Euryhaline ecology of early tetrapods revealed by stable isotopes

Abstract

The fish-to-tetrapod transition—followed later by terrestrialization—represented a major step in vertebrate evolution that gave rise to a successful clade that today contains more than 30,000 tetrapod species. The early tetrapod Ichthyostega was discovered in 1929 in the Devonian Old Red Sandstone sediments of East Greenland (dated to approximately 365 million years ago). Since then, our understanding of the fish-to-tetrapod transition has increased considerably, owing to the discovery of additional Devonian taxa that represent early tetrapods or groups evolutionarily close to them. However, the aquatic environment of early tetrapods and the vertebrate fauna associated with them has remained elusive and highly debated. Here we use a multi-stable isotope approach (δ13C, δ18O and δ34S) to show that some Devonian vertebrates, including early tetrapods, were euryhaline and inhabited transitional aquatic environments subject to high-magnitude, rapid changes in salinity, such as estuaries or deltas. Euryhalinity may have predisposed the early tetrapod clade to be able to survive Late Devonian biotic crises and then successfully colonize terrestrial environments.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: δ34Sbone and δ34Swater values of modern reptiles, amphibians and fish.
Fig. 2: δ13Cc of Devonian vertebrate bone apatites.
Fig. 3: Environmental interpretation.
Fig. 4: δ18Op of Devonian vertebrate bone apatite.

References

  1. 1.

    Ahlberg, P. E. Elginerpeton pancheni and the earliest tetrapod clade. Nature 373, 420–425 (1995).

    ADS  Article  CAS  Google Scholar 

  2. 2.

    Niedźwiedzki, G., Szrek, P., Narkiewicz, K., Narkiewicz, M. & Ahlberg, P. E. Tetrapod trackways from the early Middle Devonian period of Poland. Nature 463, 43–48 (2010).

    ADS  Article  PubMed  CAS  Google Scholar 

  3. 3.

    Coates, M. I. & Clack, J. A. Polydactyly in the earliest known tetrapod limbs. Nature 347, 66–69 (1990).

    ADS  Article  Google Scholar 

  4. 4.

    Clack, J. A. et al. A uniquely specialized ear in a very early tetrapod. Nature 425, 65–69 (2003).

    ADS  Article  PubMed  CAS  Google Scholar 

  5. 5.

    Pierce, S. E., Clack, J. A. & Hutchinson, J. R. Three-dimensional limb joint mobility in the early tetrapod Ichthyostega. Nature 486, 523–526 (2012).

    ADS  Article  PubMed  CAS  Google Scholar 

  6. 6.

    Agassiz, L. Monographie des Poissons Fossiles du Vieux Grés Rouge: Ou Système Dévonien (Old Red Sandstone) des Iles Britanniques et de Russie (Soleure, Neuchatel, 1845).

  7. 7.

    Woodward, A. S. Catalogue of the Fossil Fishes in the British Museum (Natural History), Part 2 (British Museum (Natural History), London, 1891).

    Google Scholar 

  8. 8.

    Säve-Söderbergh, G. Preliminary Note on Devonian Stegocephalians from East Greenland (Meddelelser om Grønland 94) (1932).

  9. 9.

    McClay, K. R., Norton, M. G., Coney, P. & Davis, G. H. Collapse of the Caledonian orogen and the Old Red Sandstone. Nature 323, 147–149 (1986).

    ADS  Article  Google Scholar 

  10. 10.

    Godwin-Austen, R. On the possible extension of the coal-measures beneath the south-eastern part of England. Q. J. Geol. Soc. 11, 533–536 (1855).

    Article  Google Scholar 

  11. 11.

    Barrell, J. The influence of Silurian-Devonian climates on the rise of air-breathing vertebrates. Proc. Natl Acad. Sci. USA 2, 499–504 (1916).

    ADS  Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. 12.

    Bray, A. A., Potts, W. T. W. & Milner, A. R. The evolution of the terrestrial vertebrates: environmental and physiological considerations. Phil. Trans. R. Soc. Lond. B 309, 289–322 (1985).

    ADS  Article  CAS  Google Scholar 

  13. 13.

    Schmitz, B., Åberg, G., Werdelin, L., Forey, P. & Bendix-Almgreen, S. E. 87Sr/86Sr, Na, F, Sr, and La in skeletal fish debris as a measure of the paleosalinity of fossil-fish habitats. Geol. Soc. Am. Bull. 103, 786–794 (1991).

    ADS  Article  CAS  Google Scholar 

  14. 14.

    Schultze, H.-P. & Cloutier, R. in Devonian Fishes and Plants of Miguasha, Québec, Canada (eds Schultze, H.-P. & Cloutier, R.) 348–368 (Dr Friedrich Pfeil, Munich, 1996).

  15. 15.

    Carr, R. K. & Jackson, G. L. in Guide to the Geology and Paleontology of the Cleveland Member of the Ohio Shale (ed. Hannibal, J. T.) Ch. 5 (Ohio Geological Surgey Guidebook, Cleveland, 2010).

  16. 16.

    Laurin, M. & Soler-Gijón, R. in The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface (Geological Society of London Special Publications 339) 151–179 (Geological Society, London, 2010).

    Google Scholar 

  17. 17.

    Campbell, K. S. W. & Bell, M. W. A primitive amphibian from the Late Devonian of New South Wales. Alcheringa 1, 369–381 (1977).

    Article  Google Scholar 

  18. 18.

    Ahlberg, P. E., Luksevics, E. & Lebedev, O. The first tetrapod finds from the Devonian (Upper Famennian) of Latvia. Phil. Trans. R. Soc. Lond. B 343, 303–328 (1994).

    ADS  Article  Google Scholar 

  19. 19.

    Lebedev, O. A. & Clack, J. A. Upper Devonian tetrapods from Andreyevka, Tula region, Russia. Palaeontology 36, 721–734 (1993).

    Google Scholar 

  20. 20.

    Daeschler, E. B., Shubin, N. H., Thomson, K. S. & Amaral, W. W. A Devonian tetrapod from North America. Science 265, 639–642 (1994).

    ADS  Article  PubMed  CAS  Google Scholar 

  21. 21.

    Zhu, M., Ahlberg, P. E., Zhao, W. & Jia, L. Palaeontology: first Devonian tetrapod from Asia. Nature 420, 760–761 (2002).

    ADS  Article  PubMed  CAS  Google Scholar 

  22. 22.

    Clément, G. et al. Palaeogeography: Devonian tetrapod from western Europe. Nature 427, 412–413 (2004).

    ADS  Article  PubMed  CAS  Google Scholar 

  23. 23.

    Lebedev, O. A. A new tetrapod Jakubsonia livnensis from the Early Famennian (Devonian) of Russia and palaeoecological remarks on the Late Devonian tetrapod habitats. Acta Univ. Latv. 679, 79–98 (2004).

    Google Scholar 

  24. 24.

    Shubin, N. H., Daeschler, E. B. & Coates, M. I. The early evolution of the tetrapod humerus. Science 304, 90–93 (2004).

    ADS  Article  PubMed  CAS  Google Scholar 

  25. 25.

    Clack, J. A., Ahlberg, P. E., Blom, H. & Finney, S. M. A new genus of Devonian tetrapod from North-East Greenland, with new information on the lower jaw of Ichthyostega. Palaeontology 55, 73–86 (2012).

    Article  Google Scholar 

  26. 26.

    Blieck, A. et al. The biostratigraphical and palaeogeographical framework of the earliest diversification of tetrapods (Late Devonian). Geol. Soc. Lond. Spec. Publ. 278, 219–235 (2007).

    ADS  Article  Google Scholar 

  27. 27.

    Nriagu, J. O. et al. in Stable Isotopes: Natural and Anthropogenic Sulphur in the Environment (eds Krouse, H. R. & Grinenko, V. A.) 177–265 (John Wiley & Sons, Chichester, 1991).

  28. 28.

    Nehlich, O. The application of sulphur isotope analyses in archaeological research: a review. Earth-Sci. Rev. 142, 1–17 (2015).

    Article  CAS  Google Scholar 

  29. 29.

    Nehlich, O., Barrett, J. H. & Richards, M. P. Spatial variability in sulphur isotope values of archaeological and modern cod (Gadus morhua). Rapid Commun. Mass Spectrom. 27, 2255–2262 (2013).

    Article  PubMed  CAS  Google Scholar 

  30. 30.

    Goedert, J., Fourel, F., Amiot, R., Simon, L. & Lécuyer, C. High-precision 34S/32S measurements in vertebrate bioapatites using purge-and-trap elemental analyser/isotope ratio mass spectrometry technology. Rapid Commun. Mass Spectrom. 30, 2002–2008 (2016).

    ADS  Article  PubMed  CAS  Google Scholar 

  31. 31.

    .Wagman, D. D., Evans, W. H., Parker, V. B., Schumm, R. H. & Halow, I. The NBS Tables of Chemical Thermodynamic Properties. Selected Values for Inorganic and C 1 and C 2 Organic Substances in SI Units (National Standard Reference Data System, 1982).

  32. 32.

    Stepańczak, B., Szostek, K. & Pawlyta, J. The human bone oxygen isotope ratio changes with aging. Geochronometria 41, 147–159 (2014).

    Article  Google Scholar 

  33. 33.

    Szostek, K. Chemical signals and reconstruction of life strategies from ancient human bones and teeth - problems and perspectives. Anthropol. Rev. 72, 3–30 (2009).

    Article  Google Scholar 

  34. 34.

    Iacumin, P., Bocherens, H., Mariotti, A. & Longinelli, A. Oxygen isotope analyses of co-existing carbonate and phosphate in biogenic apatite: a way to monitor diagenetic alteration of bone phosphate? Earth Planet. Sci. Lett. 142, 1–6 (1996).

    ADS  Article  CAS  Google Scholar 

  35. 35.

    Vennemann, T. W., Hegner, E., Cliff, G. & Benz, G. W. Isotopic composition of recent shark teeth as a proxy for environmental conditions. Geochim. Cosmochim. Acta 65, 1583–1599 (2001).

    ADS  Article  CAS  Google Scholar 

  36. 36.

    Zazzo, A., Lécuyer, C. & Mariotti, A. Experimentally-controlled carbon and oxygen isotope exchange between bioapatites and water under inorganic and microbially-mediated conditions. Geochim. Cosmochim. Acta 68, 1–12 (2004).

    ADS  Article  CAS  Google Scholar 

  37. 37.

    Brudevold, F. & Soremark, R. in Structural and Chemical Organization of Teeth Vol. 2 (ed. Miles, A. E. W.) 247–277 (Academic, New York, 1967).

  38. 38.

    Rink, W. J. & Schwarcz, H. P. Tests for diagenesis in tooth enamel: ESR dating signals and carbonate contents. J. Archaeol. Sci. 22, 251–255 (1995).

    Article  Google Scholar 

  39. 39.

    Passey, B. H. et al. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Archaeol. Sci. 32, 1459–1470 (2005).

    Article  Google Scholar 

  40. 40.

    Kampschulte, A. & Strauss, H. The sulfur isotopic evolution of Phanerozoic seawater based on the analysis of structurally substituted sulfate in carbonates. Chem. Geol. 204, 255–286 (2004).

    ADS  Article  CAS  Google Scholar 

  41. 41.

    Fry, B. & Chumchal, M. M. Sulfur stable isotope indicators of residency in estuarine fish. Limnol. Oceanogr. 56, 1563–1576 (2011).

    ADS  Article  Google Scholar 

  42. 42.

    Luz, B., Kolodny, Y. & Horowitz, M. Fractionation of oxygen isotopes between mammalian bone-phosphate and environmental drinking water. Geochim. Cosmochim. Acta 48, 1689–1693 (1984).

    ADS  Article  CAS  Google Scholar 

  43. 43.

    Craig, H. & Gordon, L. I. in Stable Isotopes in Oceanographic Studies and Paleotemperatures (ed. Tongiorgo, E.) 9–130 (Consiglio Nazionale delle Ricerche Laboratorio di Geologia Nucleare, Pisa, 1965).

  44. 44.

    Joachimski, M. M. et al. Devonian climate and reef evolution: insights from oxygen isotopes in apatite. Earth Planet. Sci. Lett. 284, 599–609 (2009).

    ADS  Article  CAS  Google Scholar 

  45. 45.

    Sweet, W. C. & Donoghue, P. C. Conodonts: past, present, future. J. Paleontol. 75, 1174–1184 (2001).

    Article  Google Scholar 

  46. 46.

    Lécuyer, C., Amiot, R., Touzeau, A. & Trotter, J. Calibration of the phosphate δ18O thermometer with carbonate–water oxygen isotope fractionation equations. Chem. Geol. 347, 217–226 (2013).

    ADS  Article  CAS  Google Scholar 

  47. 47.

    Licht, A. et al. Asian monsoons in a late Eocene greenhouse world. Nature 513, 501–506 (2014).

    ADS  Article  PubMed  CAS  Google Scholar 

  48. 48.

    Bouillon, S., Connolly, R. M. & Gillikin, D. P. in Treatise on Estuarine and Coastal Science (eds Wolanski, E. et al.) Ch. 7, 143–173 (Elsevier, Amsterdam, 2011).

  49. 49.

    Sallan, L. C. & Coates, M. I. End-Devonian extinction and a bottleneck in the early evolution of modern jawed vertebrates. Proc. Natl Acad. Sci. USA 107, 10131–10135 (2010).

    ADS  Article  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Clack, J. A. et al. Phylogenetic and environmental context of a Tournaisian tetrapod fauna. Nat. Ecol. Evol. 1, 002 (2016).

    Article  Google Scholar 

  51. 51.

    Blom, H., Clack, J. A. & Ahlberg, P. E. Localities, Distribution and Stratigraphical Context of the Late Devonian Tetrapods of East Greenland (Meddelelser om Grønland Geoscience 43) (Danish Polar Center, Copenhagen 2005).

  52. 52.

    Olsen, H. & Larsen, R. H. Lithostratigraphy of the continental Devonian sediments in North-East Greenland. Bull. Gronsl. Geol. Undersog. 165, 1–108 (1993).

    Google Scholar 

  53. 53.

    Blom, H., Clack, J. A., Ahlberg, P. E. & Friedman, M. Devonian vertebrates from East Greenland: a review of faunal composition and distribution. Geodiversitas 29, 119–141 (2007).

    Google Scholar 

  54. 54.

    Pan, J. et al. Continental Devonian System of Ningxia and its Biotas (Geological Publishing House, Beijing, 1987).

    Google Scholar 

  55. 55.

    Shemesh, A. Crystallinity and diagenesis of sedimentary apatites. Geochim. Cosmochim. Acta 54, 2433–2438 (1990).

    ADS  Article  CAS  Google Scholar 

  56. 56.

    Termine, J. D. & Posner, A. S. Infrared analysis of rat bone: age dependency of amorphous and crystalline mineral fractions. Science 153, 1523–1525 (1966).

    ADS  Article  PubMed  CAS  Google Scholar 

  57. 57.

    Nouri, F. Elaboration, caractérisation physico-chimique et étude des propriétés de conduction ionique et de luminescence des fluoroapatites phosphosulfatées dopées à l’europium. PhD thesis, Univ. of Carthage (2017).

  58. 58.

    Nouri, F., Panczer, G., Guyot, Y., Trabelsi-Ayadi, M. & Ternane, R. Synthesis and luminescent properties of Eu3+-doped phosphate-sulfate fluorapatites Ca10–xNax (PO4)6–x(SO4)xF2. J. Lumin. 192, 590–594 (2017).

    Article  CAS  Google Scholar 

  59. 59.

    Crowson, R. A., Showers, W. J., Wright, E. K. & Hoering, T. C. Preparation of phosphate samples for oxygen isotope analysis. Anal. Chem. 63, 2397–2400 (1991).

    Article  CAS  Google Scholar 

  60. 60.

    Lécuyer, C., Grandjean, P., O’Neil, J. R., Cappetta, H. & Martineau, F. Thermal excursions in the ocean at the Cretaceous–Tertiary boundary (northern Morocco): δ18O record of phosphatic fish debris. Palaeogeogr. Palaeoclimatol. Palaeoecol. 105, 235–243 (1993).

    Article  Google Scholar 

  61. 61.

    Lécuyer, C. et al. High-precision determination of 18O/16O ratios of silver phosphate by EA-pyrolysis-IRMS continuous flow technique. J. Mass Spectrom. 42, 36–41 (2007).

    ADS  Article  PubMed  CAS  Google Scholar 

  62. 62.

    Fourel, F. et al. 18O/16O ratio measurements of inorganic and organic materials by elemental analysis-pyrolysis-isotope ratio mass spectrometry continuous-flow techniques. Rapid Commun. Mass Spectrom. 25, 2691–2696 (2011).

    Article  PubMed  ADS  CAS  Google Scholar 

  63. 63.

    Koch, P. L., Tuross, N. & Fogel, M. L. The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J. Archaeol. Sci. 24, 417–429 (1997).

    Article  Google Scholar 

  64. 64.

    Spötl, C. & Vennemann, T. W. Continuous-flow isotope ratio mass spectrometric analysis of carbonate minerals. Rapid Commun. Mass Spectrom. 17, 1004–1006 (2003).

    ADS  Article  PubMed  CAS  Google Scholar 

  65. 65.

    Swart, P. K., Burns, S. J. & Leder, J. J. Fractionation of the stable isotopes of oxygen and carbon in carbon dioxide during the reaction of calcite with phosphoric acid as a function of temperature and technique. Chem. Geol. Isot. Geosci. Sect. 86, 89–96 (1991).

    Article  CAS  Google Scholar 

  66. 66.

    Fourel, F., Martineau, F., Seris, M. & Lécuyer, C. Measurement of 34S/32S ratios of NBS 120c and BCR 32 phosphorites using purge and trap EA-IRMS technology. Geostand. Geoanal. Res. 39, 47–53 (2015).

    Article  CAS  Google Scholar 

  67. 67.

    Marshall, J. E. A., Astin, T. R. & Clack, J. A. East Greenland tetrapods are Devonian in age. Geology 27, 637–640 (1999).

Download references

Acknowledgements

We thank N. Scharff and B. Lindow (Natural History Museum of Denmark) for authorizing the sampling of Devonian material; M. Creuzé des Châtelliers for access to the zoology collections of the Centre de Ressources pour les Sciences de l’Evolution (CERESE, FED 4271, Université de Lyon, Université Claude Bernard Lyon 1); O. de Lataillade (Ferme du Ciron), P. François (Pierrelatte), E. Liatout (Maison Liatout) and the fishery (Maison Pupier) for providing present-day material; and L. De Brito. M.Z. was supported by Natural Science Foundation of China (41530102) and Key Research Program of Frontier Sciences of CAS (QYZDJ-SSW-DQC002). This study was supported by the CNRS INSU program InterrVie, and the Institut Universitaire de France (C.L.).

Reviewer information

Nature thanks M. Böttcher, O. Nehlich and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Affiliations

Authors

Contributions

J.G., R.A. and C.L. conceived the project. J.G., F.F., L.S., X.W. and L.C. conducted the isotopic analyses. J.G. and F. A.-G. conducted elemental analyses. J.G. and G.P. conducted the Fourier-transform infrared spectroscopy analyses. G.D. provided access to some present-day material and G.C. and M.Z. provided access to the Devonian material. G.C., J.-S.S. and M.Z. provided palaeontological expertise to shape the project and interpret the data. J.G., R.A. and C.L. wrote the manuscript.

Corresponding authors

Correspondence to Jean Goedert or Christophe Lécuyer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Late Devonian vertebrate samples from East Greenland.

a, Subcomplete skull of the placoderm Remigolepis acuta (4-117; numbers in parentheses refer to sample numbers, reported in Supplementary Table 2). b, Subcomplete skull of the sarcopterygian Eusthenodon sp. (27-1151) in dorsal view. c, Dermal scales of the sarcopterygians Holoptychius sp. (30-1186). d, Partial hemimandible of an indeterminate member of Tetrapoda (42-1375). Scale bars, 10 cm.

Extended Data Fig. 2 Filtering of stable isotope data.

a, δ34Sbone of Devonian tetrapod apatites plotted as a function of sulfur concentration. Samples for which sulfur concentrations are higher than 0.6% (outlined in red) are considered to have been potentially affected by diagenetic alteration. b, Covariation of δ18Op and δ18Oc as a function of carbonate concentration. Samples with both δ18Op − δ18Oc differences higher than 14.7‰ and carbonate content higher than 13.4% (outlined in green) are considered to have been potentially affected by diagenetic alteration. (See also Supplementary Table 2). In a, b, each dot represents an independent fossil sample (n = 51) and corresponds to the average value of three repeated measurements. Each error bar corresponds to 1 s.d. (Supplementary Table 2).

Extended Data Fig. 3 Elemental analysis.

af, Sulfur content (mol% × 1,000) of apatites from Devonian tetrapod is graphically represented against various elements to test possible associations as secondary precipitated mineral phases in fossil bioapatites. The elements tested were magnesium (Mg; a), manganese (Mn; b), iron (Fe; c), copper (Cu; d), strontium (Sr; e) and barium (Ba; f). In af, each dot represents an independent Devonian apatite sample (light blue, n = 42; Supplementary Table 3) or associated matrix sample (light green, n = 7; Supplementary Table 3). A 0.6 wt% of sulfur is equal to 0.019 mol% × 1,000. Red straight lines correspond to calculated stoichiometric lines between the two elements. Black straight lines have been calculated using Pearson’s correlation test between the two elements for Devonian apatite samples and associated matrices. N.S., no significant correlation.

Extended Data Fig. 4 Fourier-transform infrared spectroscopy analysis.

Spectra of three representative fossilized biogenic apatites of Devonian vertebrates with various sulfur contents (wt% as measured by the VarioPyrocube elemental analyser). The [PO4] and [SO4] absorption bands used to calculate the SO42−/PO43− ratios are indicated in black and red dashed lines, respectively. Each spectrum corresponds to a single measurement (Supplementary Table 4).

Extended Data Fig. 5 SO42−/PO43− versus S/P ratios.

SO42−/PO43− ratios of apatites from Devonian tetrapods calculated from the infrared spectra are graphically represented against the S/P ratios calculated from elemental analysis. The two calculated regression lines (dashed) are both highly significant (Pearson’s correlation test; n = 42 and n = 36, respectively) and show a slope close to 1, which indicates that the majority of the sulfur present in apatite is in the form of sulfate that is structurally substituted for the phosphate in the crystal lattice of the apatite. Each dot represents an independent Devonian apatite sample (n = 42; Supplementary Tables 3, 5).

Extended Data Fig. 6 Calcium versus barium.

The apatite samples of Devonian tetrapods with a sulfur content over 0.019 mol% × 1,000 (Supplementary Table 3) have been outlined with a red circle. These samples display a significant negative correlation for their calcium and barium elements (Pearson’s correlation test; n = 21). This observation suggests that calcium is substituted with barium during the recrystallization process. In the same manner, some sulfates may also substitute in for the phosphates within the apatite lattice. Each dot represents an independent Devonian apatite sample (light blue, n = 42; Supplementary Table 3) or matrix sample (light green, n = 7; Supplementary Table 3).

Extended Data Fig. 7 Sulfur preservation.

a, b, Sulfur content (a) and isotope composition (b) of apatites from Devonian tetrapods are graphically represented against the cystallinity index (CI). None of them displays a significant correlation (Pearson’s correlation test; n = 47) with the crystallinity index, which indicates that recrystallization processes were not systematically associated with sulfate incorporation by elemental substitution and alteration of the sulfur isotope compositions. In a, b, each dot represents an independent Devonian apatite sample (n = 42; Supplementary Tables 2, 5).

Extended Data Fig. 8 Oxygen preservation.

ac, The oxygen isotope composition of apatites from Devonian tetrapods is graphically represented against the crystallinity index (CI; a), the CO32−/PO43− ratio (b) and the SO42−/PO43− ratio (c). None of these indicators displays a significant correlation (Pearson’s correlation test; n = 47) with the oxygen isotope composition, thus arguing in favour of at least a partial preservation of the pristine oxygen isotope composition. In ac, each dot represents an independent Devonian apatite sample (n = 47; Supplementary Tables 2, 5).

Extended Data Fig. 9 Phosphorus versus calcium.

The phosphorus (P) content of apatites from Devonian tetrapods is graphically represented against the calcium (Ca) content. On the whole, the Ca and P contents of Devonian samples are significantly correlated (Pearson’s correlation test; n = 42) with a slope of 1.19, close to that defined by the NIST 1400 and NIST 1486, both of which are modern bones (red dots; Ca/P = 1.49). These results indicate that the loss of phosphate during recrystallization was almost stoichiometric for all samples. Each dot represents an independent Devonian apatite sample (light blue, n = 42; Supplementary Table 3), a matrix sample (light green, n = 7; Supplementary Table 3) or an international standard sample (red, n = 2; Supplementary Table 3).

Supplementary information

Reporting Summary

Supplementary Table 1

Sulfur isotope composition of present-day vertebrate bones and muscles and environmental waters and food. n = 24 biologically independent animals

Supplementary Table 2

Carbon, oxygen and sulfur isotope composition of Devonian East Greenland and Chinese vertebrates. n = 51 independent Devonian apatite samples

Supplementary Table 3

Elemental concentration of Devonian apatite and some associated matrix (m) samples along with the two elemental standards NIST 1400 and NIST 1486

Supplementary Table 4

Fourier Transformed Infrared (FTIR) spectroscopy data

Supplementary Table 5

Crystallinity Index (CI), CO32−/PO43− and SO42−/PO43− ratios calculated from FTIR spectroscopy analyses

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Goedert, J., Lécuyer, C., Amiot, R. et al. Euryhaline ecology of early tetrapods revealed by stable isotopes. Nature 558, 68–72 (2018). https://doi.org/10.1038/s41586-018-0159-2

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.