Journal of Forest Research

, Volume 19, Issue 1, pp 154–165 | Cite as

What controls the distribution of the Japanese endemic hemlock, Tsuga diversifolia? Footprint of climate in the glacial period on current habitat occupancy

  • Ikutaro Tsuyama
  • Katsuhiro Nakao
  • Motoki Higa
  • Tetsuya Matsui
  • Koji Shichi
  • Nobuyuki Tanaka
Original Article


Plant distributions are thought to be controlled by climate at large scales, and by non-climatic factors including soil conditions, topography and biotic interactions at smaller scales. However, not all plant distributions are explained by the current environment. Lags between current plant distributions and suitable environment for them are suggested to exist, which is often called empty habitat. To identify the existence and cause of lags between current climate and the distribution of Tsuga diversifolia, climatic conditions for the species distribution were clarified and potential habitats under current and the last glacial maximum (LGM; 21 ka) climates have been projected. The relationships between T. diversifolia distribution and climatic variables were explored using a classification tree model and a generalized additive model based on high-resolution (ca. 1 km) climatic data and a nationwide distribution database. The models were highly accurate. We revealed that T. diversifolia requires high summer precipitation even in humid Japanese environments. Areas with cool and wet summers were classified as potential habitat. Empty habitat for the focal species was identified in Hokkaido. Meanwhile, no potential habitat was projected in Hokkaido under the LGM. Additional experiments that varied temperature and summer precipitation during the LGM showed that the potential habitat was projected in Hokkaido irrespective of temperature decrease if summer precipitation increased nearly equal to the current climate. These results suggest that T. diversifolia vanished from Hokkaido, where fossil evidence indicated its occurrence until the late Neogene, during the glacial periods of the Pleistocene because of increased summer dryness.


Empty habitat Past climate simulations Precipitation in summer Species distribution models Last glacial maximum 



We thank Mr Hiromu Daimaru, Dr Masatsugu Yasuda, Ms Etsuko Nakazono and Dr Jonathan Lenoir for their valuable comments on this study. We also thank the anonymous editor and reviewer for their helpful and valuable comments on our manuscript. This research was supported by the Environment Research and Technology Development Fund (S-8) of the Ministry of the Environment, Japan.

Supplementary material

10310_2013_399_MOESM1_ESM.pdf (17.6 mb)
Supplementary Figures (17.5 MB)


  1. Aizawa M (2005) Reconfirmation of localities recorded up to today by examination of voucher specimens and by investigation in the habitats—case study of the five subalpine conifer species in Honshu, Japan. J Phytogeogr Taxon 53:13–42 (in Japanese with English summary)Google Scholar
  2. Alba Sánchez F, López Sáez J, Benito de Pando B, Linares J, Nieto Lugilde D, López Merino L (2010) Past and present potential distribution of the Iberian Abies species: a phytogeographic approach using fossil pollen data and species distribution models. Divers Distrib 16:214–228CrossRefGoogle Scholar
  3. Armonies W, Reise K (2003) Empty habitat in coastal sediments for populations of macrozoobenthos. Helgol Mar Res 56:279–287Google Scholar
  4. Bartlein P, Harrison S, Brewer S, Connor S, Davis B, Gajewski K, Guiot J, Harrison-Prentice T, Henderson A, Peyron O, Prentice I, Scholze M, Seppä H, Shuman B, Sugita S, Thompson R, Viau A, Williams J, Wu H (2011) Pollen-based continental climate reconstructions at 6 and 21 ka: a global synthesis. Clim Dyn 37:775–802CrossRefGoogle Scholar
  5. Benito Garzón M, Sánchez de Dios R, Sáinz Ollero H (2007) Predictive modelling of tree species distributions on the Iberian Peninsula during the last glacial maximum and Mid-Holocene. Ecography 30:120–134CrossRefGoogle Scholar
  6. Clark L, Pregibon D (1992) Tree-based models. In: Chambers J, Hastie T (eds) Statistical models in S. Wadsworth & Brooks, Pacific Grove, pp 377–419Google Scholar
  7. Collins W, Bitz C, Blackmon M, Bonan G, Bretherton C, Carton J, Chang P, Doney S, Hack J, Henderson T, Kiehl J, Large W, McKenna D, Santer B, Smith R (2006) The community climate system model version 3 (CCSM3). J Clim 19:2122–2143CrossRefGoogle Scholar
  8. Comes H, Kadereit J (1998) The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci 3:432–438CrossRefGoogle Scholar
  9. Cowling S, Sykes M (1999) Physiological significance of low atmospheric CO2 for plant–climate interactions. Quat Res 52:237–242CrossRefGoogle Scholar
  10. De’ath G, Fabricius K (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192CrossRefGoogle Scholar
  11. Farjon A (1990) Pinaceae. Drawings and descriptions of the genera Abies, Cedrus, Pseudolarix, Keteleeria, Nothotsuga, Tsuga, Cathaya, Pseudotsuga, Larix and Picea. Koeltz, KönigsteinGoogle Scholar
  12. Gavin DG, Hu FS (2006) Spatial variation of climatic and non-climatic controls on species distribution: the range limit of Tsuga heterophylla. J Biogeogr 33:1384–1396CrossRefGoogle Scholar
  13. Hannah L, Midgley G, Millar D (2002) Climate change-integrated conservation strategies. Glob Ecol Biogeogr 11:485–495CrossRefGoogle Scholar
  14. Hayashi Y (1960) Nipponsan-shinyoju no Bunrui to Bumpu (Taxonomical and phytogeographical study of Japanese conifers). Norin-shuppan, Tokyo (in Japanese)Google Scholar
  15. Higgins S, Lavorel S, Revilla E (2003) Estimating plant migration rates under habitat loss and fragmentation. Oikos 101:354–366CrossRefGoogle Scholar
  16. Hijmans R, Cameron S, Parra J, Jones P, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  17. Horikawa Y (1972) Atlas of the Japanese flora: an introduction to plant sociology of East Asia. Gakken, TokyoGoogle Scholar
  18. Jansson R (2003) Global patterns in endemism explained by past climatic change. Proc R Soc Lond B 270:583–590CrossRefGoogle Scholar
  19. K-1 Model Developers (2004) K-1 coupled GCM (MIROC) description. K-1 Tech Rep 1:1–34Google Scholar
  20. Kanzaki M (1984) Regeneration in subalpine coniferous forests I. Mosaic structure and regeneration process in a Tsuga diversifolia forest. Bot Mag Tokyo 97:297–311CrossRefGoogle Scholar
  21. Karizumi N (1979) Jyumoku-konkei Zu-setsu (Illustrations of tree roots). Seibundo Shinkosha, Tokyo (in Japanese)Google Scholar
  22. Lassoie J, Hinckley T, Grier C (1985) Coniferous forests of the Pacific Northwest. In: Chabot B, Mooney H (eds) Physiological ecology of North American plant communities. Chapman & Hall, New York, pp 127–161CrossRefGoogle Scholar
  23. Lepage B (2003) A new species of Tsuga (Pinaceae) from the middle Eocene of Axel Heiberg Island, Canada, and an assessment of the evolution and biogeographical history of the genus. Bot J Linn Soc 141:257–296CrossRefGoogle Scholar
  24. Matsui T, Yagihashi T, Nakaya T, Tanaka N, Taoda H (2004) Climatic controls on distribution of Fagus crenata forests in Japan. J Veg Sci 15:57–66Google Scholar
  25. Metz C (1978) Basic principles of ROC analysis. Semin Nucl Med 8:283–298CrossRefPubMedGoogle Scholar
  26. Meyer EM, Peterson A (2006) Conservatism of ecological niche characteristics in North American plant species over the Pleistocene-to-Recent transition. J Biogeogr 33:1779–1789CrossRefGoogle Scholar
  27. Nakagawa T, Tarasov P, Nishida K, Gotanda K, Yasuda Y (2002) Quantitative pollen-based climate reconstruction in central Japan: application to surface and Late Quaternary spectra. Quat Sci Rev 21:2099–2113CrossRefGoogle Scholar
  28. Nakamura T, Obata K (1982) Differences in ecological character between Abies veitchii and Tsuga diversifolia I. Growth of saplings in gaps of subalpine forest on Mt. Fuji. Bull Tokyo Univ For 72:121–138 (in Japanese with English summary)Google Scholar
  29. Normand S, Ricklefs R, Skov F, Bladt J, Tackenberg O, Svenning J (2011) Postglacial migration supplements climate in determining plant species ranges in Europe. Proc R Soc Lond B 278:3644–3653CrossRefGoogle Scholar
  30. Ohsawa M (1993) Latitudinal pattern of mountain vegetation zonation in southern and eastern Asia. J Veg Sci 4:13–18CrossRefGoogle Scholar
  31. Opdam P, Wascher D (2004) Climate change meets habitat fragmentation: linking landscape and biogeographical scale levels in research and conservation. Biol Conserv 117:285–297CrossRefGoogle Scholar
  32. Pearson RG, Dawson TP (2003) Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Glob Ecol Biogeogr 12:361–371CrossRefGoogle Scholar
  33. Pearson RG, Dawson TP, Liu C (2004) Modelling species distributions in Britain: a hierarchical integration of climate and land-cover data. Ecography 27:285–298CrossRefGoogle Scholar
  34. Prentice I, Harrison S (2009) Ecosystem effects of CO2 concentration: evidence from past climates. Clim Past 5:297–307CrossRefGoogle Scholar
  35. R Development Core Team (2011) R version 2.12.2. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  36. Rodríguez Sánchez F, Arroyo J (2008) Reconstructing the demise of Tethyan plants: climate-driven range dynamics of Laurus since the Pliocene. Glob Ecol Biogeogr 17:685–695CrossRefGoogle Scholar
  37. Sakaguchi S, Sakurai S, Yamasaki M, Isagi Y (2010) How did the exposed seafloor function in postglacial northward range expansion of Kalopanax septemlobus? Evidence from ecological niche modelling. Ecol Res 25:1183–1195CrossRefGoogle Scholar
  38. Sakai A, Kurahashi A (1975) Freezing resistence of conifers in Japan with special reference to their distributions. Jpn J Ecol 25:192–200 (in Japanese with English summary)Google Scholar
  39. Silva D, Badeau V, Legay M, Corcket E, Dupouey J (2012) Tracking human impact on current tree species distribution using plant communities. J Veg Sci 23:313–324CrossRefGoogle Scholar
  40. Sohma K, Tsuji S (1987) Shokusei (Vegetation). In: For Quaternary Research JA (ed) Explanatory text for Quaternary maps of Japan. University of Tokyo Press, Tokyo, pp 80–86 (in Japanese)Google Scholar
  41. Sugita H (2002) Akouzantairin no Haifukusei to sono Seiritsukikou (Factors for differences in subalpine forest vegetations between Sea of Japan side and Pacific Ocean side). In: Kajimoto T, Daimaru H, Sugita H (eds) Snow environment and plant ecology of Japanese northern mountains. Tokai University Press, Tokyo, pp 74–88 (in Japanese)Google Scholar
  42. Sugita H, Tani M (2001) Difference in microhabitat-related regeneration patterns between two subalpine conifers, Tsuga diversifolia and Abies mariesii, on Mount Hayachine, northern Honshu, Japan. Ecol Res 16:423–433CrossRefGoogle Scholar
  43. Svenning JC, Normand S, Kageyama M (2008a) Glacial refugia of temperate trees in Europe: insights from species distribution modelling. J Ecol 96:1117–1127CrossRefGoogle Scholar
  44. Svenning JC, Normand S, Skov F (2008b) Postglacial dispersal limitation of widespread forest plant species in nemoral Europe. Ecography 31:316–326CrossRefGoogle Scholar
  45. Svenning JC, Skov F (2004) Limited filling of the potential range in European tree species. Ecol Lett 7:565–573CrossRefGoogle Scholar
  46. Svenning JC, Skov F (2007) Could the tree diversity pattern in Europe be generated by postglacial dispersal limitation? Ecol Lett 10:453–460CrossRefPubMedGoogle Scholar
  47. Swets J (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293CrossRefPubMedGoogle Scholar
  48. Tanai T (1961) Neogene floral change in Japan. J Fac Sci Hokkaido Univ Ser 4 Geol Mineral 11:119–398Google Scholar
  49. Tanaka N (2007) PRDB (Phytosociological Relevé Data Base) [online]. Accessed 2 Nov 2011
  50. Tanaka N, Nakazono E, Tsuyama I, Matsui T (2009) Assessing impact of climate warming on potential habitats of ten conifer species in Japan. Glob Environ Res 14:153–164 (in Japanese with English summary)Google Scholar
  51. Tatewaki M, Ito K, Tohyama M (1964) Phytosociological study on the forests of Japanese Hemlock (Tsuga diversifolia). Res Bull Coll Exp For Hokkaido Univ 23:83–146 (in Japanese with English summary)Google Scholar
  52. Thuiller W, Araújo M, Lavorel S (2003) Generalized models vs. classification tree analysis: oredicting spatial distributions of plant species at different scales. J Veg Sci 14:669–680CrossRefGoogle Scholar
  53. Thuiller W, Lavorel S, Araújo M, Sykes M, Prentice I (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA 102:8245–8250CrossRefPubMedPubMedCentralGoogle Scholar
  54. Tsukada M (1982) Late-quaternary shift of Fagus distribution. J Plant Res 95:203–217Google Scholar
  55. Tsukada M (1983) Vegetation and climate during the last glacial maximum in Japan. Quat Res 19:212–235CrossRefGoogle Scholar
  56. Tsukada M (1985) Map of vegetation during the last glacial maximum in Japan. Quat Res 23:369–381CrossRefGoogle Scholar
  57. Tsuyama I, Matsui T, Ogawa M, Kominami Y, Tanaka N (2008) Habitat prediction and impact assessment of climate change on Sasa kurilensis in eastern Honshu, Japan. Theory Appl GIS 16:11–25 (in Japanese with English summary)Google Scholar
  58. Tsuyama I, Nakao K, Matsui T, Higa M, Horikawa M, Kominami Y, Tanaka N (2011) Climatic controls of a keystone understory species, Sasamorpha borealis, and an impact assessment of climate change in Japan. Ann For Sci 68:689–699CrossRefGoogle Scholar
  59. Wood S (2006) Generalized additive models: an introduction with R. Chapman & Hall/CRC, Boca RatonGoogle Scholar
  60. Woodward F (1996) Climate and plant distribution. Cambridge University Press, CambridgeGoogle Scholar

Copyright information

© The Japanese Forest Society and Springer Japan 2013

Authors and Affiliations

  • Ikutaro Tsuyama
    • 1
  • Katsuhiro Nakao
    • 1
  • Motoki Higa
    • 1
  • Tetsuya Matsui
    • 2
  • Koji Shichi
    • 3
  • Nobuyuki Tanaka
    • 1
  1. 1.Department of Plant EcologyForestry and Forest Products Research InstituteTsukubaJapan
  2. 2.Hokkaido Research StationForestry and Forest Products Research InstituteSapporoJapan
  3. 3.Department of Forest Site EnvironmentForestry and Forest Products Research InstituteTsukubaJapan

Personalised recommendations