Skip to main content

Advertisement

SpringerLink
Log in

Paleoenvironmental conditions in the Spanish Miocene–Pliocene boundary: isotopic analyses of Hipparion dental enamel

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Expansion of C4 grasses during Late Miocene and Early Pliocene constitutes one of the most remarkable biotic events of the Cenozoic era. The Teruel–Alfambra region (northeastern Spain) contains one of the most complete Miocene–Pliocene sequences of mammalian fossil sites in the world. In this study, stable isotope (δ 13C and δ 18O) analyses have been performed on the tooth enamel from the equid Hipparion from 19 localities spanning a time interval from approximately 10.9 to 2.7 Ma. This time range starts with the first appearance of this genus in Spain and ends at its extinction. An increase in δ 13C at about 4.2 Ma has been observed, indicative of a shift toward a more open habitat. This shift may be related to a large scale vegetation change which occurred across the Miocene–Pliocene boundary when C4 grasses expanded. This expansion might in turn be linked to global tectonic events such as the uplift of the Himalaya and/or the closure of the Panama Isthmus. However, other more regional factors may have ultimately enhanced the trend toward more open habitats in the Western Mediterranean Basin. The Messinian Salinity Crisis was a major environmental event that may have been responsible for the isotopic changes seen in the equid Hipparion from the Iberian Peninsula along with an increase in the aridity detected ~4.6 Ma ago in the Sahara. Even though the exact factor triggering the isotopic change observed in the Hipparion enamel remains mostly unknown, this study demonstrates that the global environmental changes detected across the Miocene–Pliocene boundary are also recorded in the realm of the Iberian Peninsula.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Agustí J, Garcés M, Krijgsman W (2006) Evidence for African-Iberian exchanges during the Messinian in the Spanish mammalian record. Palaeogeogr Palaeoclimatol Palaeoecol 238:5–14. doi:10.1016/j.palaeo.2006.03.013

    Article  Google Scholar 

  • Alcalá L (1994) Macromamíferos Neógenos de la Fosa de Alfambra-Teruel. Instituto de Estudios Turolenses y Museo Nacional de Ciencias Naturales, CSIC, Teruel

    Google Scholar 

  • Alcalá L, Alonso-Zarza AM, Azanza B, Calvo JP, Cañaveras JC, van Dam JA, Garcés M, Krijgsman W, van der Meulen AJ, Morales J, Peláez-Campomanes P, Pérez-González A, Sánchez Moral S, Sancho R, Sanz Rubio E (2000) El registro sedimentario y faunístico de las cuencas de Calatayud-Daroca y Teruel. Evolución paleoambiental y paleoclimática durante el Neógeno. Rev Soc Geol Esp 13(2):323–343

    Google Scholar 

  • Alroy J (2000) New methods for quantifying macroevolutionary patterns and processes. Paleobiology 26:707–733. doi:10.1666/0094-8373(2000)026<0707: NMFQMP>2.0.CO;2

    Article  Google Scholar 

  • Ayliffe LK, Lister AM, Chivas AR (1992) The preservation of glacial-interglacial climatic signatures in the oxygen isotopes of elephant skeletal phosphate. Palaeogeogr Palaeoclimatol Palaeoecol 99:179–191. doi:10.1016/0031-0182(92)90014-V

    Article  Google Scholar 

  • Ayliffe LK, Chivas AR, Leakey MG (1994) The retention of primary oxygen isotope compositions of fossil elephant skeletal phosphate. Geochim Cosmochim Acta 58:5291–5298. doi:10.1016/0016-7037(94)90312-3

    Article  CAS  Google Scholar 

  • Bender MM (1971) Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10:1239–1245. doi:10.1016/S0031-9422(00)84324-1

    Article  CAS  Google Scholar 

  • Bryant JD, Froelich PN (1995) A model of oxygen isotope fractionation in body water of large mammals. Geochim Cosmochim Acta 59:4523–4537. doi:10.1016/0016-7037(95)00250-4

    Article  CAS  Google Scholar 

  • Bryant JD, Froelich PN, Showers WJ, Genna BJ (1996) A tale of two quarries: biologic and taphonomic signatures in the oxygen isotope composition of tooth enamel phosphate from modern and Miocene equids. Palaios 11:397–408

    Article  Google Scholar 

  • Cande SC, Kent DV (1995) Revised calibration of the geomagnetic polarity timescale for the Late Cretaceous and Cenozoic. J Geophys Res 100:6093–6095

    Article  Google Scholar 

  • Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120:347–363. doi:10.1007/s004420050868

    Article  Google Scholar 

  • Cerling TE, Wang Y, Quade J (1993) Expansion of C4 ecosystems as an indicator of global ecological change in the late Miocene. Nature 361:344–345. doi:10.1038/361344a0

    Article  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158. doi:10.1038/38229

    Article  CAS  Google Scholar 

  • Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468

    Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Domingo MS, Alberdi MT, Azanza B (2007) A new quantitative biochronological ordination for the Upper Neogene mammalian localities of Spain. Palaeogeogr Palaeoclimatol Palaeoecol 255:361–376. doi:10.1016/j.palaeo.2007.08.004

    Article  Google Scholar 

  • Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411–439

    Article  Google Scholar 

  • Ehleringer JR, Pearcy RW (1983) Variation in quantum yield for CO2 uptake among C3 and C4 plants. Plant Physiol 73:555–559

    Article  PubMed  CAS  Google Scholar 

  • Ehleringer JR, Cerling TE, Helliker BR (1997) C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112:285–299. doi:10.1007/s004420050311

    Article  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotopic discrimination and photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443

    Article  CAS  Google Scholar 

  • Fluteau F, Suc J-P, Fauquette S (2003) Modelling the climatic consequences of the Messinian Salinity Crisis. Geophys Res Abstr 5:11387

    Google Scholar 

  • Fortelius M, Eronen J, Liu L, Pushkina D, Tesakov A, Vislobokova I, Zhang Z (2006) Late Miocene and Pliocene large land mammals and climatic changes in Eurasia. Palaeogeogr Palaeoclimatol Palaeoecol 238:219–227. doi:10.1016/j.palaeo.2006.03.042

    Article  Google Scholar 

  • Fox DL, Koch PL (2004) Carbon and oxygen isotopic variability in Neogene paleosol carbonates: constraints on the evolution of the C4-grasslands of the Great Plains, USA. Palaeogeogr Palaeoclimatol Palaeoecol 207:305–329. doi:10.1016/j.palaeo.2003.09.030

    Article  Google Scholar 

  • Haug GH, Tiedemann R (1998) Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393:673–676. doi:10.1038/31447

    Article  CAS  Google Scholar 

  • Haug GH, Tiedemann R, Zahn R, Ravelo AC (2001) Role of Panama uplift on oceanic freshwater balance. Geology 29:207–210. doi:10.1130/0091-7613(2001)029<0207:ROPUOO>2.0.CO;2

    Article  CAS  Google Scholar 

  • Hernández Fernández M, Álvarez Sierra MA, Peláez-Campomanes P (2007) Bioclimatic analysis of rodent palaeofaunas reveals severe climatic changes in Southwestern Europe during the Plio–Pleistocene. Palaeogeogr Palaeoclimatol Palaeoecol 251:500–526. doi:10.1016/j.palaeo.2007.04.015

    Article  Google Scholar 

  • Hsü KJ, Ryan WBF, Cita MB (1973) Late Miocene dessication of the Mediterranean. Nature 242:240–244. doi:10.1038/242240a0

    Article  Google Scholar 

  • Iacumin P, Bocherens H, Mariotti A, Longinelli A (1996) 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. doi:10.1016/0012-821X(96)00093-3

    Article  CAS  Google Scholar 

  • Koch PL, Fisher DC, Dettman D (1989) Oxygen isotope variation in the tusks of extinct proboscideans: a measure of season of death and seasonality. Geology 17:515–519. doi:10.1130/0091-7613(1989)017<0515:OIVITT>2.3.CO;2

    Article  CAS  Google Scholar 

  • Koch PL, Tuross N, Fogel ML (1997) The effects of sample treatment and diagenesis on the isotopic integrity of carbonate in biogenic hydroxylapatite. J Archaeol Sci 24:417–429. doi:10.1006/jasc.1996.0126

    Article  Google Scholar 

  • Koch PL, Diffenbaugh NS, Hoppe KA (2004) The effects of Late Quaternary climate and pCO2 change on C4 plant abundance in the South-Central United States. Palaeogeogr Palaeoclimatol Palaeoecol 207:331–357. doi:10.1016/j.palaeo.2003.09.034

    Article  Google Scholar 

  • Kohn MJ (1996) Predicting animal δ18O: accounting for diet and physiological adaptation. Geochim Cosmochim Acta 60:4811–4829. doi:10.1016/S0016-7037(96)00240-2

    Article  CAS  Google Scholar 

  • Krijgsman WJ, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655. doi:10.1038/23231

    Article  CAS  Google Scholar 

  • Latorre C, Quade J, McIntosh WC (1997) The expansion of C4 grasses and global change in the late Miocene: stable isotope evidence from the Americas. Earth Planet Sci Lett 146:83–96. doi:10.1016/S0012-821X(96)00231-2

    Article  CAS  Google Scholar 

  • Lear CH, Rosenthal Y, Wright JD (2003) The closing of a seaway: ocean water masses and global climate change. Earth Planet Sci Lett 210:425–436. doi:10.1016/S0012-821X(03)00164-X

    Article  CAS  Google Scholar 

  • Lécuyer C, Picard S, Garcia J-P, Sheppard SMF, Grandjean P, Dromart G (2003) Thermal evolution of Tethyan surface waters during the Middle–Late Jurassic: evidence from δ 18O values of marine fish teeth. Paleoceanography 18:21(1)–21(16). doi:10.1029/2002PA000863

    Article  Google Scholar 

  • Lee-Thorp J, Sponheimer M (2003) Three case studies used to reassess the reliability of fossil bone and enamel isotope signals for paleodietary studies. J Anthropol Archaeol 22:208–216. doi:10.1016/S0278-4165(03)00035-7

    Article  Google Scholar 

  • Lee-Thorp J, van der Merwe NJ (1987) Carbon isotope analysis of fossil bone apatites. S Afr J Sci 83:712–715

    Google Scholar 

  • Levin NE, Cerling TE, Passey BH, Harris JM, Ehleringer JR (2006) A stable isotope aridity index for terrestrial environments. Proc Natl Acad Sci 103:11201–11205. doi:10.1073/pnas.0604719103

    Article  PubMed  CAS  Google Scholar 

  • Lunt DJ, Valdes PJ, Haywood A, Rutt IC (2008) Closure of the Panama Seaway during the Pliocene: implications for climate and Northern Hemisphere glaciation. Clim Dyn 30:1–18. doi:10.1007/s00382-007-0265-6

    Article  Google Scholar 

  • Montuire S, Maridet O, Legendre S (2006) Late Miocene–Early Pliocene temperature estimates in Europe using rodents. Palaeogeogr Palaeoclimatol Palaeoecol 238:247–262. doi:10.1016/j.palaeo.2006.03.026

    Article  Google Scholar 

  • Morgan ME, Kingston JD, Marino BD (1994) Carbon isotopic evidence for the emergence of C4 plants in the Neogene from Pakistan and Kenya. Nature 367:162–165. doi:10.1038/367162a0

    Article  CAS  Google Scholar 

  • Oms O, Dinarès-Turell J, Agustí J, Parés JM (1999) Refinements of the European Mammal Biochronology from the magnetic polarity record on the Plio–Pleistocene Zújar Section, Guadix-Baza Basin, SE Spain. Quat Res 51:94–103. doi:10.1006/qres.1998.2018

    Article  Google Scholar 

  • Opdyke N, Mein P, Lindsay A, Pérez-González A, Moissenet E, Norton VL (1997) Continental deposits, magnetostratigraphy and vertebrate paleontology, late Neogene of Eastern Spain. Palaeogeogr Palaeoclimatol Palaeoecol 133:129–148. doi:10.1016/S0031-0182(97)00080-1

    Article  Google Scholar 

  • Pagani M, Arthur MA, Freeman KH (1999) Late Miocene atmospheric CO2 concentrations and the expansion of the C4 grass. Science 285:876–878. doi:10.1126/science.285.5429.876

    Article  PubMed  CAS  Google Scholar 

  • Passey BH, Cerling TE, Perkins ME, Voorhies MR, Harris JM, Tucker ST (2002) Environmental change in the Great Plains: an isotopic record from fossil horses. J Geol 110:123–140. doi:10.1086/338280

    Article  CAS  Google Scholar 

  • Pesquero MD (2003) Hipparion del Turoliense superior de Las Casiones (Fosa de Teruel). Coloq Paleontol v. ext 1:511–548

    Google Scholar 

  • Pesquero MD, Alberdi MT, Alcalá L (2006) New species of Hipparion from La Roma 2 (Late Vallesian; Teruel, Spain): a study of the morphological and biometric variability of Hipparion primigenium. J Paleontol 80:343–356. doi:10.1666/0022-3360

    Article  Google Scholar 

  • Popov SV, Rögl F, Rozanov AY, Steininger FF, Shcherba IG, Kováè M (2004) Lithological–paleogeographic maps of Paratethys. 10 maps Late Eocene to Pliocene. Courier Forschungsinstitut Senckenberg 250:1–46

    Google Scholar 

  • Quade J, Cerling TE, Bowman JR (1989) Systematic variations in the carbon and oxygen isotopic composition of pedogenic carbonate along elevation transects in the southern Great Basin, United States. Geol Soc Am Bull 101:464–475

    Article  CAS  Google Scholar 

  • Quade J, Cerling TE, Barry JC, Morgan ME, Pilbeam DR, Chivas AR, Lee-Thorp JA, van der Merwe NJ (1992) A 16-Ma record of paleodiet using carbon and oxygen isotopes in fossil teeth from Pakistan. Chem Geol 94:183–192

    Article  CAS  Google Scholar 

  • Quade J, Solounias N, Cerling TE (1994) Stable isotopic evidence from paleosol carbonates and fossil teeth in Greece for forest or woodlands over the past 11 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 108:41–53. doi:10.1016/0031-0182(94)90021-3

    Article  Google Scholar 

  • Rouchy JM, Caruso A (2006) The Messinian salinity crisis in the Mediterranean basin: a reassessment of the data and an integrated scenario. Sediment Geol 188–189:35–67. doi:10.1016/j.sedgeo.2006.02.005

    Article  CAS  Google Scholar 

  • Rozanski K, Araguás-Araguás L Gonfiantini R (1993) Isotopic patterns in modern global rainfall. In: Swart PK, Lohmann KC, McKenzie J, Savin S (eds) Climate Change in continental isotopic records. Geophysical Monograph 78:1–36

  • Sánchez Chillón B, Alberdi MT, Leone G, Bonadonna FP, Stenni B, Longinelli A (1994) Oxygen isotopic composition of fossil equid tooth and bone phosphate: an archive of difficult interpretation. Palaeogeogr Palaeoclimatol Palaeoecol 107:317–328. doi:10.1016/0031-0182(94)90103-1

    Article  Google Scholar 

  • Ségalen L, Lee-Thorp JA, Cerling TE (2007) Timing of C4 grass expansion across sub-Saharan Africa. J Hum Evol 53:549–559. doi:10.1016/j.jhevol.2006.12.010

    Article  PubMed  Google Scholar 

  • Tiedemann R, Sarnthein M, Stein R (1989) Climatic changes in the Western Sahara: aeolo-marine sediment record of the last 8 million years (sites 657–661). Proc Ocean Drill Prog 108:241–277

    Google Scholar 

  • Tiedemann R, Sarnthein M, Shackleton NJ (1994) Astronomic timescale for the Pliocene Atlantic δ18O and dust flux records of Ocean Drilling Program site 659. Paleoceanography 9:619–638

    Article  Google Scholar 

  • Tipple BJ, Pagani M (2007) The early origins of terrestrial C4 photosynthesis. Ann Rev Earth Planet Sci 35:435–461. doi:10.1146/annurev.earth.35.031306.140150

    Article  CAS  Google Scholar 

  • van Dam JA (2006) Geographic and temporal patterns in the late Neogene (12–3 Ma) aridification of Europe: the use of small mammals as paleoprecipitation proxies. Palaeogeogr Palaeoclimatol Palaeoecol 238:190–218. doi:10.1016/j.palaeo.2006.03.025

    Article  Google Scholar 

  • van Dam JA, Alcalá L, Alonso-Zarza AM, Calvo JP, Garcés M, Krijgsman W (2001) The upper Miocene mammal record from the Teruel–Alfambra region (Spain). The MN system and continental stage/age concepts discussed. J Vertebr Paleontol 21:367–385

    Article  Google Scholar 

  • van der Made J, Morales J, Montoya P (2006) Late Miocene turnover in the Spanish mammal record in relation to palaeoclimate and the Messinian Salinity Crisis. Palaeogeogr Palaeoclimatol Palaeoecol 238:228–246. doi:10.1016/j.palaeo.2006.03.030

    Article  Google Scholar 

  • Wang Y, Deng T, Biasatti DM (2006) Ancient diets indicate significant uplift of southern Tibet after ca. 7 Ma. Geology 34:309–312. doi:10.1130/g22254.1

    Article  CAS  Google Scholar 

  • Yurtsever Y, Gat J (1981) Atmospheric waters. In: Gat JR, Gonfiantini R (eds) Stable isotope hydrology. Deuterium and oxygen-18 in the water cycle. 210. Tech. Rep. Ser. IAEA, Vienna, pp 103–142

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Spanish Ministerio de Educación y Ciencia (project CGL2006-04646/BTE and FPU predoctoral contracts to L. D. and M. S. D.). The work conducted by S. T. G. was supported by a Natural Environmental Research Council (NERC) New Investigators grant (NE/C507237/1). Authors are grateful to L. Alcalá and E. Espílez (Fundación Conjunto Paleontológico de Teruel, Dinópolis, Teruel), B. Sánchez-Chillón (Museo Nacional de Ciencias Naturales-CSIC, Madrid) and S. Menéndez (Museo Geominero, Instituto Geológico y Minero de España, Madrid) for kindly providing the studied material. Numerous sampled teeth were found in excavations conducted by L. Alcalá with the authorization of the Dirección General de Patrimonio Cultural del Gobierno de Aragón and supported by the FOCONTUR project (Research Group E-62, Gobierno de Aragón). Thanks are given to M. D. Pesquero (Museo Nacional de Ciencias Naturales-CSIC, Madrid) for the identification of some teeth and for providing information concerning some of the localities from Teruel-Alfambra region. N. López-Martínez, A. M. Alonso-Zarza, M. Hernández Fernández (Universidad Complutense de Madrid, Spain), D. L. Fox, and S. D. Matson (University of Minnesota, USA) are acknowledged for their valuable comments which substantially improved the manuscript. We also thank the editor T. Czeschlik and three anonymous reviewers for helpful review comments.

The experiments carried out in this research comply with the current laws of Spain and the United Kingdom.

Author information

Authors and Affiliations

  1. Departamento de Paleontología, Facultad CC. Geológicas, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Laura Domingo

  2. School of Earth, Ocean and Environmental Sciences, University of Plymouth, Drake Circus, Plymouth, Devon, PL4 8AA, UK

    Stephen T. Grimes

  3. Departamento de Paleobiología, Museo Nacional de Ciencias Naturales (CSIC), 28006, Madrid, Spain

    M. Soledad Domingo & M. Teresa Alberdi

Authors
  1. Laura Domingo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen T. Grimes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Soledad Domingo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Teresa Alberdi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Domingo.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM S1

(PDF 178.78 KB)

ESM S2

(PDF 179.85 KB)

ESM S3

(PDF 47.88 KB)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Domingo, L., Grimes, S.T., Domingo, M.S. et al. Paleoenvironmental conditions in the Spanish Miocene–Pliocene boundary: isotopic analyses of Hipparion dental enamel. Naturwissenschaften 96, 503–511 (2009). https://doi.org/10.1007/s00114-008-0500-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-008-0500-y

Keywords

Search

Navigation