Journal of Plant Research

, Volume 131, Issue 2, pp 239–244 | Cite as

Relicts of the Mid-Miocene Climatic Optimum may contribute to the floristic diversity of Japan: a case study of Pinus mikii (Pinaceae) and its extant relatives

  • Mariko Yamada
  • Toshihiro Yamada
Regular Paper


The epidermis of Pinus mikii leaves was studied. Pinus mikii is a fossil species from the lower Miocene to lower Pleistocene of Japan. In P. mikii, the stomata are closely set and guard cells have polar extensions of cuticle on their inner cell walls. These features suggest that P. mikii is closely related to P. luchuensis, an extant species endemic to the Ryukyu Islands of Japan. Pinus mikii also shares some epidermal characters with P. thunbergii, which is semiendemic to Japan. It is possible that P. mikii is a common ancestor of both of these extant species. The distribution of P. mikii expanded during the Mid-Miocene Climatic Optimum (MMCO), but its distribution shifted southwards as global temperatures declined. Pinus luchuensis likely speciated from the retreating population, whereas P. thunbergii arose from a population that adapted to the cooler climate. This study provides a new perspective on the contribution of MMCO relicts to the floristic diversity of Japan.


Japanese endemic plant Mid-Miocene Climatic Optimum Pinaceae Pinus luchuensis Pinus mikii Pinus thunbergii 



We thank the Kamigamo Experimental Station, Field Science Education and Research Center, Kyoto University, and K. Yamahira for providing leaf samples. M. Tsukagoshi kindly helped us to register the microscope slides and fossils used in this study.


  1. Chinzei K (1986) Faunal succession and geographic distribution of the Neogene molluscan faunas in Japan. In: Kotaka T, Marincovich L Jr (eds) Japanese Cenozoic molluscs—their origin and migration. Palaeontological Society of Japan, special papers, no. 29. Palaeontological Society of Japan, Tokyo, pp 17–32Google Scholar
  2. Debreczy Z, Rácz I (2011) Conifers around the world. DendroPress Ltd., BudapestGoogle Scholar
  3. Farjon A, Styles BT (1997) Pinus (Pinaceae). Flora neotropica monograph, no. 75. New York Botanical Garden, New YorkGoogle Scholar
  4. Fujiki T, Ozawa T (2008) Vegetation change in the main island of Okinawa, southern Japan from late Pliocene to early Pleistocene. Quat Int 184:75–83CrossRefGoogle Scholar
  5. Gernandt DS, López GG, García SO, Liston A (2005) Phylogeny and classification of Pinus. Taxon 54:29–42CrossRefGoogle Scholar
  6. Ikeda H, Carlsen T, Fujii N, Brochmann C, Setoguchi H (2012) Pleistocene climatic oscillations and the speciation history of an alpine endemic and a widespread arctic-alpine plant. New Phytol 194:583–594CrossRefPubMedGoogle Scholar
  7. Karasawa H, Nishikawa I (1991) Thalassina anomala (Herbst, 1804) (Thalassinidea: Decapoda) from the Miocene Bihoku group, southwest Japan. Trans Proc Palaeontol Soc Japan 163:852–860Google Scholar
  8. Kato M (2011) Endemic plants of Japan. In: Kato M, Ebihara A (eds) Endemic plants of Japan. A book series from the National Museum of Nature and Science, no. 11. Tokai University Press, Hatano, pp 3–10 (Japanese; original title translated) Google Scholar
  9. Kerp H, Krings M (1999) Light microscopy of cuticules. In: Jones T (ed) Fossil plants and spores: modern techniques. Geological Society, London, pp 52–56Google Scholar
  10. Kim K, Whang SS, Hill RS (1999) Cuticle micromorphology of leaves of Pinus (Pinaceae) in east and south-east Asia. Bot J Linn Soc 129:55–74Google Scholar
  11. Kubota Y, Shiono T, Kusumoto B (2015) Role of climate and geohistorical factors in driving plant richness patterns and endemicity on the east Asian continental islands. Ecography 38:639–648CrossRefGoogle Scholar
  12. Kubota Y, Kusumoto B, Shiono T, Tanaka T (2017) Phylogenetic properties of Tertiary relict flora in the east Asian continental islands: imprint of climatic niche conservatism and in situ diversification. Ecography 40:436–447CrossRefGoogle Scholar
  13. Matsuo H (1963) Notonakajima Flora of Noto Peninsula. In: Geological Survey of Japan (ed) The collaborating association to commemorate the 80th anniversary of the Geological Survey of Japan Tertiary floras of Japan: Miocene floras. Geological Survey of Japan, Kawasaki, pp 219–243 (245–258, pls. 41–56) Google Scholar
  14. Miki S (1941) On the change of flora in Eastern Asia since Tertiary Period. (I) The clay or lignite beds flora in Japan with special reference to the Pinus trifolia beds in Central Hondo. Jpn J Bot 11:237–303 (pls. 4–7) Google Scholar
  15. Miki S (1957) Pinaceae of Japan, with special reference to its remains. J Inst Polytech Osaka City Univ Ser D 8:221–272 (pls. 1–10) Google Scholar
  16. Miki S, Sakamoto T (1961) Neogene flora from Sasazu in Toyama Prefecturte, Japan. Professor Jiro Makiyama memorial volume, pp 259–264 [pls. 1, 2 (in Japanese with English abstract)] Google Scholar
  17. Milne RI, Abbott RJ (2002) The origin and evolution of tertiary relict floras. Adv Bot Res 38:281–314CrossRefGoogle Scholar
  18. Mittermeier RA, Gil PR, Hoffman M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, da Fonseca GAB (2005) Hotspots revisited: Earth’s biologically richest and most endangered terrestrial ecoregions. University of Chicago Press, ChicagoGoogle Scholar
  19. Nakayama K, Todo Collaborative Research Group (1989) Sedimentary basins of the Seto Group. Earth Sci (Chikyu Kagaku) 43:40–49 (in Japanese with English abstract) Google Scholar
  20. Nishida S, Itokazu Y (1976) A palynological study of the Shimajiri Group, Nansei Islands. Mar Sci/mo (Gekkan Kaiyo) 8:57–62 (Japanese with English abstract) Google Scholar
  21. Ogasawara K, Takano M, Nagato H, Nakano T (2008) Cenozoic molluscan faunas and climatic changes in the northern Pacific related to Pacific gateways: review and perspective. Bull Geol Surv Japan 59:355–364CrossRefGoogle Scholar
  22. Parks M, Cronn R, Liston A (2012) Separating the wheat from the chaff: mitigating the effects of noise in a plastome phylogenomic data set from Pinus L. (Pinaceae). BMC Evol Biol 12:100CrossRefPubMedPubMedCentralGoogle Scholar
  23. Saladin B, Leslie AB, Wüest RO, Litsios G, Conti E, Salamin N, Zimmermann NE (2017) Fossils matter: improved estimates of divergence times in Pinus reveal older diversification. BMC Evol Biol 17:95CrossRefPubMedPubMedCentralGoogle Scholar
  24. Saneyoshi M, Nakayama K, Tsukagoshi M (2000) Depositional processes of plant material assemblages in fluvial sediments: examples from the plant megafossils in Miocene Tokiguchi Porcelain Clay Formation at Onada mine in Tajimi, central Japan. Earth Sci (Chikyu Kagaku) 54:127–143 (Japanese with English abstract) Google Scholar
  25. Suharyanto, Shiraishi S (2011) Nucleotide diversities and genetic relationship in the three Japanese pine species; Pinus thunbergii, Pinus densiflora, and Pinus luchuensis. Diversity 3:121–135CrossRefGoogle Scholar
  26. Takahashi K, Matsumoto Y (1964) Pollenanalyse der Kohlen aus der Yaeyama-Schichtengruppe der Iriomote Insel von der Yaeyama-Inselgruppe. In: Reports of the Committee on Foreign Scientific Research, Kyushu University (second report of the Kyushu University expedition to the Yaeyama Group, Ryukyus), offprint, vol 2. Kyushu Univ, Fukuoka, pp 35–46 (Japanese with German abstract) Google Scholar
  27. Tanai T (1961) Neogene floral change in Japan. J Fac Sci Hokkaido Univ Ser 4 Geol Mineral 11:119–398Google Scholar
  28. Tanai T (1967) Tertiary floral changes of Japan. In: Jubilee Publication in the commemoration of Professor Yasuo Sasa, Dr. Sc. 60th Birthday. Jubilee Committee of Professor Yasuo Sasa, Dr. Sc. 60th Birthday, Sapporo, pp 317–334Google Scholar
  29. Tanai T (1991) Tertiary climatic and vegetational changes in the Northern Hemisphere. J Geogr 100:951–966 (Japanese with English abstract) CrossRefGoogle Scholar
  30. Tanai T (1992) Tertiary vegetational history of East Asia. Bull Mizunami Fossil Mus 19:125–163 (Japanese with English abstract) Google Scholar
  31. Tiffney BH (1985) Perspectives on the origin of the floristic similarity between eastern Asia and eastern North America. J Arnold Arbor 66:73–94CrossRefGoogle Scholar
  32. Tsuda K, Itoigawa J, Yamanoi T (1986) Mangrove swamp fauna and flora in the Middle Miocene of Japan. In: Kotaka T, Marincovich L Jr (eds) Japanese Cenozoic Molluscs—their origin and migration. Palaeontological Society of Japan, Special Papers, no. 29. Palaeontological Society of Japan, Tokyo, pp 129–134Google Scholar
  33. Uemura K (1986) Late Miocene Plants from Onbara in Northern Okayama Pref., Southwestern Honshu, Japan. Bull Nat Sci Mus Tokyo Ser C 12:121–130Google Scholar
  34. Ujiié H (1994) Early Pleistocene birth of the Okinawa Trough and Ryukyu Island Arc at the northwestern margin of the Pacific: evidence from Late Cenozoic planktonic foraminiferal zonation. Palaeogeogr Palaeoclimatol Palaeoecol 108:457–474CrossRefGoogle Scholar
  35. Wang XR, Tsumura Y, Yoshimaru H, Nagasaka K, Szmidt AE (1999) Phylogenetic relationships of Eurasian pines (Pinus, Pinaceae) based on chloroplast rbcL, matK, rpl20-rps18 spacer, and trnV intron sequences. Amer J Bot 86:1742–1753CrossRefGoogle Scholar
  36. Wolfe JA (1975) Some aspects of plant geography in the northern hemisphere during the late Cretaceous and Tertiary. Ann Mo Bot Gard 62:264–279CrossRefGoogle Scholar
  37. Yamada M, Yamada T (2017) Ovuliferous scale anatomies of Pinus species and their value for classification above the species level. Bot J Linn Soc 183:633–643CrossRefGoogle Scholar
  38. Yamada T, Yamada M, Tsukagoshi M (2014) Fossil records of subsection Pinus (genus Pinus, Pinaceae) from the Cenozoic in Japan. J Plant Res 127:193–208CrossRefPubMedGoogle Scholar
  39. Yamada T, Yamada M, Tsukagoshi M (2015) Taxonomic revision of Pinus fujiii (Yasui) Miki (Pinaceae) and its implication for the phytogeography of the Section Trifoliae in East Asia. PLoS One 10: e0143512. doi: CrossRefPubMedPubMedCentralGoogle Scholar
  40. Yamanoi T, Tsuda K (1986) On the conditions of Paleo-Mangrove forest in the Kurosedani Formation (Middle Miocene), Central Japan. Mem Nat Sci Mus Tokyo 19:55–66 (Japanese with English abstract) Google Scholar
  41. Yasui K (1928) Studies on the structure of lignite, brown coal, and bituminous coal in Japan. J Fac Sci Imp Univ Tokyo Sect 3 Bot 3:381–468 (pls. 9–24) Google Scholar
  42. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK 2017

Authors and Affiliations

  1. 1.School of Natural System, College of Science and EngineeringKanazawa UniversityKanazawaJapan

Personalised recommendations