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Thermophysiologies of Jurassic Marine Thermophysiologies of Jurassic marine crocodylomorphs inferred from the oxygen isotope composition of their tooth apatite Nicolas Séon, Romain Amiot, Jérémy Martin, Mark Young, Heather Middleton, François Fourel, Laurent Picot, Xavier Valentin, Christophe Lécuyer To cite this version: Nicolas Séon, Romain Amiot, Jérémy Martin, Mark Young, Heather Middleton, et al.. Thermophys- iologies of Jurassic marine crocodylomorphs inferred from the oxygen isotope composition of their tooth apatite. Philosophical Transactions of the Royal Society B: Biological Sciences, Royal Society, The, 2020, 375 (1793), pp.20190139. 10.1098/rstb.2019.0139. hal-02991781 HAL Id: hal-02991781 https://hal.archives-ouvertes.fr/hal-02991781 Submitted on 27 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Submitted to Phil. Trans. R. Soc. B - Issue Page 2 of 28 1 2 Thermophysiologies of Jurassic marine crocodylomorphs inferred 3 4 5 from the oxygen isotope composition of their tooth apatite 6 7 8 9 10 Nicolas Séon1, Romain Amiot1,*, Jeremy E. Martin1, Mark T. Young2, Heather Middleton3, 11 12 4 5 6,7 1 13 François Fourel , Laurent Picot , Xavier Valentin , Christophe Lécuyer 14 15 16 17 1 UMR 5276, Laboratoire de Géologie de Lyon, Terre, Planètes et Environnement, Université 18 19 20 Claude Bernard Lyon 1/CNRS/École Normale Supérieure de Lyon, 69622 Villeurbanne Cedex, 21 For Review Only 22 France; [email protected] ; [email protected]; [email protected]; 23 24 christophe.lé[email protected] 25 26 2 27 School of GeoSciences, Grant Institute, University of Edinburgh, James Hutton Road, Edinburgh, 28 29 EH9 3FE, UK; [email protected] 30 31 3 16 Rodwell Road, Weymouth, Dorset, DT4 8QL, UK; [email protected] 32 33 4 Laboratoire d'Ecologie des Hydrosystèmes Naturels et Anthropisés, CNRS UMR 5023, Université 34 35 36 Claude Bernard Lyon 1, France; [email protected] 37 38 5 Paleospace, Avenue Jean Moulin, 14640 Villers sur mer, France; [email protected] 39 40 6 Laboratoire PALEVOPRIM, UMR 7262 CNRS INEE & University of Poitiers, France; 41 42 43 [email protected] 44 45 7 Palaios, Research Association, 86300 Valdivienne, France 46 47 * Corresponding author 48 49 50 51 52 Keywords: Metriorhynchidae, Teleosauridae, Jurassic, Thermophysiology, Oxygen and carbon 53 54 isotopes, tooth apatite 55 56 57 58 59 60 http://mc.manuscriptcentral.com/issue-ptrsb Page 3 of 28 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 Summary 3 4 5 6 7 Teleosauridae and Metriorhynchidae were thalattosuchian crocodylomorph clades that 8 9 secondarily adapted to marine life and coexisted during the Middle to Late Jurassic. While 10 11 teleosaurid diversity collapsed at the end of the Jurassic, most likely as a result of a global cooling 12 13 14 of the oceans and associated marine regressions, metriorhynchid diversity was largely unaffected, 15 16 although the fossil record of Thalattosuchia is poor in the Cretaceous. In order to investigate the 17 18 possible differences in thermophysiologies between these two thalattosuchian lineages, we analysed 19 20 stable oxygen isotope compositions (expressed as δ18O values) of tooth apatite from metriorhynchid 21 For Review Only 22 18 23 and teleosaurid specimens. We then compared them to the δ O values of coexisting endo- 24 25 homeothermic ichthyosaurs and plesiosaurs, as well as ecto-poïkilothermic chondrichthyans and 26 27 osteichthyans. The distribution of δ18O values suggests that both teleosaurids and metriorhynchids 28 29 30 had body temperatures intermediate between those of typical ecto-poikilothermic vertebrates and 31 32 warm-blooded ichthyosaurs and plesiosaurs, metriorhynchids being slightly warmer than 33 34 teleosaurids. We propose that metriorhynchids were able to raise their body temperature above that 35 36 37 of the ambient environment by metabolic heat production, as endotherms do, but could not maintain 38 39 a constant body temperature compared to fully homeothermic ichthyosaurs and plesiosaurs. 40 41 Teleosaurids, on the other hand, may have raised their body temperature by mouth-gape basking, as 42 43 modern crocodilians do, and benefited from the thermal inertia of their large body mass to maintain 44 45 46 their body temperature above ambient one. Endothermy in metriorhynchids might have been a 47 48 byproduct of their ecological adaptations to active pelagic hunting, and it probably allowed them to 49 50 survive the global cooling of the Late Jurassic, thus explaining the selective extinction affecting 51 52 53 Thalattosuchia at the Jurassic-Cretaceous boundary. 54 55 56 57 58 59 60 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 4 of 28 1 2 Introduction 3 4 Extant crocodylians are archosaurs that rely on environmental sources of heat in order to 5 6 7 raise and maintain their body temperature by behavioural thermoregulation in a restricted range 8 9 bracketed by “critical minimum” and “critical maximum” temperatures (Cowles and Bogert, 1944; 10 11 Pough and Gans, 1982). Within this critical range, crocodylians tend to keep their body temperature 12 13 14 within a narrower activity range from about 25°C to 40°C as determined empirically for a few 15 16 extant species (see Markwick (1998) for a review). Consequently, the spatial and temporal 17 18 distribution of crocodylians is limited by the temperatures of their living environments and by their 19 20 seasonal fluctuations. Due to their rather conservative growth morphology and their restricted 21 For Review Only 22 23 latitudinal distribution today, and in the geologic record, extant and fossil representatives of the 24 25 crown group have been used as climate proxies for more than a century (Berg, 1965; Crichton, 26 27 1825; Markwick, 1998; Owen, 1850). Based on observations of extant representatives of crown 28 29 30 group Crocodylia Owen, 1842, Markwick (1998) proposed that the occurrence of fossil 31 32 representatives imply a living Mean Annual Air temperature (MAT) ≥14.2°C and a Coldest Month 33 34 Mean temperature (CMM) ≥5.5°C. These minimum limits have been tentatively used to constrain 35 36 37 the climatic environment of long-extinct crocodylomorphs (Amiot et al., 2011), as well as the more 38 39 distantly related clade Choristodera (Tarduno et al., 1998). 40 41 The crocodylomorph clade Thalattosuchia became secondarily adapted to marine life during 42 43 the Mesozoic, and is subdivided into the families Teleosauridae Saint-Hilaire, 1831 and 44 45 46 Metriorhynchidae Fitzinger, 1843. While teleosaurids retained a morphology reminiscent of typical 47 48 semi-aquatic longirostrine crocodylomorphs, in having extensive osteoderm coverage and limbs 49 50 adapted for terrestrial locomotion (Eudes-Deslongchamps, 1869), metriorhynchids had a more 51 52 53 hydrodynamic body plan, with a hypocercal tail, and hydrofoil-like forelimbs (Fraas, 1902; Young 54 55 et al., 2010). The bone histology of Callovian teleosaurids and metriorhynchids has been used to 56 57 hypothesize that thalattosuchians were ectothermic (i.e. they rely on environmental sources of heat 58 59 60 in order to raise their body temperature) and poikilothermic (i.e. their body temperature vary along http://mc.manuscriptcentral.com/issue-ptrsb Page 5 of 28 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 with that of their environment), with teleosaurids being capable of mouth-gape basking on shore, 3 4 whereas metriorhynchids thermoregulated differently by staying close to the water surface (Hua and 5 6 7 De Buffrénil, 1996). Hua and de Buffrénil (1996) did note that young metriorhynchids may have 8 9 had a faster growth rate than wild extant crocodylians. 10 11 Martin et al. (2014) analysed the diversity of marine crocodylomorphs through the Mesozoic 12 13 14 and Paleogene, and observed a significant correlation between Sea Surface Temperatures (SST) and 15 16 generic diversity within four lineages, including the teleosaurids. Teleosaurids, at least European 17 18 representatives, experienced a diversity crash at the end of the Jurassic during a global cooling of 19 20 Tethyan waters (Lécuyer et al., 2003b), but according to Fanti et al. (2016) they may have 21 For Review Only 22 23 continued to survive until at least the Hauterivian along the southern coast of the Tethys Sea. 24 25 Metriorhynchids however, appear to have experienced an explosive radiation during the Callovian, 26 27 surviving through the Late Jurassic until the Aptian (Chiarenza et al., 2015). When metriorhynchids 28 29 30 became extinct is currently unclear. Young et al. (2010) hypothesized a two-step extinction for 31 32 Metriorhynchidae, first a diversity crash at the end Jurassic, then a final extinction during the cold 33 34 icehouse interval of the Valanginian (Pucéat et al., 2003). However, recent re-evaluations of 35 36 37 Cretaceous fossils and updated phylogenetic studies have disproved both steps of this hypothesis, 38 39 with post-Valanginian metriorhynchid specimens known and no fewer than four metriorhynchid
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