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Leaf litter of a dominant cushion plant shifts nitrogen mineralization to immobilization at high but not low temperature in an alpine meadow

Abstract

Aims

We evaluated the effects of temperature and addition of leaf litter of Androsace tapete MaximWe–a dominant cushion plant species of alpine meadows on the Tibetan Plateau–on carbon (C) and nitrogen (N) mineralization, microbial biomass C (MBC) and N (MBN).

Methods

A laboratory incubation experiment with and without cushion plant litter addition was conducted for 112 days at three temperature regimes (−1, 5 and 11 °C). C and net N mineralization were simultaneously measured during the incubation period.

Results

C and N mineralization were affected by interactions between litter addition and temperature. Litter addition increased C mineralization and MBN but shifted N mineralization to immobilization at higher temperature. The positive relationship between net N mineralization and MBC and MBN was shifted to a negative one through cushion plant litter addition. Cushion plant litter also changed the relationship between C mineralization and net N mineralization from insignificantly positive to significantly negative.

Conclusions

These findings indicate that low temperature in winter could be important for alpine plants because low temperature can increase net N mineralization and supply plants with available N for their growth in the early growing season. During the growing season, climate warming–either directly through a temperature effect or indirectly through triggering increased cushion plant litter production–might lead to stronger competition for N between alpine plants and microorganisms.

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References

  • Arroyo MTK, Cavieres LA, Penaloza A, Arroyo-Kalin MA (2003) Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecol 169:121–129

    Article  Google Scholar 

  • Aubert S, Boucher F, Lavergne S, Renaud J, Choler P (2014) 1914–2014: A revised worldwide catalogue of cushion plants 100 years after Hauri and Schröter. Alp Botany 124:59–70

    Article  Google Scholar 

  • Badano EI, Jones CG, Cavieres LA, Wright JP (2006) Assessing impacts of ecosystem engineers on community organization: a general approach illustrated by effects of a high-Andean cushion plant. Oikos 115:369–385

    Article  Google Scholar 

  • Bai JB, Xu XL, Fu G, Song MH, He YT, Jiang J (2011a) Effects of temperature and nitrogen input on nitrogen mineralization in alpine soils on Tibetan Plateau. Agri Sci Tech 12:1909–1912

    CAS  Google Scholar 

  • Bai JB, Xu XL, Song MH, He YT, Jiang J, Shi PL (2011b) Effects of temperature and added nitrogen on carbon mineralization in alpine soils on the Tibetan Plateau. Ecol Environ Sci 20:855–859

    Google Scholar 

  • Barrett JE, Burke IC (2000) Potential nitrogen immobilization in grassland soils across a soil organic matter gradient. Soil Biol Biochem 32:1707–1716

    Article  CAS  Google Scholar 

  • Berg B, McClaugherty CA (eds) (2003) Plant Litter: Decomposition, Humus Formation, Carbon Sequestration. Springer, Berlin

    Google Scholar 

  • Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529

    Article  Google Scholar 

  • Blagodatskaya E, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fert Soils 45:115–131

    Article  Google Scholar 

  • Bowman WD, Steltzer H, Rosenstiel TN, Cleveland CC, Meier CL (2004) Litter effects of two co-occurring alpine species on plant growth, microbial activity and immobilization of nitrogen. Oikos 104:336–344

    Article  Google Scholar 

  • Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil-nitrogen - a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842

    Article  CAS  Google Scholar 

  • Buckeridge KM, Zufelt E, Chu HY, Grogan P (2010) Soil nitrogen cycling rates in low arctic shrub tundra are enhanced by litter feedbacks. Plant Soil 330:407–421

    Article  CAS  Google Scholar 

  • Butterfield BJ, Cavieres LA, Callaway RM, Cook BJ, Kikvidze Z, Lortie CJ, Michalet R, Pugnaire FI, Schob C, Xiao S, Zaitchek B, Anthelme F, Bjork RG, Dickinson K, Gavilan R, Kanka R, Maalouf J-P, Noroozi J, Parajuli R, Phoenix GK, Reid A, Ridenour W, Rixen C, Wipf S, Zhao L, Brooker RW (2013) Alpine cushion plants inhibit the loss of phylogenetic diversity in severe environments. Ecol Lett 16:478–486

    PubMed  Article  CAS  Google Scholar 

  • Casanova-Katny MA, Torres-Mellado GA, Palfner G, Cavieres LA (2011) The best for the guest: high Andean nurse cushions of Azorella madreporica enhance arbuscular mycorrhizal status in associated plant species. Mycorrhiza 21:613–622

    PubMed  Article  Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Gomez-Gonzalez S, Molina-Montenegro MA (2006) Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytol 169:59–69

    PubMed  Article  Google Scholar 

  • Cavieres LA, Badano EI, Sierra-Almeida A, Molina-Montenegro MA (2007) Microclimatic modifications of cushion plants and their consequences for seedling survival of native and non-native herbaceous species in the high Andes of Central Chile. Arct Anarct Alp Res 39:229–236

    Article  Google Scholar 

  • Chapman SK, Langley JA, Hart SC, Koch GW (2006) Plants actively control nitrogen cycling: uncorking the microbial bottleneck. New Phytol 169:27–34

    PubMed  Article  CAS  Google Scholar 

  • Craine JM, Morrow C, Fierer N (2007) Microbial nitrogen limitation increases decomposition. Ecology 88:2105–2113

    PubMed  Article  Google Scholar 

  • Fierer N. Colman BP. Schimel JP. Jackson RB (2006) Predicting the temperature dependence of microbial respiration in soil: A continental-scale analysis. Global Biogeochem Cy 20:Gb3026

  • Fierer N, Craine JM, McLauchlan K, Schimel JP (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326

    Article  Google Scholar 

  • Gao YX (ed) (1984) Xi Zang Climate. Science Press, Beijing, In Chinese

    Google Scholar 

  • Geng Y, Tang S, Tashi T, Song Z, Zhang G, Zeng L, Zhao J, Wang L, Shi J, Chen J, Zhong Y (2009) Fine-and landscape-scale spatial genetic structure of cushion rockjasmine, Androsace tapete (Primulaceae), across southern Qinghai-Tibetan Plateau. Genetica 135:419–427

    PubMed  Article  Google Scholar 

  • Giblin AE, Nadelhoffer KJ, Shaver GR, Laundre JA, Mckerrow AJ (1991) Biogeochemical diversity along a riverside toposequence in Arctic Alaska. Ecol Monogr 61:415–435

    Article  Google Scholar 

  • He YT. Kueffer C. Shi PL. Zhang XZ. Du MY. Yan W. Sun W (2014) Variation of biomass and morphology of the cushion plant Androsace tapete along an elevational gradient in the Tibetan Plateau. Plant Spec Biol. In Press

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecol Monogr 66:503–522

    Article  Google Scholar 

  • Hobbie SE, Chapin FS (1996) Winter regulation of tundra litter carbon and nitrogen dynamics. Biogeochemistry 35:327–338

    Article  Google Scholar 

  • Huang RF, Wang WY (1991) The flora and community succession of cushion plant in Qinghai-Xizang Plateau. Acta Biologica Plateau Sinica 10:15–26, In Chinese

    Google Scholar 

  • Jiang J, Li YK, Wang MZ, Zhou CP, Cao GM, Shi PL, Song MH (2013) Litter species traits, but not richness, contribute to carbon and nitrogen dynamics in an alpine meadow on the Tibetan Plateau. Plant Soil 373:931–941

    Article  CAS  Google Scholar 

  • Johnson LC, Shaver GR, Giblin AE, Nadelhoffer KJ, Rastetter ER, Laundre JA, Murray GL (1996) Effects of drainage and temperature on carbon balance of tussock tundra microcosms. Oecologia 108:737–748

    Article  Google Scholar 

  • Jonasson S, Havstrom M, Jensen M, Callaghan TV (1993) In-situ mineralization of nitrogen and phosphorus of Arctic soils after perturbations simulating climate-change. Oecologia 95:179–186

    Article  Google Scholar 

  • Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient, and light regimes in the Arctic. Ecology 80:1828–1843

    Article  Google Scholar 

  • Jonasson S, Castro J, Michelsen A (2004) Litter, warming and plants affect respiration and allocation of soil microbial and plant C, N and P in arctic mesocosms. Soil Biol Biochem 36:1129–1139

    Article  CAS  Google Scholar 

  • Jonasson S, Castro J, Michelsen A (2006) Interactions between plants, litter and microbes in cycling of nitrogen and phosphorus in the arctic. Soil Biol Biochem 38:526–532

    Article  CAS  Google Scholar 

  • Kalembas SJ, Jenkinson DS (1973) Comparative study of titrimetric and gravimetric methods for determination of organic carbon in soil. J Sci Food Agr 24:1085–1090

  • Kleier C, Rundel PW (2004) Microsite requirements, population structure and growth of the cushion plant Azorella compacta in the tropical Chilean Andes. Austral Ecol 29:461–470

    Article  Google Scholar 

  • Koch O. Tscherko D. Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochem Cy 21:Gb4017

  • Körner C (ed) (2003) Alpine plant life: functional plant ecology of high mountain ecosystems, 2nd edn. Springer, Berlin

    Google Scholar 

  • Li BS, Zhang JW, Wang JT, Chen WL (1985) The alpine cushion vegetation of Xizang. Acta Botanica Sinica 27:311–317, In Chinese

    Google Scholar 

  • Li BS, Wang JT, Li SY (1987) The floristic features and geographic distribution of the cushion plant in Xizang. Mountain Research 5:14–20, In Chinese

    Google Scholar 

  • Li RC, Luo TX, Tang YH, Du MY, Zhang XZ (2013) The altitudinal distribution center of a widespread cushion species is related to an optimum combination of temperature and precipitation in the central Tibetan Plateau. J Arid Environ 88:70–77

    Article  Google Scholar 

  • Lipson DA, Schmidt SK, Monson RK (2000) Carbon availability and temperature control the post-snowmelt decline in alpine soil microbial biomass. Soil Biol Biochem 32:441–448

    Article  CAS  Google Scholar 

  • Lipson DA, Schadt CW, Schmidt SK (2002) Changes in soil microbial community structure and function in an alpine dry meadow following spring snow melt. Microb Ecol 43:307–314

    PubMed  Article  CAS  Google Scholar 

  • Liu XD, Chen BD (2000) Climatic warming in the Tibetan Plateau during recent decades. Int J Climatol 20:1729–1742

    Article  Google Scholar 

  • Magid J, Henriksen O, Thorup-Kristensen K, Mueller T (2001) Disproportionately high N-mineralisation rates from green manures at low temperatures - implications for modeling and management in cool temperate agro-ecosystems. Plant Soil 228:73–82

    Article  CAS  Google Scholar 

  • Manzoni S, Porporato A (2007) Theoretical analysis of nonlinearities and feedbacks in soil carbon and nitrogen cycles. Soil Biol Biochem 39:1542–1556

    Article  CAS  Google Scholar 

  • Meier CL, Bowman WD (2008) Links between plant litter chemistry, species diversity, and below-ground ecosystem function. PNAS 105:19780–19785

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Mikan CJ, Schimel JP, Doyle AP (2002) Temperature controls of microbial respiration in arctic tundra soils above and below freezing. Soil Biol Biochem 34:1785–1795

    Article  CAS  Google Scholar 

  • Moore TR (1983) Winter-time litter decomposition in a Subarctic woodland. Arct Alp Res 15:413–418

    Article  Google Scholar 

  • Moriyama A, Yonemura S, Kawashima S, Du MY, Tang YH (2013) Environmental indicators for estimating the potential soil respiration rate in alpine zone. Ecol Indic 32:245–252

    Article  CAS  Google Scholar 

  • Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA (1991) Effects of temperature and substrate quality on element mineralization in 6 Arctic soils. Ecology 72:242–253

    Article  Google Scholar 

  • Nagy L, Grabherr G (2009) The Biology of Alpine Habitats. Oxford University Press, Oxford

    Google Scholar 

  • Oechel WC, Vourlitis GL, Hastings SJ, Zulueta RC, Hinzman L, Kane D (2000) Acclimation of ecosystem CO2 exchange in the Alaskan Arctic in response to decadal climate warming. Nature 406:978–981

    PubMed  Article  CAS  Google Scholar 

  • Ohtsuka T, Hirota M, Zhang XZ, Shimono A, Senga Y, Du MY, Yonemura S, Kawashima S, Tang YH (2008) Soil organic carbon pools in alpine to nival zones along an altitudinal gradient (4400–5300 m) on the Tibetan Plateau. Polar Sci 2:277–285

    Article  Google Scholar 

  • Paul EA, Clark FE (1996) Soil Microbiology and Biochemistry, 2nd edn. Academic, Sandigo

    Google Scholar 

  • Reid AM, Lamarque LJ, Lortie CJ (2010) A systematic review of the recent ecological literature on cushion plants: champions of plant facilitation. Web Ecol 10:44–49

    Article  Google Scholar 

  • Rinkes ZL, Weintraub MN, Deforest JL, Moorhead DL (2011) Microbial substrate preference and community dynamics during decomposition of acer saccharum. Fungal Ecol 4:396–407

    Article  Google Scholar 

  • Rinnan R, Michelsen A, Baath E, Jonasson S (2007) Mineralization and carbon turnover in subarctic heath soil as affected by warming and additional litter. Soil Biol Biochem 39:3014–3023

    Article  CAS  Google Scholar 

  • Rinnan R, Michelsen A, Jonasson S (2008) Effects of litter addition and warming on soil carbon, nutrient pools and microbial communities in a subarctic heath ecosystem. Appl Soil Ecol 39:271–281

    Article  Google Scholar 

  • Roy J, Albert CH, Choler P, Clément J, Ibanez S, Lavergne S, Saccone P, Zinger L, Geremia RA (2013) Microbes on the cliff: alpine cushion plants structure bacterial and fungal communities. Front Microbio 4:64

    CAS  Google Scholar 

  • Schaeffer SM, Evans RD (2005) Pulse additions of soil carbon and nitrogen affect soil nitrogen dynamics in an arid Colorado Plateau shrubland. Oecologia 145:425–433

    PubMed  Article  Google Scholar 

  • Schmidt SK, Lipson DA (2004) Microbial growth under the snow: implications for nutrient and allelochemical availability in temperate soils. Plant Soil 259:1–7

    Article  CAS  Google Scholar 

  • Schmidt IK, Jonasson S, Michelsen A (1999) Mineralization and microbial immobilization of N and P in arctic soils in relation to season, temperature and nutrient amendment. Appl Soil Ecol 11:147–160

    Article  Google Scholar 

  • Song MH, Jiang J, Cao GM, Xu XL (2010) Effects of temperature, glucose and inorganic nitrogen inputs on carbon mineralization in a Tibetan alpine meadow soil. Eur J Soil Biol 46:375–380

    Article  CAS  Google Scholar 

  • Song MH, Jiang J, Xu XL, Shi PL (2011) Correlation between CO2 efflux and net nitrogen mineralization and its response to external C or N supply in an alpine meadow soil. Pedosphere 21:666–675

    Article  CAS  Google Scholar 

  • Tan X, Chang SX (2007) Soil compaction and forest litter amendment affect carbon and net nitrogen mineralization in a boreal forest soil. Soil Till Res 93:77–86

    Article  Google Scholar 

  • Thiessen S, Gleixner G, Wutzler T, Reichstein M (2013) Both priming and temperature sensitivity of soil organic matter decomposition depend on microbial biomass - an incubation study. Soil Biol Biochem 57:739–748

    Article  CAS  Google Scholar 

  • Van Veen JA, Ladd JN, Frissel MJ (2004) Modelling C and N turnover through the microbial biomass in soil. Plant Soil 76:257–274

    Article  Google Scholar 

  • Vanhala P, Karhu K, Tuomi M, Bjorklof K, Fritze H, Liski J (2008) Temperature sensitivity of soil organic matter decomposition in southern and northern areas of the boreal forest zone. Soil Biol Biochem 40:1758–1764

    Article  CAS  Google Scholar 

  • Wang Z, Luo TX, Li RC, Tang YH, Du MY (2013) Causes for the unimodal pattern of biomass and productivity in alpine grasslands along a large altitudinal gradient in semi-arid regions. J Vet Sci 24:189–201

    Google Scholar 

  • Wu ZY (ed) (1986) Flora of Xizang. Science Press, Beijing, In Chinese

    Google Scholar 

  • Wu J, Joergensen RG, Pommerening B, Chaussod R, Brookes PC (1990) Measurement of soil microbial biomass C by fumigation extraction - an automated procedure. Soil Biol Biochem 22:1167–1169

    Article  CAS  Google Scholar 

  • Xie H, Ye JS, Liu XM, CY E (2010) Warming and drying trends on the Tibetan Plateau (1971–2005). Theor Appl Climat 101:241–253

    Article  Google Scholar 

  • Xu XL, Ouyang H, Richter A, Wanek W, Cao GM, Kuzyakov Y (2011) Spatio-temporal variations determine plant-microbe competition for inorganic nitrogen in an alpine meadow. J Ecol 99:563–571

    CAS  Google Scholar 

  • Yang Y, Niu Y, Cavieres LA, Sun H (2010) Positive associations between the cushion plant Arenaria polytrichoides (Caryophyllaceae) and other alpine plant species increase with altitude in the Sino-Himalayas. J Vet Sci 21:1048–1057

    Google Scholar 

  • Zeng LY, Xu LL, Tang SQ, Tersing T, Geng YP, Zhong Y (2010) Effect of sampling strategy on estimation of fine-scale spatial genetic structure in Androsace tapete (Primulaceae), an alpine plant endemic to Qinghai-Tibetan Plateau. J Syst Evol 48:257–264

    Article  Google Scholar 

  • Zhou XM (ed) (2001) Chinese Kobresia Meadows. Science Press, Beijing, In Chinese

    Google Scholar 

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Acknowledgments

We thank the following people and institution: Kai Fan, Gang Fu, Bingsong Zhang and Jingrong Yang for their help in the laboratory, and other members of the Lhasa Station for Tibetan Plateau Ecological Research, the Chinese Academy of Sciences for field work on the Tibetan Plateau. This research was supported by the National Key Projects for Basic Research of China (2010CB951704; 2010CB833501) and the National Natural Science Foundation of China (30700080; 31070391).

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Correspondence to Xingliang Xu.

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He, Y., Xu, X., Kueffer, C. et al. Leaf litter of a dominant cushion plant shifts nitrogen mineralization to immobilization at high but not low temperature in an alpine meadow. Plant Soil 383, 415–426 (2014). https://doi.org/10.1007/s11104-014-2216-4

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Keywords

  • Alpine meadow
  • Climate change
  • Cushion plant
  • C mineralization
  • Litter decomposition
  • N mineralization
  • Nutrient cycling
  • Tibetan Plateau