) from the Lower Cretaceous of western Liaoning, China. Cretaceous Research, 25, 761–769. https://doi.org/10.1016/j.cretres.2004.06.011.

    Article  Google Scholar 

  • Gao, K.-Q., & Chen, J. (2017). A new crown-group frog (Amphibia: Anura) from the Early Cretaceous of northeastern Inner Mongolia, China. American Museum Novitates, 3876, 1e39. https://doi.org/10.1206/3876.1.

  • Gao, K.-Q., Li, Q.-G., Wei, M., Pak, H., & Pak, I. (2009). Early Cretaceous birds and pterosaurs from the Sinuijui Series, and geographic extension of the Jehol Biota into the Korean Peninsula. Journal of the Paleontological Society of Korea, 25, 57–71.

    Google Scholar 

  • Gao, K., & Wang, Y. (2001). Mesozoic anurans from Liaoning Province China, and phylogenetic relationships of archaeobatrachian anuran clades. Journal of Vertebrate Paleontology, 21, 460–476.

    Article  Google Scholar 

  • Gardner, J. D., Roček, Z., Přikryl, T., Eaton, J. G., Blob, R. W., & Sankey, J. T. (2010). Comparative morphology of the ilium of anurans and urodeles (Lissamphibia) and a re-assessment of the anuran affinities of Nezpercius dodsoni Blob et al., 2001. Journal of Vertebrate Paleontology, 30, 1684–1696. https://doi.org/10.1080/02724634.2010.521605.

    Article  Google Scholar 

  • Gaupp, E. (1896). Anatomie des Frosches. Lehre vom Skelett und vom Muskelsystem. Brauschweig. https://www.biodiversitylibrary.org/item/25840#page/5/mode/1up

  • Gómez, R. O., & Lires, A. I. (2019). High ecomorphological diversity among Early Cretaceous frogs from a large subtropical wetland of Iberia. Comptes Rendus Palevol, 18, 711–723.

    Article  Google Scholar 

  • Gosner, K. L. (1960). A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183–190.

    Google Scholar 

  • Grabau, A. W. (1928). Stratigraphy of China. Part II. Mesozoic. Beijing: Geological Survey of China.

  • Gu, Z.-W. (1962). The Jurassic and Cretaceous of China. Beijing: Science Press. [In Chinese]

    Google Scholar 

  • Hecht, M. K. (1970). The morphology of Eodiscoglossus, a complete Jurassic frog. American Museum Novitates, 2424, 1–17.

    Google Scholar 

  • Ikeda, T., Ota, H., & Matsui, M. (2016). New fossil anurans from the Lower Cretaceous Sasayama Group of Hyogo Prefecture, Western Honshu, Japan. Cretaceous Research, 61, 108–123. https://doi.org/10.1016/j.cretres.2015.12.024.

    Article  Google Scholar 

  • Jarvik, E. (1996). The Devonian tetrapod Ichthyostega. Fossils Strata, 40, 1–213.

    Article  Google Scholar 

  • Jenkins Jr., F., & Shubin, N. H. (1998). Prosalirus bitis and the anuran caudopelvic mechanism. Journal of Vertebrate Paleontology, 18, 495–510.

    Article  Google Scholar 

  • Ji, S., & Ji, Q. (1998). The first Mesozoic frog from China (Amphibia: Anura). Chinese Geology, 250, 39–42. [in Chinese, with English abstract]

  • Jones, M. E. H., Evans, S.E., & Sigogneau-Russel, D. (2003). Early Cretaceous frogs from Morocco. Annals of Carnegie Museum, 72, 65–97.

    Article  Google Scholar 

  • Leal, M. E. C., & Brito, P. M. (2006). Anura do Cretáceo Inferior da Bacia do Araripe, Nordeste do Brasil. In V. Gallo, P. M. Brito, H. M. A. Silva, & F. J. Figueiredo (Eds.), Paleontología de Vertebrados. Grandes Temas e Contribuçoes Científicas (pp. 145–152). Rio de Janeiro.

  • Lebedkina, N. S. (2004). Evolution of the amphibian skull. Advances in amphibian research in the former Soviet Union, 9. Sofia-Moscow, Pensoft.

  • Lires, A. I., Soto, I. M., & Gómez, R.O. (2016). Walk before you jump: new insights on early frog locomotion from the oldest known salientian. Paleobiology, 42, 612–623. https://doi.org/10.1017/pab.2016.11.

    Article  Google Scholar 

  • Moura, P. H. A. G., Costa, F. R., Anelli, L. E., & Nunes, I. (2021). A new genus of fossil frog (Anura) from lower Cretaceous deposits in South America. Annals of the Brazilian Academy of Sciences, 93 (Suppl. 2), e20191560. https://doi.org/10.1590/0001-3765202120201560.

  • Nieuwkoop, P. D., & Faber, J. (1967). Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company.

    Google Scholar 

  • Pan, Y. H., Sha, J. G., Zhou, Z. H., & Fürsich, F. T. (2013). The Jehol Biota: definition and distribution of exceptionally preserved relicts of a continental Early Cretaceous ecosystem. Cretaceous Research, 44, 30–38. https://doi.org/10.1016/j.cretres.2013.03.007.

    Article  Google Scholar 

  • Přikryl, T., Aerts, P., Havelková, P., Herrel, A., & Roček, Z. (2009). Pelvic and thigh musculature in frogs (Anura) and origin of anuran jumping locomotion. Journal of Anatomy, 214, 100–139. https://doi.org/10.1111/j.1469-7580.2008.01006.x.

    Article  Google Scholar 

  • Púgener, L. A., & Maglia, A. M. (1997). Osteology and skeletal development of Discoglossus sardus (Anura: Discoglossidae). Journal of Morphology, 233, 267–286.

    Article  Google Scholar 

  • Ridewood, W. G. (1898). On the development of the hyobranchial skeleton of the Midwife-Toad (Alytes obstetricans). Proceedings of the Zoological Society of London, (1898), 4–12.

    Article  Google Scholar 

  • Ritland R. M. (1955) Studies on the post-cranial morphology of Ascaphus truei. Journal of Morphology, 97, 119–176.

    Article  Google Scholar 

  • Roček, Z. (1974). Veränderungen der Körperproportionalität während des Wachstums im Populationsmuster des Wasserfrosches Rana esculenta (Linnaeus, 1758) (Amphibia: Ranidae). Věstník Československé společnosti zoologické, 38, 215–227.

    Google Scholar 

  • Roček, Z., & Dijk, E. van (2006) Patterns of larval development in Cretaceous pipid frogs. Acta Palaeontologica Polonica, 51, 111–126.

    Google Scholar 

  • Ročková, H., & Roček, Z. (2005). Development of the pelvis and posterior part of the vertebral column in the Anura. Journal of Anatomy, 206, 17–35.

    Article  Google Scholar 

  • Roček, Z., Wang, Y., & Dong, L. (2012). Post-metamorphic development of Early Cretaceous frogs as a tool for taxonomic comparisons. Journal of Vertebrate Paleontology, 32, 1285–1292.

    Article  Google Scholar 

  • Roček, Z., Gardner, J. D., Eaton, J. G., & Přikryl, T. (2013). Anuran ilia from the Upper Cretaceous of Utah – Diversity and stratigraphic patterns. In Titus, A. L, & Loewen, M. A. (Eds.), At the top of the Grand Staircase. The Late Cretaceous of Southern Utah (pp. 273–294). Bloomington & Indianapolis: Indiana University Press.

  • Roček Z., Halámková, L., & Muzzopappa, P. (2021): Developmental dynamics of two closely related species Bombina bombina and B. variegata (Amphibia: Anura) in the context of their fossil evidence. Historical Biology, 33, 3384–3401. https://doi.org/10.1080/08912963.2020.1867979.

    Article  Google Scholar 

  • Roček, Z., Dong, L., Fabrezi, M., Rong, Y., & Wang, Y. (2022). Carpus in Mesozoic anurans: The Early Cretaceous anuran Genibatrachus from northeastern China. Cretaceous Research, 129, 104984.

    Article  Google Scholar 

  • Scotese, C. R. (2013). Map Folio 27, Early Cretaceous, (early Aptian, 121.8 Ma), PALEOMAP PaleoAtlas for ArcGIS, volume 2, Cretaceous Paleogeographic, Paleoclimatic and Plate Tectonic Reconstructions, PALEOMAP Project, Evanston, IL. Retrieved December 14, 2020, from https://www.academia.edu/10604006/Map_Folio_27_Early_Cretaceous_early_Aptian_121_8_Ma_.

  • Schmalhausen, J. J. (1907). Die Entwicklung des Skelettes der vorderen Extremität der Anuren Amphibien. Anatomischer Anzeiger, 31, 177–187. https://www.biodiversitylibrary.org/item/43576#page/191/mode/1up.

  • Scotese, C. R., & Scotese, J. D. (2006). Plate Tectonic Evolution of South America, PALEOMAP Project, Evanston, IL. Retrieved July 18, 2022 from https://www.youtube.com/watch?v=X0AqBCT8n4g.

  • Smirnov, S. V. (1990). Evidence of neoteny: A paedomorphic morphology and retarded development in Bombina orientalis (Anura, Discoglossidae). Zoologischer Anzeiger, 225, 324–332.

    Google Scholar 

  • So, K.-S., Jong, T.-M., Won, C. G., & Jo, S.-D. (2022). A fossil anuran from the Lower Cretaceous Sinuiju Formation, North Phyongan Province, Democratic People's Republic of Korea. Cretaceous Research, 140, 105304. https://doi.org/10.1016/j.cretres.2022.105304.

  • Stephenson, E. M. (1952). The vertebral column and appendicular skeleton of Leiopelma hochstetteri Fitzinger. Transactions of the Royal Society of New Zealand, 79, parts 3-4, 601–631.

  • Stephenson, E. M. (1960). The skeletal characters of Leiopelma hamiltoni McCulloch, with particular reference to the effects of heterochrony on the genus. Transactions of the Royal Society of New Zealand, 88, part 3, 473–488.

  • Stocker, M. R., Nesbitt, S. J., Kligman, B. T., Paluh, D. J., Marsh, A. D., Blackburn, D. C., & Parker, W. G. (2019). The earliest equatorial record of frogs from the Late Triassic of Arizona. Biology Letters, 15, 20180922. https://doi.org/10.1098/rsbl.2018.0922.

    Article  Google Scholar 

  • Tan, K., Lu, L.-W., Chen, X.-Y., & Jin, Y.-G. (2018). New Early Cretaceous Anuran amphibian from Northeast China. Geological Bulletin of China, 37, 1783–1788.

    Google Scholar 

  • Tissier, J., Rage, J.-C., Boistel, R., Fernandez, V., Pollet, N., Garcia, G., & Laurin, M. (2016). Synchrotron analysis of a ‘mummified’ salamander (Vertebrata: Caudata) from the Eocene of Quercy, France. Zoological Journal of the Linnean Society, 177, 147–164.

    Article  Google Scholar 

  • Trewavas, E. (1933). The Hyoid and Larynx of the Anura. Philosophical Transactions of the Royal Society of London B, 222, 401–527.

    Google Scholar 

  • Vergnaud-Grazzini, C., & Wenz, S. (1975). Les discoglossidés du Jurassique supérieur du Montsech (Province de Lérida, Espagne). Annales de Paléontologie (Vertébrés), 61, fasc.1, 19–36.

  • Villalta, J. F. (1954). Novedades paleomastologicas desde el ultimo cursillo (1952) (pp. 1–9). II Cursillo Internacional Paleontologia, Sabadell: Museo de Sabadel.

  • Wuttke, M., Přikryl, T., Ratnikov, V. Y., Dvořák, Z., & Roček, Z. (2012). Generic diversity and distributional dynamics of the Palaeobatrachidae (Amphibia: Anura). Palaeobiodiversity and Palaeoenvironments, 92(3), 367–395. http://dx.doi.org/https://doi.org/10.1007/s12549-012-0071-y.

    Article  Google Scholar 

  • Xing, L., Stanley, E. L., Bai, M., & Blackburn, D. C. (2018). The earliest direct evidence of frogs in wet tropical forests from Cretaceous Burmese amber. Scientific Reports, 8, 8770; https://doi.org/10.1038/s41598-018-26848-w.

  • Xu, X., Zhou, Z., Wang, Y., & Wang, M. (2020). Study on the Jehol Biota: Recent advances and future prospects. Science China Earth Sciences, 63, 757773. https://doi.org/10.1007/s11430-019-9509-3.

  • Yu, Z., Dong, L., Huyskens, M. H., Yin, Q.-Z., Wang, Y., Deng, C., & He, H. (2022). The exceptionally preserved Early Cretaceous “Moqi Fauna” from eastern Inner Mongolia, China, and its age relationship with the Jehol Biota. Palaeogeography, Palaeoclimatology, Palaeoecology, 589, 110824. https://doi.org/10.1016/j.palaeo.2021.110824.

  • Zhou, Z. (2014). The Jehol Biota, an Early Cretaceous terrestrial Lagerstätte: new discoveries and implications. National Science Review 1, 543–559. https://doi.org/10.1093/nsr/nwu055.

    Article  Google Scholar 

  • Zhou, Z.-H., & Wang, Y. (2017). Vertebrate assemblages of the Jurassic Yanliao Biota and the Early Cretaceous Jehol Biota: Comparisons and implications. Palaeoworld, 26, 241–252.

    Article  Google Scholar 

  • Zyl, J. H. M. van (1950). Die Beskrywende en Verglychende Anatomie van die Skedel van Discoglossus pictus (Gravenhorst). Annale Universiteit van Stellenbosch (Ser. A), 26, 1–26.

Download references

Acknowledgements

We are indebted to Tadahiro Ikeda, University of Hyogo, Japan, for providing previously unpublished CT images of Hyogobatrachus and Tambabatrachus, which we used for comparisons with Genibatrachus, and to Jim Gardner, Royal Tyrrell Museum of Palaeontology, Canada, for his final linguistic revision and many useful comments, and to Alfred Lemierre and Raúl Orencio Gómez for taking the time to review our manuscript. This research was supported by the National Natural Science Foundation of China (42288201) and the Strategic Priority Research Programme (B) of the Chinese Academy of Sciences (XDB 18000000) to YW, and by the research plan of the Institute of Geology of the Czech Academy of Sciences (RVO67985831) and by the Chinese Academy of Sciences President's International Fellowship Initiative for 2017 and 2019 (2017VBA0035and 2019VBA0025, respectively) in the case of ZR.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zbyněk Roček.

Ethics declarations

Conflict of interest

The authors declare no competing interests that are directly or indirectly related to this work.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roček, Z., Dong, L. & Wang, Y. The Early Cretaceous frog Genibatrachus from China: Osteology, development, and palaeogeographic relations. Palaeobio Palaeoenv 103, 799–825 (2023). https://doi.org/10.1007/s12549-023-00579-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12549-023-00579-x

Keywords

Navigation