Advertisement

Trees

, Volume 29, Issue 1, pp 171–184 | Cite as

Differences in growth characteristics and dynamics of elements in seedlings of two birch species grown in serpentine soil in northern Japan

  • Masazumi KayamaEmail author
  • Takayoshi Koike
Original Paper

Abstract

Key message

Seedlings of two birch species were grown in serpentine soil, with Betula ermanii showing high tolerance.

Abstract

Betula ermanii and Betula platyphylla var. japonica, two typical light-demanding-deciduous trees in northern Japan, usually invade disturbed areas. B. ermanii can invade serpentine soil and grow in it, whereas B. platyphylla var. japonica can hardly regenerate in it. Serpentine soil is distributed throughout Japan and is characterized by excessive Mg and heavy metals (Ni, Cr, and Co) which can lead to suppressed plant growth. We examined the tolerance of the two Betula species by planting seedlings in serpentine and non-serpentine (brown forest) soils. The dry mass of each organ was suppressed in both birches planted in serpentine soil, and the photosynthetic rate was reduced by accumulation of Ni. Also, uptakes of K and Ca were inhibited by accumulation of Mg, Ni, Cr and Co. B. ermanii planted in serpentine soil showed high value of net assimilation rate in the second year and maintained the photosynthetic rate from June to September. The effects of Mg, Ni, Cr and Co accumulation were small on the relative growth rate of B. ermanii. In contrast, B. platyphylla var. japonica planted in serpentine soil showed decreased photosynthetic rate in September and smaller net assimilation rate than B. ermanii at the same time. In addition, B. platyphylla var. japonica showed decreased relative growth rate, induced by accumulation of Mg in leaves and Co in roots. We conclude that B. ermanii has the high advantage of regenerating in serpentine soil.

Keywords

Birch Serpentine soil Photosynthetic capacity Heavy metal Nutrient physiology 

Notes

Author contribution statement

M. K. and T. K. designed the experiments and grew seedlings of birch species. M. K. conducted the experiments, measured the photosynthetic rates, and analyzed the various nutrients. Both analyzed the data, discussed the results, and co-authored the paper.

Acknowledgments

We thank Prof. K. Sasa, Dr. Y. Akibayashi, and Prof. F. Satoh for their valuable comments on this study. We are grateful to the technical staff of Teshio Experimental Forest of Hokkaido University for their excellent technical assistance. Our thanks are due to Dr. S. Kitaoka and Ms. Y. Yanagihara for preparation of the nurseries. Analyses of plant organs were carried out at the Kyushu Research Center, Forestry and Forest Products Research Institute. We are indebted to Dr. K. Makoto and Ms. N. Aoki of the Kyushu Research Center for the analyses. For the ICP analyses of Ni, Cr, and Co concentrations, we are grateful to Dr. H. Kubotera of the National Agriculture and Food Research Organization. Thanks are also due to Mr. E. Agathokleous, Diploma of AUA, and Dr. Anthony Garrett of SCITEXT in Cambridge, UK, for English proofreading. Financial support to M. K. and T. K. by the JSPS and the Japan Science Society is gratefully acknowledged.

Conflict of interest

The source support for this study is a non-profit organization (Japan Society for the Promotion of Science, and Japan Science Society). We declare that our research has no conflict of interest.

References

  1. Alexander EB, Coleman RG, Keeler-Wolf T, Harrison SP (2007) Serpentine geoecology of western north America, geology, soils and vegetation. Oxford University Press, New YorkGoogle Scholar
  2. Ali B, Hayat S, Ahmad A (2010) Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J Plant Interact 5:223–231CrossRefGoogle Scholar
  3. American Public Health Association, American Water Works Association, Water Environment Federation (1998) Standard methods for the examination of water and wastewater. American Public Health Association, Washington, DCGoogle Scholar
  4. Baccouch S, Chaoui A, El Ferjari E (1998) Nickel toxicity: effects on growth and metabolism of maize. J Plant Nutr 21:577–588CrossRefGoogle Scholar
  5. Bai JH, Cui BS, Deng W, Wang QG, Ding QY (2007) Plant Pb contents in elevation zones of the Changbai mountain national nature reserve, China. Pedosphere 17:229–234CrossRefGoogle Scholar
  6. Baillon F, Dalschaert X, Grassi S, Geiss F (1988) Spruce photosynthesis: possibility of early damage diagnosis due to exposure to magnesium or potassium deficiency. Trees 2:173–179CrossRefGoogle Scholar
  7. Baker AJM (1987) Metal tolerance. New Phytol 106:93–111CrossRefGoogle Scholar
  8. Blandon DMZ, Satoh F, Matsuda K, Sasa K, Igarashi T (1994) The mineral condition of soils and tree species in serpentine and non-serpentine areas of northern Hokkaido. Res Bull Hokkaido Univ For 51:1–13Google Scholar
  9. Bown HE, Watt MS, Clinton PW, Mason EG, Richardson B (2007) Partitioning concurrent influences of nitrogen and phosphorus supply on photosynthetic model parameters of Pinus radiata. Tree Physiol 27:335–344PubMedCrossRefGoogle Scholar
  10. Brady K, Kruckberg A, Bradshaw H (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  11. Brooks RR (1987) Serpentine and its vegetation. Dioscorides Press, PortlandGoogle Scholar
  12. Cocucci SM, Morgutti S (1986) Stimulation of proton extrusion by K+ and divalent cations (Ni2+, Co2+, Zn2+) in maize root segments. Physiol Plant 68:497–501CrossRefGoogle Scholar
  13. Ding Y, Luo W, Xu G (2006) Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice. Ann Appl Biol 149:111–123CrossRefGoogle Scholar
  14. Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78:9–19CrossRefGoogle Scholar
  15. Gabbrielli R, Pandolfini T, Vergnano O, Palandri MR (1990) Comparison of two serpentine species with different nickel tolerance strategies. Plant Soil 122:271–277CrossRefGoogle Scholar
  16. Ishibashi S (1998) The relationship between natural regeneration and land/forest description in natural cool-temperature and boreal forests. J Jpn For Soc 80:74–79 (in Japanese and English summary)Google Scholar
  17. Jones MD, Hutchinson TC (1988a) Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. I Effects on growth, photosynthesis, respiration and transpiration. New Phytol 108:451–459CrossRefGoogle Scholar
  18. Jones MD, Hutchinson TC (1988b) Nickel toxicity in mycorrhizal birch seedlings infected with Lactarius rufus or Scleroderma flavidum. II Uptake of nickel, calcium, magnesium, phosphorus and iron. New Phytol 108:461–470CrossRefGoogle Scholar
  19. Kanai S, Moghaieb RE, El-Shemy HA, Panigrahi R, Mohapatra PK, Ito J, Nguyen NT, Saneoka H, Fujita K (2011) Potassium deficiency affects water status and photosynthetic rate of the vegetative sink in the green house tomato prior to its effects on source activity. Plant Sci 180:368–374PubMedCrossRefGoogle Scholar
  20. Kayama M (2006) Study on the adaptation capacity of spruce species grown on serpentine soil and its application for forest rehabilitation. Res Bull Hokkaido Univ For 63:33–78 (in Japanese and English summary)Google Scholar
  21. Kayama M, Quoreshi AM, Uemura S, Koike T (2005) Differences in growth characteristics and dynamics of elements absorbed in seedlings of three spruce species raised on serpentine soil in northern Japan. Ann Bot 95:661–672PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kayama M, Choi DS, Tobita H, Utsugi H, Kitao M, Maruyama Y, Nomura M, Koike T (2006) Comparison of growth characteristics and tolerance to serpentine soil of three ectomycorrhizal spruce seedlings in northern Japan. Trees 20:430–440CrossRefGoogle Scholar
  23. Kayama M, Kitaoka S, Wang W, Choi DS, Koike T (2007) Needle longevity, photosynthetic rate and nitrogen concentration of eight spruce taxa planted in northern Japan. Tree Physiol 27:1585–1593PubMedCrossRefGoogle Scholar
  24. Kitao M, Lei TT, Koike T (1999) Effects of manganese in solution culture on the growth of five deciduous broad-leaved tree species with different successional characters from northern Japan. Photosynthetica 36:31–40CrossRefGoogle Scholar
  25. Kobayashi H, Masaoka Y, Sato S (2005) Effects of excess magnesium on the growth and mineral content of rice and Echinochloa. Plant Prod Sci 8:38–43CrossRefGoogle Scholar
  26. Koike T (1995) Physiological ecology of the growth characteristics of Japanese mountain birch in northern Japan: a comparison with Japanese white birch. In: Box EO, Peet RK, Masuzawa T, Yamada I, Fujiwara K, Maycock PF (eds) Vegetation science in forestry. Kluwer Academic Publishers, Dordrecht, pp 409–422Google Scholar
  27. Koyama H, Yajima T (1989) The distributional pattern and stand structure of seedlings on the raked ground. Trans Mtg Hokkaido Br Jap For Soc 37:55–57 (in Japanese)Google Scholar
  28. Kubota J, Cary EE (1982) Cobalt, molybdenum, and selenium. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis, Part 2. Chemical and microbiological properties, 2nd edn. Soil Science Society of America Inc, Madison, pp 485–490Google Scholar
  29. Lambers H, Chapin FS III, Pons TL (1998) Plant physiological ecology. Springer, New YorkCrossRefGoogle Scholar
  30. Lazarus BE, Richards JH, Claassen VP, O’Dell RE, Ferrell MA (2011) Species specific plant–soil interactions influence plant distribution on serpentine soils. Plant Soil 342:327–344CrossRefGoogle Scholar
  31. Liu J, Duan CQ, Zhang XH, Zhu YN, Hu C (2009) Subcellular distribution of chromium in accumulating plant Leersia hexandra Swartz. Plant Soil 322:187–195CrossRefGoogle Scholar
  32. Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, LondonGoogle Scholar
  33. Matsumura H, Mikami C, Sakai Y, Murayama K, Izuta T, Yonekura T, Miwa M, Kohno Y (2005) Impacts of elevated O3 and/or CO2 on growth of Betula platyphylla, Betula ermanii, Fagus crenata, Pinus densiflora and Cryptomeria japonica seedlings. J Agric Meteorol 60:1121–1124Google Scholar
  34. Millard P (1996) Ecophysiology of the internal cycling of nitrogen for tree growth. Z Pflanzenernähr Bodenk 159:1–10Google Scholar
  35. Miller SP, Cumming JR (2000) Effects of serpentine soil factors on Virginia pine (Pinus virginiana). Tree Physiol 20:1129–1135PubMedCrossRefGoogle Scholar
  36. Miyawaki A (1988) Vegetation of Japan. Hokkaido, Shibundo (in Japanese and English summary)Google Scholar
  37. Mizuno N, Nosaka S (1992) The distribution and extent of serpentinized areas in Japan. In: Roberts BA, Proctor J (eds) The ecology of areas with serpentinized rocks. Kluwer, Dordrecht, pp 271–311CrossRefGoogle Scholar
  38. Molas J (2002) Changes of chloroplast ultrastructure and total chlorophyll concentration in cabbage leaves caused by excess of organic Ni (II) complexes. Environ Exp Bot 47:115–126CrossRefGoogle Scholar
  39. Nakata M, Kojima S (1987) Effects of serpentine substrate on vegetation and soil development with special reference to Picea glehnii in Teshio district, Hokkaido, Japan. For Ecol Manage 20:265–290CrossRefGoogle Scholar
  40. Neilsen D, Millard P, Neilsen GH, Hogue EJ (1997) Sources of N for leaf growth in a high-density apple (Malus domestica) orchard irrigated with ammonium nitrate solution. Tree Physiol 17:733–739PubMedCrossRefGoogle Scholar
  41. Oze C, Fendorf S, Bird DK, Coleman RG (2004) Chromium geochemistry of serpentine soils. Int Geol Rev 46:97–126CrossRefGoogle Scholar
  42. Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60:149–181CrossRefGoogle Scholar
  43. Palm E, Brady K, Van Volkenburgh E (2012) Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Funct Plant Biol 39:679–688CrossRefGoogle Scholar
  44. Pandolfini T, Gabrielli R, Comparini C (1992) Nickel toxicity and peroxidase activity in seedlings of Triticum aestivum L. Plant Cell Environ 15:719–725CrossRefGoogle Scholar
  45. Pettigrew WT (2008) Potassium influences on yield and quality production for maize, wheat, soybean and cotton. Physiol Plant 133:670–681PubMedCrossRefGoogle Scholar
  46. Proctor J (1971) The plant ecology of serpentine III. The influence of a high calcium/magnesium ratio and high nickel and chromium levels in some British and Swedish serpentine soil. J Ecol 59:827–842CrossRefGoogle Scholar
  47. Raaimakers D, Boot RGA, Dijkstra P, Pot S, Pons T (1995) Photosynthetic rates in relation to leaf phosphorus content in pioneer versus climax tropical rainforest trees. Oecologia 102:120–125CrossRefGoogle Scholar
  48. Rao M, Sharp RE, Boyer J (1987) Leaf Magnesium alters photosynthetic response to low water potentials in sunflower. Plant Physiol 84:1214–1219PubMedCentralPubMedCrossRefGoogle Scholar
  49. Santana KB, de Almeida AAF, Souza VL, Mangabeira PAO, Silva DD, Gomes FP, Dutruch L, Loguercio LL (2012) Physiological analysis of Genipa americana L. reveals a tree with ability as phytostabilizer and rhizofilterer of chromium ions for phytoremediation of polluted watersheds. Environ Exp Bot 80:35–42CrossRefGoogle Scholar
  50. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Rus J Plant Physiol 53:257–277CrossRefGoogle Scholar
  51. Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254CrossRefGoogle Scholar
  52. Sinha P, Khurana N, Nautiyal N (2012) Induction of oxidative stress and antioxidant enzymes by excess cobalt in mustard. J Plant Nutr 35:952–960CrossRefGoogle Scholar
  53. Takahashi K, Azuma H, Yasue K (2003) Effects of climate on the radial growth of tree species in the upper and lower distribution limits of an altitudinal ecotone on mount Norikura, central Japan. Ecol Res 18:549–558CrossRefGoogle Scholar
  54. Takikawa S, Kobayashi M, Mizuno H, Haruki M (1994) Natural-seedling regeneration in a serpentine area in the Teshio Experimental Forest of Hokkaido University. Trans Mtg Hokkaido Br Jap For Soc 42:82–84 (in Japanese)Google Scholar
  55. Tatewaki M, Igarashi T (1971) Forest vegetation in the Teshio and the Nakagawa district experimental forests of Hokkaido University, Prov. Teshio, N. Hokkaido, Japan. Res Bull Hokkaido Univ For 28:1–192 (in Japanese and English summary)Google Scholar
  56. Thornley JHM (1976) Mathematical models in plant physiology. Academic Press, LondonGoogle Scholar
  57. Tilistone GH, Macnair MR (1997) Nickel tolerance and copper-nickel co-tolerance in Mimulus guttatus from copper mine and serpentine habitats. Plant Soil 191:173–180CrossRefGoogle Scholar
  58. Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emission in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066PubMedCrossRefGoogle Scholar
  59. Vernay P, Gauthier-Moussard C, Jean L, Bordas F, Faure O, Ledoigt G, Hitmi A (2008) Effect of chromium species of phytochemical and physiological parameters in Datura innoxia. Chemosphere 72:763–771PubMedCrossRefGoogle Scholar
  60. Yamada K (1999) Growth of secondary forests on serpentine soil after different soil disturbance intensity. J Jpn For Soc 81:291–297 (in Japanese and English summary)Google Scholar
  61. Yamada K (2001) Regeneration technique on the serpentine soil region of northern Hokkaido. Bull Hokkaido For Res Inst 38:23–36 (in Japanese and English summary)Google Scholar
  62. Yang X, Baligar VC, Martens DC, Clark RB (1996) Plant tolerance to nickel toxicity. II Nickel effects on influx and transport of mineral in four plant species. J Plant Nutr 19:265–279CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Hokkaido University Forests, FSCSapporoJapan
  2. 2.Silviculture and Forest Ecological StudiesHokkaido UniversitySapporoJapan
  3. 3.Japan International Research Center for Agricultural SciencesTsukubaJapan

Personalised recommendations