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
Braun J, Reif W-E (1985) A survey of aquatic locomotion in fishes and tetrapods. N Jb Geol Pal, Abh 169:307–312
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
Carroll RL (1985a) A pleurosaur from the lower Jurassic and the taxonomic position of the Sphenodontida. Palaeontogr Abt A 189(1–3):1–28
Carroll RL (1985b) Evolutionary constraints in aquatic diapsid reptiles. Spec Pap Palaeontol 33:145–155
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
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
Cree A (2014) Tuatara: biology and conservation of a venerable survivor. Canterbury University Press, Christchurch
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
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
Günther A (1867) Contribution to the anatomy of Hatteria (Rhynchocephalus, Owen). Phil Trans R Soc Lond 157:595–629
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
Heidsieck E (1929) Der Bau der Skeletteile der freien Extremitäten bei den Reptilien. 2. Mitteilung: Hatteria (Sphenodon) punctata. Gegenbaurs Morphol Jahrb 62:319–354
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
Jones MEH (2008) The evolution of skull shape and feeding strategy in Rhynchocephalia (Diapsida: Lepidosauria). J Morphol 269:945–966
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
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
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
Klein N, Houssaye A, Neenan JM, Scheyer TM (2015a) Long bone histology and microanatomy of Placodontia (Diapsida: Sauropterygia). Contr Zool 84(1):59–84
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
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
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
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
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
Reynoso VH (2000) An unusual aquatic sphenodontian (Reptilia: Diapsida) from the Tlayua Formation (Albian), central Mexico. J Paleontol 74:133–148
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
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
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
Wettstein O (1931) 1. Ordnung der Klasse Reptilia: Rhynchocephalia. Handbuch der Zoologie 7:1–235
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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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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DOI: https://doi.org/10.1007/s00114-016-1427-3