Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Plant fossils reveal major biomes occupied by the late Miocene Old-World Pikermian fauna

Nature Ecology & Evolution volume 2, pages 1864–1870 (2018)Cite this article

Subjects

Abstract

Reconstruction of palaeobiomes, ancient communities that exhibit a physiognomic and functional structure controlled by their environment, depends on proxies from different disciplines. Based on terrestrial mammal fossils, the late Miocene vegetation from China to the eastern Mediterranean and East Africa has been reconstructed as a single cohesive biome with increasingly arid conditions, with modern African savannahs the surviving remnant. Here, we test this reconstruction using plant fossils spanning 14–4 million years ago from sites in Greece, Bulgaria, Turkey, the Tian Shan Mountains and Baode County in China, and East Africa. The western Eurasian sites had a continuous forest cover of deciduous or evergreen angiosperms and gymnosperms, with 15% of 1,602 fossil occurrences representing conifers, which were present at all but one of the sites. Raup–Crick analyses reveal high floristic similarity between coeval eastern Mediterranean and Chinese sites, and low similarity between Eurasian and African sites. The disagreement between plant-based reconstructions, which imply that late Miocene western Eurasia was covered by evergreen needleleaf forests and mixed forests, and mammal-based reconstructions, which imply a savannah biome, throws into doubt the approach of inferring Miocene precipitation and open savannah habitats solely from mammalian dental traits. Organismal communities are constantly changing in their species composition, and neither animal nor plant traits by themselves are sufficient to infer entire ancient biomes. The plant fossil record, however, unambiguously rejects the existence of a cohesive savannah biome from eastern Asia to northeast Africa.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Vegetation and landscapes inhabited by the Pikermian fauna from Greece to Anatolia.
Fig. 2: Raup–Crick genus-level floristic similarity12,13 to Pikermi for different time periods.
Fig. 3: Raup–Crick similarities12,13 over time between Europe and East Asia, Europe and Africa, and East Asia and Africa computed on the fossil dataset, using reference sites from the same time periods (14–10 Ma, 9–6 Ma, 5–4 Ma).

Similar content being viewed by others

Data availability

The authors declare that all data supporting the findings of this study are available in the supplementary tables.

References

  1. Solounias, N. & Dawson-Saunders, B. Dietary adaptations and paleoecology of the late Miocene ruminants from Pikermi and Samos in Greece. Palaeogeogr. Palaeoclimatol. Palaeoecol. 65, 149–172 (1988).

    Article  Google Scholar 

  2. Bernor, R. L., Solounias, N., Swisher, C. C. III & van Couvering, J. A. in The Evolution of Western Eurasian Neogene Mammal Faunas (eds Bernor, R. L., Fahlbusch, V. & Mittmann, H.-W.) 137–154 (Columbia Univ. Press, New York, 1996).

  3. Fortelius, M. et al. in The Evolution of Western Eurasian Neogene Mammal Faunas (eds Bernor, R. L., Fahlbusch, V. & Mittmann, H.-W.) 414–448 (Columbia Univ. Press, New York, 1996).

  4. Eronen, J. T. et al. Distribution history and climatic controls of the late Miocene Pikermian chronofauna. Proc. Natl Acad. Sci. USA 106, 11867–11871 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Solounias, N., Rivals, F. & Semprebon, G. M. Dietary interpretation and paleoecology of herbivores from Pikermi and Samos (late Miocene of Greece). Paleobiology 36, 113–136 (2010).

    Article  Google Scholar 

  6. Bernor, R. L., Andrews, P. J., Solounias, N. & van Couvering, J. A. H. The evolution of ‘Pontian’ mammal faunas: some zoogeographic, paleoecologic and chronostratigraphic considerations. Ann. Géol. Pays Hellén. Hors Sér. 1, 81–89 (1979).

    Google Scholar 

  7. Solounias, N., Plavcan, J. M., Quade, J. & Witmer, L. in The Evolution of Neogene Terrestrial Ecosystems in Europe (eds Agustí, J., Rook, L. & Andrews, P.) 436–453 (Cambridge Univ. Press, Cambridge, 1999).

  8. Jernvall, J. & Fortelius, M. Common mammals drive the evolutionary increase of hypsodonty in the Neogene. Nature 417, 538–540 (2002).

    Article  CAS  PubMed  Google Scholar 

  9. Fortelius, M. et al. Fossil mammals resolve regional patterns of Eurasian climate change over 20 million years. Evol. Ecol. Res. 4, 1005–1016 (2002).

    Google Scholar 

  10. Kaya, F. et al. The rise and fall of the Old-World savannah fauna and the origins of the African savannah biome. Nat. Ecol. Evol. 2, 241–246 (2018).

    Article  PubMed  Google Scholar 

  11. Bernor, R. L. et al. Systematic, stratigraphic, and paleoenvironmental contexts of first-appearing Hipparion in the Vienna Basin, Austria. J. Vertebr. Paleontol. 8, 427–452 (1988).

    Article  Google Scholar 

  12. Raup, D. & Crick, R. E. Measurement of faunal similarity in paleontology. J. Paleontol. 53, 1213–1227 (1979).

    Google Scholar 

  13. Chase, J. M., Kraft, N. J. B., Smith, K. G., Vellend, M. & Inouye, B. D. Using null models to disentangle variation in community dissimilarity from variation in α-diversity. Ecosphere 2, art24 (2011).

    Article  Google Scholar 

  14. Harzhauser, M. & Piller, W. E. Benchmark data of a changing sea—palaeogeography, palaeobiogeography and events in the central Paratethys during the Miocene. Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, 8–31 (2007).

    Article  Google Scholar 

  15. Cohen, K. M., Finney, S. C., Gibbard, P. L. & Fan, J.-X. The ICS international chronostratigraphic chart. Episodes 36, 199–204 (2013).

    Article  Google Scholar 

  16. Woodward, F. I., Lomas, M. R. & Kelly, C. K. Global climate and the distribution of plant biomes. Phil. Trans. R. Soc. Lond. B 359, 1465–1476 (2004).

    Article  CAS  Google Scholar 

  17. Olson, D. M. et al. Terrestrial ecosystems of the world: a new map of life on Earth. Bioscience 51, 933–938 (2001).

    Article  Google Scholar 

  18. Kovar-Eder, J. Pannonian (upper Miocene) vegetational character and climatic inferences in the central Paratethys area. Ann. Naturhist. Mus. Wien 88, 117–129 (1987).

    Google Scholar 

  19. Kovar-Eder, J., Kvaček, Z., Martinetto, E. & Roiron, P. Late Miocene to early Pliocene vegetation of southern Europe (7–4 Ma) as reflected in the megafossil plant record. Palaeogeogr. Palaeoclimatol. Palaeoecol. 238, 321–339 (2006).

    Article  Google Scholar 

  20. Ivanov, D. et al. Miocene vegetation and climate dynamics in eastern and central Paratethys (southeastern Europe). Palaeogeogr. Palaeoclimatol. Palaeoecol. 304, 262–275 (2011).

    Article  Google Scholar 

  21. Draxner-Höck, G., Harzhauser, M. & Göhlich, U. B. Fossil record and dynamics of late Miocene small mammal faunas of the Vienna Basin and adjacent basins, Austria. C. R. Palevol. 15, 855–862 (2016).

    Article  Google Scholar 

  22. Bouchal, J. M. et al. Miocene palynofloras of the Tınaz lignite mine, Muğla, southwest Anatolia: taxonomy, palaeoecology and local vegetation change. Rev. Palaeobot. Palyno. 243, 1–36 (2017).

    Article  Google Scholar 

  23. Syabryaj, S., Utescher, T., Molchanoff, S. & Bruch, A. A. Vegetation and palaeoclimate in the Miocene of Ukraine. Palaeogeography, Palaeoclimatology, Palaeoecology 253, 153–168 (2007).

    Article  Google Scholar 

  24. Merceron, G., Novello, A. & Scott, R. S. Paleoenvironments inferred from phytoliths and dental microwear texture analyses of meso-herbivores. Geobios 49, 135–146 (2016).

  25. Velitzelos, D., Bouchal, J. M. & Denk, T. Review of the Cenozoic floras and vegetation of Greece. Rev. Palaeobot. Palyno. 204, 56–117 (2014).

    Article  Google Scholar 

  26. Denk, T., Güner, H. T. & Grimm, G. W. From mesic to arid: leaf epidermal features suggest preadaptation in Miocene dragon trees (Dracaena). Rev. Palaeobot. Palyno. 200, 211–228 (2014).

    Article  Google Scholar 

  27. Bertini, A. & Martinetto, E. Messinian to Zanclean vegetation and climate of northern and central Italy. B. Soc. Paleontol. Ital. 47, 105–121 (2008).

    Google Scholar 

  28. Kurtén, B. The Chinese Hipparion fauna. A quantitative survey with comments on the ecology of the machairodonts and hyaenids and the taxonomy of the gazelles. Comment. Biol. 13, 1–82 (1952).

    Google Scholar 

  29. Kovar-Eder, J. & Kvaček, Z. The integrated plant record (IPR) to reconstruct Neogene vegetation: the IPR-vegetation analysis. Palaios 23, 97–111 (2007).

    Article  Google Scholar 

  30. Jiang, H. & Ding, Z. A 20 Ma pollen record of East Asian summer monsoon evolution from Guyuan, Ningxia, China. Palaeogeogr. Palaeoclimatol. Palaeoecol. 265, 30–38 (2008).

    Article  Google Scholar 

  31. Bosboom, R. et al. Linking Tarim Basin sea retreat (West China) and Asian aridification in the late Eocene. Basin Res. 26, 621–640 (2014).

    Article  Google Scholar 

  32. Quade, J., Solounias, N. & Cerling, T. E. 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 (1994).

    Article  Google Scholar 

  33. Kayseri-Özer, M. S. et al. Palaeoclimatic and palaeo-environmental interpretations of the late Oligocene, late Miocene–early Pliocene in the Çankiri-Çorum Basin. Palaeogeogr. Palaeoclimatol. Palaeoecol. 467, 16–36 (2017).

    Article  Google Scholar 

  34. Spassov, N., Böhme, M., Geraads, D., Kötter, S. & van Baak C. Pikermian mammal event, post-Pikermian mammal turnover and appearance of Graecopithecus. In 15th Congress of the Regional Committee on Mediterranean Neogene Stratigraphy, Book of Abstracts, 29 (RCMNS, 2017); http://www.rcmns2017.com/files/pdf/BOOK-OF-ABSTRACTS.pdf

  35. Böhme, M. et al. Messinian age and savannah environment of the possible hominin Graecopithecus from Europe. PLoS ONE 12, e0177347 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Urban, M. A. et al. Isotopic evidence of C4 grasses in southwestern Europe during the early Oligocene–middle Miocene. Geology 38, 1091–1094 (2010).

    Article  CAS  Google Scholar 

  37. Urban, M. A., Nelson, D. M., Jiménez-Moreno, G. & Hu, F. S. Carbon isotope analyses reveal relatively high abundance of C4 grasses during early–middle Miocene in southwestern Europe. Palaeogeogr. Palaeoclimatol. Palaeoecol. 443, 10–17 (2016).

    Article  Google Scholar 

  38. Passey, B. H., Eronen, J. T., Fortelius, M. & Zhang, Z. Paleodiets and paleoenvironments of late Miocene gazelles from north China: evidence from stable carbon isotopes. Vertebrat. Palasiatic. 45, 118–127 (2007).

    Google Scholar 

  39. Zhang, C. et al. C4 expansion in the central Inner Mongolia during the latest Miocene and early Pliocene. Earth Planet Sc. Lett. 287, 311–319 (2009).

    Article  CAS  Google Scholar 

  40. Bernor, R. L., Ataabadi, M. M., Meshida, K. & Wolf, D. The Maragheh hipparions, late Miocene of Azarbaijan, Iran. Palaeobio. Palaeoenv. 96, 453–488 (2016).

    Article  Google Scholar 

  41. Barry, J. C. et al. Faunal and environmental change in the Late Miocene Siwaliks of northern Pakistan. Paleobiology 28, 1–71 (2002).

    Article  Google Scholar 

  42. Feakins, S. J., Levin, N. E., Liddy, H. M., Sieracki, A., Eglinton, T. I. & Bonnefille, R. Northeast African vegetation change over 12 m.y. Geology 41, 295–298 (2013).

    Article  Google Scholar 

  43. Flynn, L. J., Pilbeam, D., Barry, J. C. & Morgan, M. E. Siwalik synopsis: a long stratigraphic sequence for the later Cenozoic of South Asia. C. R. Palevol. 15, 877–887 (2016).

    Article  Google Scholar 

  44. Clements, F. E. The development and structure of biotic communities. J. Ecol. 5, 120–121 (1917).

    Google Scholar 

  45. Egerton, F. N. History of ecological sciences, part 59: niches, biomes, ecosystems, and systems. Bull. Ecol. Soc. Am. 98, 298–337 (2017).

    Article  Google Scholar 

  46. Bastin, J.-F. et al. The extent of forest in dryland biomes. Science 356, 635–638 (2017).

    Article  CAS  PubMed  Google Scholar 

  47. Parr, C. L., Lehmann, C. E. R., Bond, W. J., Hoffmann, W. A. & Andersen, A. N. Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol. Evol. 29, 205–213 (2014).

    Article  PubMed  Google Scholar 

  48. Ratnam, J. et al. When is a ‘forest’ a savanna, and why does it matter? Glob. Ecol. Biogeogr. 20, 653–660 (2011).

    Article  Google Scholar 

  49. Ratnam, J., Tomlinson, K. W., Rasquinha, D. N. & Sankaran, M. Savannahs of Asia: antiquity, biogeography, and an uncertain future. Phil. Trans. R. Soc. B 371, 20150305 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Lehmann, C. E., Archibald, S. A., Hoffmann, W. A. & Bond, W. J. Deciphering the distribution of the savanna biome. New Phytol. 191, 197–209 (2011).

    Article  PubMed  Google Scholar 

  51. Griffith, D. M. et al. Comment on ‘The extent of forest in dryland biomes’. Science 358, eaao1309 (2017).

    Article  CAS  PubMed  Google Scholar 

  52. Whittaker, R. H. Communities and Ecosystems 2nd edn (Macmillan, New York, 1975).

  53. Gleason, H. A. The individualistic concept of the plant association. Torrey Botanical Club Bull. 53, 7–26 (1926).

    Article  Google Scholar 

  54. Ricklefs, R. E. History and diversity: explorations at the intersection of ecology and evolution. Am. Nat. 170, S56–S70 (2007).

    Article  PubMed  Google Scholar 

  55. Ricklefs, R. E. Disintegration of the ecological community. Am. Nat. 172, 741–750 (2008).

    Article  PubMed  Google Scholar 

  56. Hayek, L.-A. C., Bernor, R. L., Solounias, N. & Steigerwald, P. Preliminary studies of hipparionine horse diet as measured by tooth microwear. Ann. Zool. Fenn. 28, 187–200 (1992).

    Google Scholar 

  57. Kaiser, T. M., Solounias, N., Fortelius, M., Bernor, R. & Schrenk, F. Tooth mesowear analysis on Hippotherium primigenium from the Vallesian Dinotheriensande (Germany)—a blind test study. Carolinea 58, 103–114 (2000).

    Google Scholar 

  58. Terrestrial Ecoregions (WWF, 2018); https://www.worldwildlife.org/biome-categories/terrestrial-ecoregions

  59. Walter, H. & Breckle, S.-W. Ökologie der Erde. 3. Spezielle Ökologie der gemäßigten und Arktischen Zonen Euro-Nordasiens (Gustav Fischer Verlag, Stuttgart, 1986).

  60. Woldring, H. & Cappers, R. The origin of the ‘wild orchards’ of Central Anatolia. Turk. J. Bot. 25, 1–9 (2001).

    Google Scholar 

  61. Bremond, L., Alexandre, A., Véla, E. & Guiot, J. Advantages and disadvantages of phytolith analysis for the reconstruction of Mediterranean vegetation: an assessment based on modern phytolith, pollen and botanical data (Luberon, France). Rev. Palaeobot. Palyno. 129, 213–228 (2004).

    Article  Google Scholar 

  62. Lisitsyna, O. V., Giesecke, T. & Hicks, S. Exploring pollen percentage threshold values as an indicator for the regional presence of major European trees. Rev. Palaeobot. Palyno. 166, 311–324 (2011).

    Article  Google Scholar 

  63. Salzmann, U. Are modern savannas degraded forests? A Holocene pollen record from the Sudanian vegetation zone of NE Nigeria. Veg. Hist. Archaebot. 9, 1–15 (2000).

    Article  Google Scholar 

  64. Zhou, Y. et al. Vascular flora of Kenya, based on the flora of tropical East Africa. PhytoKeys 90, 113–126 (2017).

    Google Scholar 

  65. Van Zeist, W., Woldring, H. & Stapert, D. Late Quaternary vegetation and climate of southwestern Turkey. Palaeohistoria 17, 53–143 (1975).

    Google Scholar 

  66. Sirenko, E. A. Microrhythms in the evolution of Pliocene and early Pleistocene vegetation in eastern Ukraine. Paleontol. J. 34(suppl.1), S81–S86 (2000).

    Google Scholar 

  67. Qin, F. et al. Utility of surface pollen assemblages to delimit eastern Eurasian steppe types. PLoS ONE 10, e0119412 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Strömberg, C. A. E., Werdelin, L., Friis, E. M. & Saraç, G. The spread of grass-dominated habitats in Turkey and surrounding areas during the Cenozoic: phytolith evidence. Palaeogeogr. Palaeoclimatol. Palaeoecol. 250, 18–49 (2007).

    Article  Google Scholar 

  69. Peel, M. C., Finlayson, B. L. & McMahon, T. A. Updated world map of the Köppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 11, 1633–1644 (2007).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a Swedish Research Council grant to T.D. and an Austrian Science Fund Grant M 1751 (to G.W.G.). We thank F. Kaya for discussion of his Raup–Crick analyses and the shortcomings of different proxies for inferring past biomes.

Author information

Author notes

  1. Unaffiliated: gwgrimm@gmx.de.

Authors and Affiliations

  1. Department of Palaeobiology, Swedish Museum of Natural History, Stockholm, Sweden

    Thomas Denk

  2. Institute of Integrative Biology, ETH Zurich (Swiss Federal Institute of Technology), Zurich, Switzerland

    Constantin M. Zohner

  3. Systematic Botany and Mycology, University of Munich (LMU), Munich, Germany

    Susanne S. Renner

Authors
  1. Thomas Denk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Constantin M. Zohner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guido W. Grimm
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susanne S. Renner
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.D. designed the initial study and performed analyses. C.M.Z. performed Raup–Crick analyses. G.W.G. performed Köppen climate analyses and designed most figures. S.S.R. provided conceptual input and wrote the first draft. All authors co-wrote the final paper.

Corresponding author

Correspondence to Thomas Denk.

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.

Supplementary information

Supplementary Information

Supplementary Figures.

Reporting Summary

Supplementary Table 1

Western Eurasian plant fossil localities considered for this study. Location, type of floral assemblage (macrofossil, leaf; macrofossil, fruit; seed; microfossil, pollen and spores), Neogene mammal zone, age inference and full references.

Supplementary Table 2

Taxon lists and vegetation unit scoring for the Western Eurasian plant localities associated with mammal faunas in Greece, Bulgaria and Turkey. Also included are phytolith counts from Strömberg et al. (2007) as shown in Supplementary Fig. 2.

Supplementary Table 3

Taxon lists (genus, family levels) of plant assemblages from western Eurasia, Northeast Asia and East Africa spanning MN7+8–MN14 used for calculating Raup–Crick similarity indices.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Denk, T., Zohner, C.M., Grimm, G.W. et al. Plant fossils reveal major biomes occupied by the late Miocene Old-World Pikermian fauna. Nat Ecol Evol 2, 1864–1870 (2018). https://doi.org/10.1038/s41559-018-0695-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0695-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene