Plant and Soil

, Volume 394, Issue 1–2, pp 315–327 | Cite as

Differential responses of needle and branch order-based root decay to nitrogen addition: dominant effects of acid-unhydrolyzable residue and microbial enzymes

  • Liang Kou
  • Weiwei Chen
  • Xinyu Zhang
  • Wenlong Gao
  • Hao Yang
  • Dandan Li
  • Shenggong Li
Regular Article


Background and aims

Both chemical differences between foliage and different orders of fine roots and their contrasting decomposing microenvironments may affect their decomposition. However, little is known about how foliage and branch order-based root decomposition responds to increased N availability and the response mechanisms behind.


The effects of different doses of N addition on the decomposition of needles and order-based roots of Pinus elliottii (slash pine) were monitored using the litterbag method for 524 days in a subtropical slash pine plantation in south China. The acid-unhydrolyzable residue (AUR) concentration and microbial extracellular enzymatic activities (EEA) in decomposing needles and roots were also determined.


Our results indicate that the responses of needle and order-based root decomposition were N-dose-specific. The decomposition of both needles and lower-order roots was inhibited under the high N dose rate. The retarded decomposition of lower-order roots could be explained more by the increased binding of AUR to inorganic N ions, while the retarded decomposition of needles could be explained more by the reduced microbial EEA. Further, in contrast to lower-order roots, N addition had no effect on the decomposition of higher-order roots.


We conclude that the decomposition of foliage and fine roots may fail to mirror each other at ambient conditions or in response to N deposition due to their contrasting decomposition microenvironments and tissue chemistry. Given the differential effects of N addition on order-based roots, our findings highlight the need to consider the tissue chemistry heterogeneity within branching fine root systems when predicting the responses of root decomposition to N loading.


Decomposition Fine root Foliage Microorganism Nitrogen deposition 



This research is financially supported by the grants from the National Natural Science Foundation of China (No. 31130009) and the National Key Project of Scientific and Technical Supporting Program (No. 2013BAC03B03). The authors acknowledge the contributions of the anonymous reviewers.

Compliance with ethical standards

The authors declare no conflict of interest. All authors have been personally and actively involved in this work and have consented to this submission.


  1. Aber JD, Melillo JM, McClaugherty CA (1990) Predicting long-term patterns of mass loss, nitrogen dynamics, and soil organic matter formation from initial fine litter chemistry in temperate forest ecosystems. Can J Bot 68:2201–2208CrossRefGoogle Scholar
  2. Aber JD, Nadelhoffer KJ, Steudler P, Melillo JM (1989) Nitrogen saturation in northern forest ecosystems. Bioscience 39:378–386CrossRefGoogle Scholar
  3. Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449CrossRefGoogle Scholar
  4. Ågren GI, Bosatta E, Magill AH (2001) Combining theory and experiment to understand effects of inorganic nitrogen on litter decomposition. Oecologia 128:464–464CrossRefPubMedGoogle Scholar
  5. Axelsson G, Berg B (1988) Fixation of ammonia (15N) to Pinus silvestris needle litter in different stages of decomposition. Scand J For Res 3:273–279CrossRefGoogle Scholar
  6. Berg B, Liu CJ, Laskowski R, Davey M (2013) Relationships between nitrogen, acid-unhydrolyzable residue, and climate among tree foliar litters. Can J For Res 43:103–107CrossRefGoogle Scholar
  7. 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
  8. Berg B, McClaugherty C (2014) Plant litter-decomposition, humus formation, carbon sequestration, 3rd edn. Springer, BerlinGoogle Scholar
  9. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  10. Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365CrossRefGoogle Scholar
  11. Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  12. Conn CE, Day FP (1996) Response of root and cotton strip decay to nitrogen amendment along a barrier island dune chronosequence. Can J Bot 74:276–284CrossRefGoogle Scholar
  13. Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113CrossRefPubMedGoogle Scholar
  14. Crow SE, Lajtha K, Filley TR, Swanston CW, Bowden RD, Caldwell BA (2009) Sources of plant-derived carbon and stability of organic matter in soil: implications for global change. Glob Chang Biol 15:2003–2019CrossRefGoogle Scholar
  15. Dijkstra FA, Hobbie SE, Knops JMH, Reich PB (2004) Nitrogen deposition and plant species interact to influence soil carbon stabilization. Ecol Lett 7:1192–1198CrossRefGoogle Scholar
  16. Fan PP, Guo DL (2010) Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil. Oecologia 163:509–515CrossRefPubMedGoogle Scholar
  17. Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63:433–462CrossRefGoogle Scholar
  18. 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, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  19. 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 81:89–102CrossRefGoogle Scholar
  20. Guo CJ, Dannenmann M, Gasche R, Zeller B, Papen H, Polle A, Rennenberg H, Simon J (2013) Preferential use of root litter compared to leaf litter by beech seedlings and soil microorganisms. Plant Soil 368:519–534CrossRefGoogle Scholar
  21. Guo DL, Xia 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 180:673–683CrossRefPubMedGoogle Scholar
  22. Hessen DO, Ågren GI, Anderson TR, Elser JJ, De Ruiter PC (2004) Carbon, sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192CrossRefGoogle Scholar
  23. Hobbie SE (2008) Nitrogen effects on decomposition: a five-year experiment in eight temperate sites. Ecology 89:2633–2644CrossRefPubMedGoogle Scholar
  24. Hobbie SE, Eddy WC, Buyarski CR, Adair EC, Ogdahl ML, Weisenhorn P (2012) Response of decomposing litter and its microbial community to multiple forms of nitrogen enrichment. Ecol Monogr 82:389–405CrossRefGoogle Scholar
  25. Hobbie SE, Oleksyn J, Eissenstat DM, Reich PB (2010) Fine root decomposition rates do not mirror those of leaf litter among temperate tree species. Oecologia 162:505–513CrossRefPubMedGoogle Scholar
  26. Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12:1–15CrossRefGoogle Scholar
  27. Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257CrossRefGoogle Scholar
  28. Mao R, Zeng DH, Li LJ (2011) Fresh root decomposition pattern of two contrasting tree species from temperate agroforestry systems: effects of root diameter and nitrogen enrichment of soil. Plant Soil 347:115–123CrossRefGoogle Scholar
  29. Matson PA, McDowell WH, Townsend AR, Vitousek PM (1999) The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46:67–83Google Scholar
  30. Matulich KL, Martiny JB (2014) Microbial composition alters the response of litter decomposition to environmental change. Ecology 96:154–163CrossRefGoogle Scholar
  31. Moorhead DL, Sinsabaugh RL (2006) A theoretical model of litter decay and microbial interaction. Ecol Monogr 76:151–174CrossRefGoogle Scholar
  32. Norris MD, Avis PG, Reich PB, Hobbie SE (2013) Positive feedbacks between decomposition and soil nitrogen availability along fertility gradients. Plant Soil 367:347–361CrossRefGoogle Scholar
  33. Olson JS (1963) Energy storage and the balance of producers and decomposers in ecological systems. Ecology 44:322–331CrossRefGoogle Scholar
  34. Ostertag R, Hobbie SE (1999) Early stages of root and leaf decomposition in Hawaiian forests: effects of nutrient availability. Oecologia 121:564–573CrossRefGoogle Scholar
  35. Perakis SS, Matkins JJ, Hibbs DE (2012) Interactions of tissue and fertilizer nitrogen on decomposition dynamics of lignin-rich conifer litter. Ecosphere 3Google Scholar
  36. Pietsch KA, Ogle K, Cornelissen JHC, Cornwell WK, Bönisch G, Craine JM, Jackson BG, Kattge J, Peltzer DA, Penuelas J, Reich PB, Wardle DA, Weedon JT, Wright IJ, Zanne AE, Wirth C (2014) Global relationship of wood and leaf litter decomposability: the role of functional traits within and across plant organs. Glob Ecol Biogeogr 23:1046–1057CrossRefGoogle Scholar
  37. 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
  38. Preston CM, Nault JR, Trofymow JA (2009) Chemical changes during 6 years of decomposition of 11 litters in some canadian forest sites. Part 2. 13C abundance, solid-state 13C NMR spectroscopy and the meaning of “lignin. Ecosystems 12:1078–1102CrossRefGoogle Scholar
  39. Rasse DP, Rumpel C, Dignac MF (2005) Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–356CrossRefGoogle Scholar
  40. Ryan MG, Melillo JM, Ricca A (1990) A comparison of methods for determining proximate carbon fractions of forest litter. Can J For Res 20:166–171CrossRefGoogle Scholar
  41. Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315CrossRefGoogle Scholar
  42. Sanaullah M, Chabbi A, Leifeld J, Bardoux G, Billou D, Rumpel C (2011) Decomposition and stabilization of root litter in top- and subsoil horizons: what is the difference? Plant Soil 338:127–141CrossRefGoogle Scholar
  43. Silver WL, Miya RK (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419CrossRefGoogle Scholar
  44. Solly EF, Schöning I, Boch S, Kandeler E, Marhan S, Michalzik B, Müller J, Zscheischler J, Trumbore SE, Schrumpf M (2014) Factors controlling decomposition rates of fine root litter in temperate forests and grasslands. Plant Soil 382:203–218CrossRefGoogle Scholar
  45. Strickland MS, Lauber C, Fierer N, Bradford MA (2009) Testing the functional significance of microbial community composition. Ecology 90:441–451CrossRefPubMedGoogle Scholar
  46. Sun Y, Gu JC, Zhuang HF, Guo DL, Wang ZQ (2011) Lower order roots more palatable to herbivores: a case study with two temperate tree species. Plant Soil 347:351–361CrossRefGoogle Scholar
  47. Wallenstein MD, Hall EK (2012) A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning. Biogeochemistry 109:35–47CrossRefGoogle Scholar
  48. Wang YD, Wang ZL, Wang HM, Guo CC, Bao WK (2012) Rainfall pulse primarily drives litterfall respiration and its contribution to soil respiration in a young exotic pine plantation in subtropical China. Can J For Res 42:657–666CrossRefGoogle Scholar
  49. Wen XF, Wang HM, Wang JL, Yu GR, Sun XM (2010) Ecosystem carbon exchanges of a subtropical evergreen coniferous plantation subjected to seasonal drought, 2003–2007. Biogeosciences 7:357–369CrossRefGoogle Scholar
  50. 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
  51. Zhan XY, Yu GR, He NP, Fang HJ, Jia BR, Zhou M, Wang CK, Zhang JH, Zhao GD, Wang SL, Liu YF, Yan JH (2014) Nitrogen deposition and its spatial pattern in main forest ecosystems along north–south transect of eastern China. Chinese Geogr Sci 24:137–146CrossRefGoogle Scholar
  52. Zhang JB, Cai ZC, Zhu TB, Yang WY, Müller C (2013) Mechanisms for the retention of inorganic N in acidic forest soils of southern China. Sci Rep-Uk 3Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Liang Kou
    • 1
    • 2
  • Weiwei Chen
    • 1
    • 2
  • Xinyu Zhang
    • 1
  • Wenlong Gao
    • 1
    • 2
  • Hao Yang
    • 1
  • Dandan Li
    • 1
    • 3
  • Shenggong Li
    • 1
  1. 1.Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources ResearchChinese Academy of SciencesBeijingChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.College of Biological Science and TechnologyShenyang Agricultural UniversityShenyangChina

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