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

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Abstract

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.

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References

  • 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

  • Benton MJ (2005) Vertebrate Paleontology, 3rd edn. Blackwell Publishing Ltd, Malden, Ma, p. 455

    Google Scholar 

  • Braun J, Reif W-E (1985) A survey of aquatic locomotion in fishes and tetrapods. N Jb Geol Pal, Abh 169:307–312

    Google Scholar 

  • Buffrénil V de, Castanet J (2000) Age estimation by skeletochronology in the Nile monitor (Varanus niloticus), a high exploited species. J Herpetol 34:414–424

  • Buffrénil V de, Houssaye A, Böhme W (2008) Bone vascular supply in monitor lizards (Squamata: Varanidae): influence of size, growth, and phylogeny. J Morphol 269:533–543

  • 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 

  • Carroll RL (1985a) A pleurosaur from the lower Jurassic and the taxonomic position of the Sphenodontida. Palaeontogr Abt A 189(1–3):1–28

    Google Scholar 

  • Carroll RL (1985b) Evolutionary constraints in aquatic diapsid reptiles. Spec Pap Palaeontol 33:145–155

    Google Scholar 

  • 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. 70–83

    Google Scholar 

  • 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):25–37

    Google Scholar 

  • Cree A (2014) Tuatara: biology and conservation of a venerable survivor. Canterbury University Press, Christchurch

    Google Scholar 

  • Dupret V (2004) The pleurosaurs: anatomy and phylogeny. Rev Paléobiol, Genève Vol. spéc. 9:61–80

  • Erickson GM, Makovicky PJ, Currie PJ, Norell MA, Yerby SA, Brochu CA (2004) Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772–775

    Article  CAS  PubMed  Google Scholar 

  • 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 471–530

  • Girondot M, Laurin M (2003) Bone profiler: a tool to quantify, model, and statistically compare bone-section compactness profiles. JVP 23(2):458–461

    Google Scholar 

  • Günther A (1867) Contribution to the anatomy of Hatteria (Rhynchocephalus, Owen). Phil Trans R Soc Lond 157:595–629

    Article  Google Scholar 

  • 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 11:1063–1081

    Article  Google Scholar 

  • Heidsieck E (1929) Der Bau der Skeletteile der freien Extremitäten bei den Reptilien. 2. Mitteilung: Hatteria (Sphenodon) punctata. Gegenbaurs Morphol Jahrb 62:319–354

    Google Scholar 

  • 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 10:413–426

  • 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 46:312–324

    Article  Google Scholar 

  • Jones MEH (2008) The evolution of skull shape and feeding strategy in Rhynchocephalia (Diapsida: Lepidosauria). J Morphol 269:945–966

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 77:169–206

    Google Scholar 

  • 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):389–408

    Article  Google Scholar 

  • Klein N, Houssaye A, Neenan JM, Scheyer TM (2015a) Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia). Contr Zool 84(1):59–84

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 10:403–411

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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):33

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynoso VH (2000) An unusual aquatic sphenodontian (Reptilia: Diapsida) from the Tlayua Formation (Albian), central Mexico. J Paleontol 74:133–148

    Article  Google Scholar 

  • 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 289–310

  • Schauinsland H (1900) Weitere Beiträge zur Entwicklungsgeschichte der Hatteria. Skelettsystem, schallleitender Apparat, Hirnnerven etc. Arch Mikrosk Anat 56:747–867

    Article  Google Scholar 

  • Street HP, O'Keefe FR (2010) Evidence of pachyostosis in the cryptocleidoid plesiosaur Tatenectes laramiensis from the Sundance Formation of Wyoming. J Vertebr Paleontol 30:1279–1282

    Article  Google Scholar 

  • Vickaryous MK, Hall BK (2008) Development of the dermal skeleton in Alligator mississippiensis (Archosauria, Crocodylia) with comments on the homology of osteoderms. J Morphol 269:398–422

    Article  PubMed  Google Scholar 

  • Wettstein O (1931) 1. Ordnung der Klasse Reptilia: Rhynchocephalia. Handbuch der Zoologie 7:1–235

    Google Scholar 

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Acknowledgements

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).

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Correspondence to Nicole Klein.

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Communicated by: Robert Reisz

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Klein, N., Scheyer, T.M. Microanatomy and life history in Palaeopleurosaurus (Rhynchocephalia: Pleurosauridae) from the Early Jurassic of Germany. Sci Nat 104, 4 (2017). https://doi.org/10.1007/s00114-016-1427-3

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