The Science of Nature

, 104:4 | Cite as

Microanatomy and life history in Palaeopleurosaurus (Rhynchocephalia: Pleurosauridae) from the Early Jurassic of Germany

  • Nicole KleinEmail author
  • Torsten M. Scheyer
Original Paper


The tuatara (Sphenodon punctatus) from New Zealand is often—erroneously—identified as a ‘living fossil’, although it is the lone survivor of a large, successful radiation of Rhynchocephalia, sister taxon to squamates (lizards and snakes), that thrived through the Mesozoic and Cenozoic and experienced an intricate evolution of life histories and feeding habits. Within Rhynchocephalia, only Pleurosauridae are thought to be marine and piscivorous. Here, we present bone histological data of the Jurassic pleurosaurid Palaeopleurosaurus, showing osteosclerosis (i.e. bone mass increase) in its gastralia, and some osteosclerosis in its rib but no increase in bone mass in the femur, supporting a gradual skeletal specialization for an aquatic way of life. Similar to Sphenodon, the bone tissue deposited in Palaeopleurosaurus is lamellar zonal bone. The femoral growth pattern in Palaeopleurosaurus differs from that of terrestrial Sphenodon in a more irregular spacing of growth marks and deposition of non-annual (i.e. non-continuous) rest lines, indicating strong dependency on exogenous factors. The annual growth mark count in adult but not yet fully grown Palaeopleurosaurus is much lower when compared to adult individuals of Sphenodon, which could indicate a lower lifespan for Palaeopleurosaurus. Whereas the gastral ribs of Palaeopleurosaurus and Sphenodon are similar in composition, the ribs of Sphenodon differ profoundly in being separated into a proximal tubular rib part with a thick cortex, and an elliptical, flared ventral part characterised by extremely thin cortical bone. The latter argues against a previously inferred protective function of the ventral rib parts for the vulnerable viscera in Sphenodon.


Sphenodon punctatus Aquatic adaptation Histology Microanatomy Femur Ribs Gastralia 



We are indebted to R. Schoch (SMNS) and C. Klug (PIMUZ) who kindly gave permission for sampling specimens. Ch. Wimmer-Pfeil (SMNS) and Ch. Kolb and K. Veitschegger (PIMUZ) are thanked for the production of thin sections. M. Kamenz (SMNS) helped to prepare the specimen for histological sampling. This work was partially funded by the SNSF (grant no. 31003A-149506 to TMS).


  1. Apesteguía S, Gómez RO, Rougier GW (2014) The youngest South American rhynchocephalian, a survivor of the K/Pg extinction. Proc R Soc B 281. doi: 10.1098/rspb.2014.0811
  2. Benton MJ (2005) Vertebrate Paleontology, 3rd edn. Blackwell Publishing Ltd, Malden, Ma, p. 455Google Scholar
  3. Braun J, Reif W-E (1985) A survey of aquatic locomotion in fishes and tetrapods. N Jb Geol Pal, Abh 169:307–312Google Scholar
  4. Buffrénil V de, Castanet J (2000) Age estimation by skeletochronology in the Nile monitor (Varanus niloticus), a high exploited species. J Herpetol 34:414–424Google Scholar
  5. Buffrénil V de, Houssaye A, Böhme W (2008) Bone vascular supply in monitor lizards (Squamata: Varanidae): influence of size, growth, and phylogeny. J Morphol 269:533–543Google Scholar
  6. Canoville A, Vde B, Laurin M (2016) Microanatomical diversity of amniote ribs: an exploratory quantitative study. Biol J Linn Soc. doi: 10.1111/bij.12779 Google Scholar
  7. Carroll RL (1985a) A pleurosaur from the lower Jurassic and the taxonomic position of the Sphenodontida. Palaeontogr Abt A 189(1–3):1–28Google Scholar
  8. Carroll RL (1985b) Evolutionary constraints in aquatic diapsid reptiles. Spec Pap Palaeontol 33:145–155Google Scholar
  9. Carroll RL, Wild R (1994) Marine members of the Sphenodontia. In: Fraser N, Sues H-D (eds) In the shadow of the dinosaurs—early Mesozoic tetrapods. Cambridge University Press, Cambridge, pp. 70–83Google Scholar
  10. Castanet J, Newmann DG, Saint Girons H (1988) Skeletochronological data on the growth, age, and population structure of the Tuatara, Sphenodon punctatus, on Stephans and Lady Aloice Islands, New Zealand. Herpetologica 44(1):25–37Google Scholar
  11. Cree A (2014) Tuatara: biology and conservation of a venerable survivor. Canterbury University Press, ChristchurchGoogle Scholar
  12. Dupret V (2004) The pleurosaurs: anatomy and phylogeny. Rev Paléobiol, Genève Vol. spéc. 9:61–80Google Scholar
  13. Erickson GM, Makovicky PJ, Currie PJ, Norell MA, Yerby SA, Brochu CA (2004) Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772–775CrossRefPubMedGoogle Scholar
  14. Francillon-Vieillot H, Buffrénil V de, Castanet J, Géraudie J, Meunier FJ, Sire JY, Zylberberg L, Ricqlès A de (1990) Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG (ed) Skeletal biomineralization: patterns, processes, evolutionary trends, vol I. Van Nostrand Reinhold, New York, pp 471–530Google Scholar
  15. Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. JVP 23(2):458–461Google Scholar
  16. Günther A (1867) Contribution to the anatomy of Hatteria (Rhynchocephalus, Owen). Phil Trans R Soc Lond 157:595–629CrossRefGoogle Scholar
  17. Hay JM, Sarre SD, Lambert DM, Allendorf FW, Daugherty CH (2010) Genetic diversity and taxonomy: a reassessment of species designation in tuatara (Sphenodon: Reptilia). Conserv Genet 11:1063–1081CrossRefGoogle Scholar
  18. Heidsieck E (1929) Der Bau der Skeletteile der freien Extremitäten bei den Reptilien. 2. Mitteilung: Hatteria (Sphenodon) punctata. Gegenbaurs Morphol Jahrb 62:319–354Google Scholar
  19. Hugi J, Scheyer TM, Sander PM, Klein N, Sánchez-Villagra MR (2011) Long bone microstructure gives new insights into the life of pachypleurosaurids from the Middle Triassic of Monte San Giorgio, Switzerland/Italy. C R Palevol 10:413–426Google Scholar
  20. Hugi J, Sánchez-Villagra MR (2012) Life history and skeletal adaptations in the Galapagos marine iguana (Amblyrhynchus cristatus) as reconstructed with bone histological data: a comparative study of iguanines. J Herpetol 46:312–324CrossRefGoogle Scholar
  21. Jones MEH (2008) The evolution of skull shape and feeding strategy in Rhynchocephalia (Diapsida: Lepidosauria). J Morphol 269:945–966CrossRefPubMedGoogle Scholar
  22. Jones MEH, Anderson CL, Hipsley CA, Müller J, Evans SE, Schoch RR (2013) Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara). BMC Evol Biol 13:208. doi: 10.1186/1471-2148-13-208 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Klein N, Sander PM (2007) Bone histology and growth of the prosauropod Plateosaurus engelhardti Meyer, 1837 from the Norian bonebeds of Trossingen (Germany) and Frick (Switzerland). Spec Pap Palaeontol 77:169–206Google Scholar
  24. Klein N (2012) Postcranial morphology and growth of the Winterswijk pachypleurosaur Anarosaurus heterodontus (Sauropterygia) from the Lower Muschelkalk of Winterswijk, The Netherlands. Pal Z 86(4):389–408CrossRefGoogle Scholar
  25. Klein N, Houssaye A, Neenan JM, Scheyer TM (2015a) Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia). Contr Zool 84(1):59–84Google Scholar
  26. Klein N, Neenan J, Scheyer TM, Griebeler EM (2015b) Growth patterns and life history strategies in Placodontia (Diapsida: Sauroptertygia). R Soc Open Sci 2:140440. doi: 10.1098/rsos.140440 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kolb C, Sánchez-Villagra MR, Scheyer TM (2011) The palaeohistology of the basal ichthyosaur Mixosaurus Baur, 1887 (Ichthyopterygia, Mixosauridae) from the Middle Triassic: Palaeobiological implications. CR Palevol 10:403–411CrossRefGoogle Scholar
  28. Lyson TR, Schachner ER, Botha-Brink J, Scheyer TM, Lambertz M, Bever GS, Rubidge B, Kde Q (2014) Origin of the unique ventilatory apparatus of turtles. Nat Commun 5:5211. doi: 10.1038/ncomms6211 CrossRefPubMedGoogle Scholar
  29. Pedersen S (2015) Osteohistology of a new sauropodomorph dinosaur from Antarctica. 49th Annual GSA Meeting (19-20 May 2015)—North-Central Sect. Abstracts with Programs 47(5):33Google Scholar
  30. Rauhut OWM, Heyng AM, López-Arbarello A, Hecker A (2012) A new rhynchocephalian from the Late Jurassic of Germany with a dentition that is unique amongst tetrapods. PLoS One 7(10):e46839. doi: 10.1371/journal.pone.0046839 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Reynoso VH (2000) An unusual aquatic sphenodontian (Reptilia: Diapsida) from the Tlayua Formation (Albian), central Mexico. J Paleontol 74:133–148CrossRefGoogle Scholar
  32. Ricqlès A de, Buffrénil V de (2001) Bone histology, heterochronies and the return of tetrapods to life in water: where are we? In: Mazin JM, Buffrénil V de (eds) Secondary adaptation of tetrapods to life in water. Friedrich Pfeil Verlag, Munich, pp 289–310Google Scholar
  33. Schauinsland H (1900) Weitere Beiträge zur Entwicklungsgeschichte der Hatteria. Skelettsystem, schallleitender Apparat, Hirnnerven etc. Arch Mikrosk Anat 56:747–867CrossRefGoogle Scholar
  34. Street HP, O'Keefe FR (2010) Evidence of pachyostosis in the cryptocleidoid plesiosaur Tatenectes laramiensis from the Sundance Formation of Wyoming. J Vertebr Paleontol 30:1279–1282CrossRefGoogle Scholar
  35. Vickaryous MK, Hall BK (2008) Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. J Morphol 269:398–422CrossRefPubMedGoogle Scholar
  36. Wettstein O (1931) 1. Ordnung der Klasse Reptilia: Rhynchocephalia. Handbuch der Zoologie 7:1–235Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.State Museum of Natural History StuttgartStuttgartGermany
  2. 2.Palaeontological Institute and MuseumUniversity of ZurichZurichSwitzerland

Personalised recommendations