Skip to main content
SpringerLink
Log in

Soil Phosphorus Bioavailability and Recycling Increased with Stand Age in Chinese Fir Plantations

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

Phosphorus (P) is a limiting nutrient for plant growth in most forest ecosystems. In response to P deficiency, plants alter root exudates (organic acids, phosphatases, and protons) to increase P bioavailability in soils. However, little is known about how bioavailable P pools (soluble-P, exchangeable-P, hydrolysable-P, and ligand-P extracted by CaCl2, citric acid, enzyme mixture, and HCl solution, respectively) change with stand age, especially for plantation forests. We selected a chronosequence of second-generation Chinese fir [Cunninghamia lanceolata (Lamb.) Hook., Taxodiaceae] plantations with increasing age including 3, 8–11, 16, 20, 25, 29, and 32 years. We measured total P and four bioavailable P pools in organic (O) and mineral horizons, and rhizosphere soil, as well as root exudates in the rhizosphere, litter biomass on the forest floor, and annual P uptake. Soluble-P, exchangeable-P, and ligand-P in the O horizon increased with stand age due to litter accumulation. Exchangeable-P and ligand-P in mineral soil decreased with stand age because of the increasing annual P uptake that depleted inorganic P. Exchangeable-P and ligand-P in the rhizosphere increased with stand age because the decrease in pH and citric acid concentration led to phosphate being more strongly bound to Fe and Al oxyhydroxides. Consequently, the trees’ ability for P mobilization decreased with stand age, but the P recycling within the tree increased. Continuous mineralization of hydrolysable-P by acid phosphatase replenished inorganic P pools, especially in solution. The progressive incorporation of P in the biological cycle with increasing tree age indicates that extending rotation periods might be an appropriate measure to increase P supply.

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

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7
Figure 8

Similar content being viewed by others

References

  • Becker J, Pabst H, Mnyonga J, Kuzyakov Y. 2015. Annual litterfall dynamics and nutrient deposition depending on elevation and land use at Mt. Kilimanjaro. Biogeosciences 12:5635–46.

    CAS  Google Scholar 

  • Bol R, Julich D, Brödlin D, Siemens J, Kaiser K, Dippold MA, Spielvogel S, Zilla T, Mewes D, von Blanckenburg F et al. 2016. Dissolved and colloidal phosphorus fluxes in forest ecosystems—an almost blind spot in ecosystem research. J Plant Nutr Soil Sc 179:425–38.

    CAS  Google Scholar 

  • Boris L, Tomáš L, Manschadi AM. 2018. Arbuscular mycorrhizae modify winter wheat root morphology and alleviate phosphorus deficit stress. Plant Soil Environ 64:47–52.

    Google Scholar 

  • Brandtberg PO, Bengtsson J, Lundkvist H. 2004. Distributions of the capacity to take up nutrients by Betula spp. and Picea abies in mixed stands. For Ecol Manage 198:193–208.

    Google Scholar 

  • Calama R, Montero G. 2004. Interregional nonlinear height-diameter model with random coefficients for stone pine in Spain. Can J Forest Res 34:150–63.

    Google Scholar 

  • Chen CR, Condron LM, Davis MR, Sherlock RR. 2002. Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol Biochem 34:487–99.

    CAS  Google Scholar 

  • Chen CR, Condron LM, Xu ZH. 2008. Impacts of grassland afforestation with coniferous trees on soil phosphorus dynamics and associated microbial processes: a review. For Ecol Manage 255:396–409.

    Google Scholar 

  • Chen LC, Wang H, Yu X, Zhang WD, Lü XT, Wang SL. 2017. Recovery time of soil carbon pools of conversional Chinese fir plantations from broadleaved forests in subtropical regions, China. Sci Total Environ 587:296–304.

    PubMed  Google Scholar 

  • Chen Y, Nguyen THN, Qin J, Jiao Y, Li Z, Ding S, Lu Y, Liu QF, Luo ZB. 2018. Phosphorus assimilation of Chinese fir from two provenances during acclimation to changing phosphorus availability. Environ Exp Bot 153:21–34.

    CAS  Google Scholar 

  • Comerford NB. 2005. Nutrient acquisition by plants: soil factors affecting nutrient bioavailability. Berlin: Springer.

    Google Scholar 

  • Dai XQ, Fu XL, Kou L, Wang HM, Shock CC. 2018. C:N: P stoichiometry of rhizosphere soils differed significantly among overstory trees and understory shrubs in plantations in subtropical China. Can J Forest Res 48:1398–405.

    CAS  Google Scholar 

  • Darch T, Blackwell MSA, Chadwick D, Haygarth PM, Hawkins JMB, Turner BL. 2016. Assessment of bioavailable organic phosphorus in tropical forest soils by organic acid extraction and phosphatase hydrolysis. Geoderma 284:93–102.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deluca TH, Glanville HC, Harrisb M, Emmett BA, Pingree MRA, de Sosa LL, Cerdá-Moreno C, Jones DL. 2015. A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–19.

    CAS  Google Scholar 

  • Deng M, Liu L, Sun Z, Piao S, Ma Y, Chen Y, Wang J, Qiao C, Wang X, Li P. 2016. Increased phosphate uptake but not resorption alleviates phosphorus deficiency induced by nitrogen deposition in temperate Larix principis-rupprechtii plantations. New Phytol 212:1019–29.

    CAS  PubMed  Google Scholar 

  • Fox TR, Miller BW, Rubilar R, Stape JL, Albaugh TJ. 2011. Phosphorus nutrition of forest plantations: the role of inorganic and organic phosphorus. Phosphorus in Action. Springer, Berlin, Heidelberg 317–38.

  • Gao XL, Li XG, Zhao L, Kuzyakov Y. 2019. Regulation of soil phosphorus cycling in grasslands by shrubs. Soil Biol Biochem (submitted).

  • Giles CD, Richardson AE, Cade-Menun BJ, Mezeli MM, Brown LK, Menezes-Blackburn D, Darch T, Blackwell MS, Shand CA, Stutter MI et al. 2018. Phosphorus acquisition by citrate- and phytase-exuding Nicotiana tabacum plant mixtures depends on soil phosphorus availability and root intermingling. Physiol Plant 163:356–71.

    CAS  Google Scholar 

  • Gower ST, Mcmurtrie RE, Murty D. 1996. Aboveground net primary production decline with stand age: potential causes. Trends Ecol Evol 11:378–82.

    CAS  PubMed  Google Scholar 

  • Grinsted MJ, Hedley MJ, White RE, Nye PH. 1982. Plant-induced changes in the rhizosphere of rape (brassica napus var. emerald) seedlings: I. ph change and the increase in p concentration in the soil solution. New Phytol 91:19–29.

    CAS  Google Scholar 

  • Hacker N, Ebeling A, Gessler A, Gleixner G, González MO, De KH, Lange M, Mommer L, Eisenhauer N, Ravenek J et al. 2015. Plant diversity shapes microbe-rhizosphere effects on P mobilisation from organic matter in soil. Ecol Lett 18:1356–65.

    PubMed  Google Scholar 

  • Havlin JL, Beaton JD, Tisdale SL, Nelson WL. 1999. Soil fertility and fertilizers: an introduction to nutrient management. pp 160–98.

  • Hedley MJ, Stewart JWB, Chauhan BS. 1982a. Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations. Soil Sci Soc Am J 46:970–6.

    CAS  Google Scholar 

  • Hedley MJ, White RE, Nye PH. 1982b. Plant-induced changes in the rhizosphere of rape (brassica napus var. emerald) seedlings. III. changes in l value, soil phosphate fractions and phosphatase activity. New Phytol 91:45–56.

    CAS  Google Scholar 

  • Hinsinger P. 2001. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–95.

    CAS  Google Scholar 

  • Institute of Soil Science, Chinese Academy of Sciences. 1978. Analytical Methods of Soil Physics and Chemistry. Shanghai: Shanghai Scientific and Technical Publishers.

    Google Scholar 

  • Institute of Soil Science, Chinese Academy of Sciences. 2001. Chinese Soil Taxonomy. Beijing: Science Press.

    Google Scholar 

  • Jonard M, Augusto L, Morel C, Achat DL, Saur E. 2009. Forest floor contribution to phosphorus nutrition: experimental data. Ann Forest Sci 66:510.

    Google Scholar 

  • Kochian LV. 2012. Plant nutrition: rooting for more phosphorus. Nature 488:466–7.

    CAS  PubMed  Google Scholar 

  • Lang F, Bauhus J, Frossard E, George E, Kaiser K, Kaupenjohann M, Krüger J, Matzner E, Polle A, Prietzel J et al. 2016. Phosphorus in forest ecosystems: new insights from an ecosystem nutrition perspective. J Plant Nutr Soil Sci 179:129–35.

    CAS  Google Scholar 

  • Latati M, Blavet D, Alkama N, Laoufi H, Drevon JJ, Gérard F, Ounane SM. 2016. The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 385:181–91.

    Google Scholar 

  • Li S, Su J, Liu W, Lang X, Huang X, Jia C, Zhang Z, Tong Q. 2015. Changes in biomass carbon and soil organic carbon stocks following the conversion from a secondary coniferous forest to a pine plantation. PLoS ONE 10:e0135946.

    PubMed  PubMed Central  Google Scholar 

  • Lodhiyal N, Lodhiyal LS. 2003. Biomass and net primary productivity of Bhabar Shisham forests in central Himalaya, India. Forest Ecol Manage 176:217–35.

    Google Scholar 

  • Lovett GM, Goodale CL, Ollinger SV, Fuss CB, Ouimette AP, Likens GE. 2018. Nutrient retention during ecosystem succession: a revised conceptual model. Front Ecol Environ 16:1–7.

    Google Scholar 

  • Ma X, Heal KV, Liu A, Jarvis PG. 2007. Nutrient cycling and distribution in different-aged plantations of Chinese fir in southern China. Forest Ecol Manage 243:61–74.

    Google Scholar 

  • Maranguit D, Guillaume T, Kuzyakov Y. 2017. Land-use change affects phosphorus fractions in highly weathered tropical soils. Catena 149:385–93.

    CAS  Google Scholar 

  • Odum EP. 1969. The strategy of ecosystem development. Science 164:262–70.

    CAS  PubMed  Google Scholar 

  • Oelmann Y, Richter AK, Roscher C, Rosenkranz S, Temperton VM, Weisser WW, Wilcke W. 2011. Does plant diversity influence phosphorus cycling in experimental grasslands? Geoderma 167–168:178–87.

    Google Scholar 

  • Osman KT. 2013. Nutrient Dynamics in Forest Soil. Forest Soils: Springer International Publishing.

    Google Scholar 

  • Pan F, Liang Y, Zhang W, Zhao J, Wang K. 2016. Enhanced nitrogen availability in karst ecosystems by oxalic acid release in the rhizosphere. Front Plant Sci 7:678.

    Google Scholar 

  • Pausch J, Kuzyakov Y. 2018. Carbon input by roots into the soil: quantification of rhizodeposition from root to ecosystem scales. Global Change Biol 24:1–12.

    Google Scholar 

  • R Core Team. 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

  • Ranger J, Allie S, Gelhaye D, Pollier B, Turpault MP, Granier A. 2002. Nutrient budgets for a rotation of a douglas-fir plantation in the beaujolais (France) based on a chronosequence study. Forest Ecol Manage 171:3–16.

    Google Scholar 

  • Sharma G, Sharma R, Sharma E. 2009. Impact of stand age on soil C, N and P dynamics in a 40-year chronosequence of alder-cardamom agroforestry stands of the Sikkim Himalaya. Pedobiologia 52:401–14.

    CAS  Google Scholar 

  • Shimizu A, Kato K, Komatsu A, Motomura K, Ikehashi H. 2008. Genetic analysis of root elongation induced by phosphorus deficiency in rice (Oryza sativa L.): Fine QTL mapping and multivariate analysis of related traits. Theor Appl Genet 117:987–96.

    CAS  PubMed  Google Scholar 

  • Spohn M, Kuzyakov Y. 2013. Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation—coupling soil zymography with 14C imaging. Soil Biol Biochem 67:106–13.

    CAS  Google Scholar 

  • State Forestry Administration of China. 2013. Forestry resource statistics for China in 2009–2013. Beijing: Chinese Forestry Press. (in Chinese)

    Google Scholar 

  • Tarafdar JC, Claassen N. 1988. Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol Fert Soils 5:308–12.

    CAS  Google Scholar 

  • Traina SJ, Sposito G, Bradford GR, Kafkafi U. 1987. Kinetic study of citrate effects on orthophosphate solubility in an acidic, montmorillonitic soil. Soil Sci Soc Am J 51:1483–7.

    CAS  Google Scholar 

  • Turner J, Lambert M. 2008. Nutrient cycling in age sequences of two Eucalyptus plantation species. Forest Ecol Manage 255:1701–12.

    Google Scholar 

  • Turner J, Lambert MJ. 2002. Litterfall and forest floor dynamics in Eucalyptus pilularis forests. Austral Ecol 27:192–9.

    Google Scholar 

  • Walker LR, del Moral R. 2003. Primary succession and ecosystem rehabilitation. Cambridge: Cambridge University Press.

    Google Scholar 

  • Walker LR, Wardle DA, Bardgett RD, Clarkson BD. 2010. The use of chronosequences in studies of ecological succession and soil development. J Ecol 98:725–36.

    Google Scholar 

  • Wang JR, Zhong AL, Simard SW, Kimmins JP. 1996. Aboveground biomass and nutrient accumulation in an age sequence of paper birch (Betula papyrifera) in the Interior Cedar Hemlock zone, British Columbia. Forest Ecol Manage 83:27–38.

    Google Scholar 

  • Wu HL, Xiang WH, Ouyang S, Forrester DI, Zhou B, Chen LX, Ge TD, Lei PF, Chen L, Zeng YL et al. 2019. Linkage between tree species richness and soil microbial diversity improves phosphorus bioavailability. Funct Ecol 33:1549–60.

    Google Scholar 

  • Xiang WH, Chai HX, Tian DL, Peng CH. 2009. Marginal effects of silvicultural treatments on soil nutrients following harvest in a Chinese fir plantation. Soil Sci Plant Nutr 55:523–31.

    CAS  Google Scholar 

  • Yang JL, Zhang GL, Huang LM. 2013. Rock weathering and soil formation rates of a forested watershed in the typical subtropical granite area. Acta Pedologica Sinica 2:253–9 (in Chinese).

    Google Scholar 

  • Zhang K, Cheng X, Dang H, Ye C, Zhang Y, Zhang Q. 2013. Linking litter production, quality and decomposition to vegetation succession following agricultural abandonment. Soil Biol Biochem 57:803–13.

    CAS  Google Scholar 

  • Zou X, Wei D, Wu P, Zhang Y, Hu Y, Chen S, Ma XQ. 2018. Strategies of organic acid production and exudation in response to low-phosphorus stress in Chinese fir genotypes differing in phosphorus-use efficiencies. Trees 32:897–912.

    CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Key Research and Development Program of China (2016YFD0600202) and the Huitong Forest Ecological Station funded by the State Forestry Administration of China. We thank the postgraduates for their assistance in field sampling: Lingxiu Chen, Wenbo Zhou, Linying Jiang, Chuantao Yang, Chuanhong Xu, Yuyu You, and Jiani Ma. Thanks also go to the staff from the Institute of Subtropical Agriculture, Chinese Academy of Sciences, Changsha, Hunan Province, for their experimental support. Special thanks to the Ministry of Education providing Yakov Kuzyakov the Chanjiang Professorship Award. We would like to thank Prof. Simon Queenborough at the Yale University for his assistance with English language editing of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Life Science and Technology, Central South University of Forestry and Technology, Changsha, 410004, Hunan Province, China

    Huili Wu, Wenhua Xiang, Liang Chen, Shuai Ouyang, Pifeng Lei, Yelin Zeng, Xiangwen Deng & Yakov Kuzyakov

  2. Huitong National Station for Scientific Observation and Research of Chinese Fir Plantation Ecosystem in Hunan Province, Huitong, 438107, China

    Huili Wu, Wenhua Xiang, Liang Chen, Shuai Ouyang, Pifeng Lei, Yelin Zeng, Xiangwen Deng & Yakov Kuzyakov

  3. Key Laboratory of Forest Ecology and Environment, State Forestry Administration, Research Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing, 100091, China

    Wenfa Xiao & Lixiong Zeng

  4. Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing, 100101, China

    Shenggong Li

  5. Swiss Federal Institute of Forest, Snow and Landscape Research WSL, Zürcherstrasse 111, 8903, Birmensdorf, Switzerland

    David I. Forrester

  6. Department of Soil Science of Temperate Ecosystems and Agricultural Soil Science, University of Goettingen, 37077, Göttingen, Germany

    Yakov Kuzyakov

Authors
  1. Huili Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenhua Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shuai Ouyang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenfa Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shenggong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. David I. Forrester
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Pifeng Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yelin Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiangwen Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lixiong Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yakov Kuzyakov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenhua Xiang.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 795 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wu, H., Xiang, W., Chen, L. et al. Soil Phosphorus Bioavailability and Recycling Increased with Stand Age in Chinese Fir Plantations. Ecosystems 23, 973–988 (2020). https://doi.org/10.1007/s10021-019-00450-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-019-00450-1

Keywords

Search

Navigation