Advertisement

Exogenous and endogenous nitrogen differentially affect the decomposition of fine roots of different diameter classes of Mongolian pine in semi-arid northeast China

  • Qun Gang
  • Scott X. Chang
  • Guigang Lin
  • Qiong Zhao
  • Bing Mao
  • De-Hui Zeng
Regular Article
  • 124 Downloads

Abstract

Aims

Nitrogen (N) addition could affect litter decomposition through its direct effects on soil N availability and indirect effects on initial litter chemistry. The aim of this study was to evaluate the relative contribution of these direct and indirect effects to the decomposition of fine roots with different diameter classes.

Methods

A two-year reciprocal replant–transplant field experiment was conducted in a Mongolian pine (Pinus sylvestris var. mongolica) plantation to examine the relative effect of exogenous and endogenous N enrichment induced by N addition (10 g N m−2 yr.−1) on the decomposition of fine roots with different diameter classes: < 0.5 mm (small fine root, SFR) and 0.5–2 mm (large fine root, LFR).

Results

The LFR had significantly higher decomposition rates (k: 0.315–0.397 yr.−1) than the SFR (0.245–0.274 yr.−1) after 2 years of incubation. Exogenous N (i.e., increased soil N availability due to N addition) had no significant effect on the decomposition rates of fine roots, whereas endogenous N (i.e. increased N concentration in litter due to N addition) inhibited and accelerated the decomposition of SFR and LFR, respectively. Endogenous N decreased the net release of N but both endogenous and exogenous N increased the net release of phosphorus (P) from SFR. By contrast, exogenous and endogenous N decreased the net release of N and P from LFR.

Conclusions

Our results suggest that N addition affected fine root decomposition indirectly by changing the chemical traits of fine roots rather than directly through changing soil N availability. Elevated input and decreased net N release of fine roots might be a potential mechanism explaining the increases of total organic carbon and total N in the semi-arid forest soil under N addition. Our study also suggests that SFR may be a more important source of stable soil organic matter relative to LFR.

Keywords

Decomposition Nitrogen addition Fine root Root diameter class Pinus sylvestris var. mongolica 

Notes

Acknowledgments

This study was funded by the National Natural Science Foundation of China (31870603, 41877341). We thank Gui-Yan Ai for help with the laboratory work and the CAS Key Laboratory of Forest Ecology and Management for funding Qun Gang’s visit to Canada. We also thank three anonymous reviewers for their comments and suggestions that greatly improved an earlier version of the manuscript.

Supplementary material

11104_2018_3910_MOESM1_ESM.doc (712 kb)
ESM 1 (DOC 712 kb)

References

  1. Attiwill PM, Adams MA (1993) Nutrient cycling in forests. New Phytol 124:561–582CrossRefGoogle Scholar
  2. Berg B (1986) Nutrient release from litter and humans in coniferous forest soils: a mini review. Scand J For Res 1:359–369CrossRefGoogle Scholar
  3. Berg B, Matzner E (1997) Effect of N deposition on decomposition of plant litter and soil organic matter in forest systems. Environ Rev 5:1–25CrossRefGoogle Scholar
  4. Brooks ML (2003) Effects of increased soil nitrogen on the dominance of alien annual plants in the Mojave Desert. J Appl Ecol 40:344–353CrossRefGoogle Scholar
  5. Carreiro MM, Sinsabaugh RL, Report DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  6. Cleveland CC, Townsend AR (2006) Nutrient additions to tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci U S A 103:10316–10321CrossRefGoogle Scholar
  7. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995CrossRefGoogle Scholar
  8. Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE, Hauglustaine D, Heinze C, Holland E, Jacob D, Lohmann U, Ramachandran S, da Silva Dias PL, Wofsy SC, Zhang XY (2007) Couplings between changes in the climate system and biogeochemistry. Cambridge University Press, pp 499–587Google Scholar
  9. Dornbush ME, Isenhart TM, Raich JW (2002) Quantifying fine-root decomposition: an alternative to buried litterbags. Ecology 83:2985–2990CrossRefGoogle Scholar
  10. Eissenstat DM, Volder A (2005) The efficiency of nutrient acquisition over the life of a root. Nutrient acquisition by plants: an ecological perspective. Ecol Stud 181:185–220CrossRefGoogle Scholar
  11. Fan PP, Guo DL (2010) Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil. Oecologia 163:509–515CrossRefGoogle Scholar
  12. Fang H, Mo J, Peng S, Li Z, Wang H (2007) Cumulative effects of nitrogen additions on litter decomposition in three tropical forests in southern China. Plant Soil 297:233–242CrossRefGoogle Scholar
  13. Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462CrossRefGoogle Scholar
  14. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vorosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  15. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892CrossRefGoogle Scholar
  16. Goebel M, Hobbie SE, Bulaj B, Zadworny M, Archibald DD, Oleksyn J, Reich PB, Eissenstat DM (2011) Decomposition of the finest root branching orders: linking belowground dynamics to fine-root function and structure. Ecol Monogr 81(1):89–102CrossRefGoogle Scholar
  17. Guo DL, Xiao MX, Wei X, Chang WJ, Liu Y, Wang ZQ (2008) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683CrossRefGoogle Scholar
  18. Haddix M, Paul E, Cotrofo MF (2016) Dual, differential isotope labeling shows the preferential movement of labile plant constituents into mineral-bonded soil organic matter. Glob Chang Biol 22:2301–2312CrossRefGoogle Scholar
  19. Hättenschwiler S, Coq S, Barantal S, Handa IT (2011) Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytol 189:950–965CrossRefGoogle Scholar
  20. Hobbie SE (2008) Nitrogen effects on litter decomposition: a five-year experiment in eight temperate grassland and forest sites. Ecology 89:2633–2644CrossRefGoogle Scholar
  21. Hobbie SE, Horton TR (2007) Evidence that saprotrophic fungi mobilise carbon and mycorrhizal fungi mobilise nitrogen during litter decomposition. New Phytol 173:447–449CrossRefGoogle Scholar
  22. Huang JP, Yu HP, Guan XD, Wang GY, Guo RX (2015) Accelerated dryland expansion under climate change. Nat Clim Chang 6:166–172CrossRefGoogle Scholar
  23. Iiyama K, Wallis AFA (1990) Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:145–161CrossRefGoogle Scholar
  24. Janusz G, Kucharzyk KH, Pawlik A, Staszczak M, Paszczynskic AJ (2013) Fungal laccase, manganese peroxidase and lignin peroxidase: gene expression and regulation. Enzym Microb Technol 52:1–12CrossRefGoogle Scholar
  25. King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398CrossRefGoogle Scholar
  26. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257CrossRefGoogle Scholar
  27. Kozovits AR, Bustamante MMC, Garofalo CR, Bucci S, Franco AC, Goldstein G, Meinzer FC (2007) Nutrient resorption and patterns of litter production and decomposition in a Neotropical savanna. Funct Ecol 21:1034–1043CrossRefGoogle Scholar
  28. Kramer C, Trumbores S, Froberg M, Cisneros Dozal LM, Zhang D, Xu X, Santos GM, Hanson PJ (2010) Recent (<4 year old) leaf litter is not a major source of microbial carbon in a temperate forest mineral soil. Soil Biol Biochem 42:1028–1037CrossRefGoogle Scholar
  29. Li A, Fahey TJ, Pawlowska TE, Fisk MC, Burtis J (2015) Fine root decomposition, nutrient mobilization and fungal communities in a pine forest ecosystem. Soil Biol Biochem 83:76–83CrossRefGoogle Scholar
  30. Lin GG, Zeng DH (2017) Heterogeneity in decomposition rates and annual litter inputs within fine-root architecture of tree species: implications for forest soil carbon accumulation. For Ecol Manag 389:386–394CrossRefGoogle Scholar
  31. Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL, Cui ZL, Vitousek P, Erisman JW, Goulding K, Christie P, Fangmeier A, Zhang FS (2013) Enhanced nitrogen deposition over China. Nature 494:459–462CrossRefGoogle Scholar
  32. Magill AH, Aber JD (1998) Long-term effects of experimental nitrogen additons on foliar litter decay and humans formation in forest ecosystems. Plant Soil 203:301–311CrossRefGoogle Scholar
  33. Mao B, Mao R, Hu YL, Huang Y, Zeng DH (2016) Decomposition of Mongolian pine litter in the presence of understory species in semi-arid Northeast China. J For Res 27:329–337CrossRefGoogle Scholar
  34. McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo DL, Helmisaari H-S, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518CrossRefGoogle Scholar
  35. Micks P, Aber JD, Boone RD, Davidson EA (2004) Short-term soil respiration and nitrogen immobilization response to nitrogen applications in control and nitrogen-enriched temperate forests. For Ecol Manag 196:57–70CrossRefGoogle Scholar
  36. Morrison IM (1972a) A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops. J Sci Food Agric 23:455–463CrossRefGoogle Scholar
  37. Morrison IM (1972b) Improvements in the acetyl bromide technique to determine lignin and digestibility and its application to legumes. J Sci Food Agric 23:1463–1469CrossRefGoogle Scholar
  38. Nadelhoffer KJ, Raich JW (1992) Fine root production estimates and belowground carbon allocation in forest ecosystems. Ecology 73:1139–1147CrossRefGoogle Scholar
  39. Nelson DW, Sommers LE (1996) Total carbon, organic carbon and organic matter. Part 3: chemical methods. Wisconsin: Soil Science Society of America and American Society of Agronomy, pp 961–1010Google Scholar
  40. Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44(2):322–331CrossRefGoogle Scholar
  41. Ostonen I, Lõhmus K, Pajuste K (2005) Fine root biomass, production and its proportion of NPP in a fertile middle-aged Norway spruce forest: comparison of soil core and ingrowth core methods. For Ecol Manag 212:264–277CrossRefGoogle Scholar
  42. Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Carol Adair E, Brandt LA, Hart SC, Fasth B (2007) Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315:361–364CrossRefGoogle Scholar
  43. Powers JS, Treseder KK, Lerdau MT (2005) Fine roots, arbuscular mycorrhizal hyphae and soil nutrients in four neotropical rain forests: patterns across large geographic distances. New Phytol 165:913–921CrossRefGoogle Scholar
  44. Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine north American trees. Ecol Monogr 72:293–309CrossRefGoogle Scholar
  45. Prescott CE (2010) Litter decomposition: what controls it and how can we alter it to sequester more carbon in forest soils? Biogeochemistry 101:133–149CrossRefGoogle Scholar
  46. Resendes ML, Bryla DR, Eissenstat DM (2008) Early events in the life of apple roots: variation in root growth rate is linked to mycorrhizal and nonmycorrhizal fungal colonization. Plant Soil 313:175–186CrossRefGoogle Scholar
  47. Silver WL, Miya RKS (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419CrossRefGoogle Scholar
  48. Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404CrossRefGoogle Scholar
  49. Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215CrossRefGoogle Scholar
  50. Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264CrossRefGoogle Scholar
  51. Sun T, Mao Z, Han Y (2013) Slow decomposition of very fine roots and some factors controlling the process: a 4-year experiment in four temperate tree species. Plant Soil 372:445–458CrossRefGoogle Scholar
  52. Sun T, Dong LL, Wang ZW, Lü XT, Mao ZJ (2016) Effects of long-term nitrogen deposition on fine root decomposition and its extracellular enzyme activities in temperature forests. Soil Biol Biochem 93:50–59CrossRefGoogle Scholar
  53. Tamura M, Tharayil N (2014) Plant litter chemistry and microbial priming regulate the accrual, composition and stability of soil carbon in invaded ecosystem. New Phytol 203:110–124CrossRefGoogle Scholar
  54. Tu LH, Hu HL, Chen G, Peng Y, Xiao YL, Hu TX, Zhang J, Li XW, Liu L, Tang Y (2014) Nitrogen addition significantly affects forest litter decomposition under high levels of ambient nitrogen deposition. PLoS One 9:e88752CrossRefGoogle Scholar
  55. Tu LH, Peng Y, Chen G, Hu HL, Xiao YL, Hu TX, Liu L, Yi T (2015) Direct and indirect effects of nitrogen additions on fine root decomposition in a subtropical bamboo forest. Plant Soil 389:273–288CrossRefGoogle Scholar
  56. Van Groenigen KJ, Six J, Hungate BA, de Graadd MA, van Breemen N, van Kessel C (2006) Element interactions limit soil carbon storage. Proc Natl Acad Sci U S A 103:6571–6574CrossRefGoogle Scholar
  57. Waldrop MP, Zak DR, Sinsabaugh RL, Gallo M, Lauber C (2004) Nitrogen deposition modifies soil carbon storage through changes in microbial enzymatic activity. Ecol Appl 14:1172–1177CrossRefGoogle Scholar
  58. Xia MX, Tdhelm AF, Pregitzer KS (2018) Long-term simulated atmospheric nitrogen deposition alters leaf and fine root decomposition. Ecosystems 21:1–14CrossRefGoogle Scholar
  59. Xiong YM, Fan PP, Fu SL, Zeng H, Guo DL (2013) Slow decomposition and limited nitrogen release by lower order roots in eight Chinese temperate and subtropical trees. Plant Soil 363:19–31CrossRefGoogle Scholar
  60. Yang YS, Chen GS, Guo JF, Lin P (2004) Decomposition dynamic of fine roots in a mixed forest of Cunninghamia lanceolata and Tsoongiodendron odorum in mid-subtropics. Ann For Sci 61:65–72CrossRefGoogle Scholar
  61. Zak DR, Holmes WE, Burton AJ, Pregitzer KS, Talhelm AF (2008) Simulated atmospheric NO3 deposition increases soil organic matter by slowing decomposition. Ecol Appl 18:2016–2027CrossRefGoogle Scholar
  62. Zeng DH, Hu YL, Chang SX, Fan ZP (2009) Land cover change effects on soil chemical and biological properties after planting Mongolian pine (Pinus sylvestris var. mongolica) in sandy lands in Keerqin, Northeast China. Plant Soil 317:121–133CrossRefGoogle Scholar
  63. Zhang DQ, Hui DF, Luo YQ, Zhou GY (2008) Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93CrossRefGoogle Scholar
  64. Zheng LL, Zhao Q, Yu ZY, Zhao SY, Zeng DH (2017a) Altered leaf functional traits by nitrogen addition in a nutrient-poor pine plantation: a consequence of decreased phosphorus availability. Sci Rep 7:7415CrossRefGoogle Scholar
  65. Zheng ZM, Mamuti M, Liu HM, Shu YQ, Hu SJ, Wang XH, Li BB, Lin L, Li X (2017b) Effects of nutrient additions on litter decomposition regulated by phosphorus-induced changes in litter chemistry in a subtropical forest, China. For Ecol Manag 400:123–128CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Qun Gang
    • 1
    • 2
    • 3
  • Scott X. Chang
    • 3
  • Guigang Lin
    • 1
  • Qiong Zhao
    • 1
  • Bing Mao
    • 1
  • De-Hui Zeng
    • 1
  1. 1.CAS Key Laboratory of Forest Ecology and Management/Daqinggou Ecological Station, Institute of Applied EcologyChinese Academy of SciencesShenyangChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada

Personalised recommendations