Abstract
Plant invasions may alter soil nutrient cycling due to differences in physiological traits between the invader and species they displace as well as differences in responses to anthropogenic factors such as nitrogen deposition and warming. Moso bamboo is expanding its range rapidly around the world, displacing diverse forests. In addition, near expansion fronts where invasions are patchy, moso bamboo and other species each contribute soil inputs. Nitrogen transformations and greenhouse gas (GHG) emissions are important processes associated with nutrient availability and climate change that may be impacted by bamboo invasions. We collected soils from uninvaded, mixed, and bamboo forests to understand bamboo invasion effects on carbon and N cycling. We incubated soils with warming and N addition and measured net nitrification and N mineralization rates and GHG (CO2 and N2O) emissions. Mixed forest soils had higher pH and total N and lower total organic carbon and C/N than either uninvaded or bamboo forest soils. Bamboo forest soils had higher total carbon, dissolved organic carbon, and ammonium N but lower total and nitrate N than uninvaded forest soils. Soil GHG emissions did not vary among forest types at lower temperatures but bamboo forest soils had higher CO2 and lower N2O emissions at higher temperatures. While net N transformation rates were lower in bamboo and uninvaded forest soils, they were highest in mixed forest soils, indicating non-additive effects of bamboo invasions. This suggests that plant invasion effects on N transformations and GHG emissions with global change in forests partially invaded by bamboo are difficult to predict from only comparing uninvaded and bamboo-dominated areas.
Similar content being viewed by others
References
Allison SD, Vitousek PM (2004) Rapid nutrient cycling in leaf litter from invasive plants in Hawai'i. Oecologia 141:612–619
Bai S, Zhou G, Wang Y, Liang Q, Chen J et al (2013) Plant species diversity and dynamics in forests invaded by Moso bamboo (Phyllostachys edulis) in Tianmu Mountain Nature Reserve. Biodivers Sci 21:288–295
Berglund SL, Ågren GI (2012) When will litter mixtures decompose faster or slower than individual litters? A model for two litters. Oikos 121:1112–1120
Berglund SL, Ågren GI, Ekblad A (2013) Carbon and nitrogen transfer in leaf litter mixtures. Soil Biol Biochem 57:341–348
Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157
Bremner JM (1997) Sources of nitrous oxide in soils. Nutr Cycl Agroecosyst 49:7–16
Brenner RE, Boone RD, Ruess RW (2005) Nitrogen additions to pristine, high-latitude, forest ecosystems: consequences for soil nitrogen transformations and retention in mid and late succession. Biogeochemistry 72:257–282
Cai Y, Chang SX, Ma B, Bork EW (2016) Watering increased DOC concentration but decreased N2O emission from a mixed grassland soil under different defoliation regimes. Biol Fertil Soils 52:987–996
Chang EH, Chiu CY (2015) Changes in soil microbial community structure and activity in a cedar plantation invaded by moso bamboo. Appl Soil Ecol 91:1–7
Chapman SK, Newman GS, Hart SC, Schweitzer JA, Koch GW (2013) Leaf litter mixtures alter microbial community development: mechanisms for non-additive effects in litter decomposition. PLoS One 8:e62671
Cheng Y, Wang J, Wang SQ, Zhang JB, Cai ZC (2014) Effects of soil moisture on gross N transformations and N2O emission in acid subtropical forest soils. Biol Fertil Soils 50:1099–1108
Corre MD, Brumme R, Veldkamp E, Beese FO (2007) Changes in nitrogen cycling and retention processes in soils under spruce forests along a nitrogen enrichment gradient in Germany. Glob Chang Biol 13:1509–1527
Cremer M, Kern NV, Prietzel J (2016) Soil organic carbon and nitrogen stocks under pure and mixed stands of European beech, Douglas fir and Norway spruce. For Ecol Manag 367:30–40
Deng BL, Li ZZ, Zhang L, Ma YC, Li Z et al (2016) Increases in soil CO2 and N2O emissions with warming depend on plant species in restored alpine meadows of Wugong Mountain, China. J Soils Sediments 16:777–784
Drenovsky RE, Grewell BJ, D'Antonio CM, Funk JL, James JJ et al (2012) A functional trait perspective on plant invasion. Ann Bot 110:141–153
Fang H, Cheng S, Yu G, Xu M, Wang Y et al (2014) Experimental nitrogen deposition alters the quantity and quality of soil dissolved organic carbon in an alpine meadow on the Qinghai-Tibetan Plateau. Appl Soil Ecol 81:1–11
Flückiger W, Braun S (1998) Nitrogen deposition in Swiss forests and its possible relevance for leaf nutrient status, parasite attacks and soil acidification. Environ Pollut 102:69–76
Fukushima K, Usui N, Ogawa R, Tokuchi N (2015) Impacts of moso bamboo (Phyllostachys pubescens) invasion on dry matter and carbon and nitrogen stocks in a broad-leaved secondary forest located in Kyoto, western Japan. Plant Species Biol 30:81–95
Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892
Gao W, Yang H, Kou L, Li S (2015) Effects of nitrogen deposition and fertilization on N transformations in forest soils: a review. J Soils Sediments 15:863–879
Guan F, Tang X, Fan S, Zhao J, Peng C (2015) Changes in soil carbon and nitrogen stocks followed the conversion from secondary forest to Chinese fir and Moso bamboo plantations. Catena 133:455–460
Gundersen P, Emmett BA, Kjønaas OJ, Koopmans CJ, Tietema A (1998) Impact of nitrogen deposition on nitrogen cycling in forests: a synthesis of NITREX data. For Ecol Manag 101:37–55
Hickman JE, Ashton IW, Howe KM, Lerdau MT (2013) The native-invasive balance: implications for nutrient cycling in ecosystems. Oecologia 173:319–328
Hobbie SE (2015) Plant species effects on nutrient cycling: revisiting litter feedbacks. Trends Ecol Evol 30:357–363
Hogberg P, Fan H, Quist M, Binkley D, Tamm CO (2006) Tree growth and soil acidification in response to 30 years of experimental nitrogen loading on boreal forest. Glob Chang Biol 12:489–499
IPCC (2007) Climate change 2007 the physical science basis: summary for policymakers. Cambridge University Press, New York
IPCC (2014) Synthesis report, climate change 2014. Cambridge University Press, New York
Jensen LS, Mueller T, Magid J, Nielsen NE (1997) Temporal variation of C and N mineralization, microbial biomass and extractable organic pools in soil after oilseed rape straw incorporation in the field. Soil Biol Biochem 29:1043–1055
Jiang L, Zhang L, Deng B, Liu X, Yi H et al. (2017) Alpine meadow restorations by non-dominant species increased soil nitrogen transformation rates but decreased their sensitivity to warming. J Soils Sediments 17:2329–2337
Li YF, Zhang JJ, Chang SX, Jiang PK, Zhou GM et al (2013) Long-term intensive management effects on soil organic carbon pools and chemical composition in Moso bamboo (Phyllostachys pubescens) forests in subtropical China. For Ecol Manag 303:121–130
Lima RAF, Rother DC, Muler AE, Lepsch IF, Rodrigues RR (2012) Bamboo overabundance alters forest structure and dynamics in the Atlantic Forest hotspot. Biol Conserv 147:32–39
Lin YT, Tang SL, Pai CW, Whitman WB, Coleman DC et al (2014) Changes in the soil bacterial communities in a cedar plantation invaded by Moso bamboo. Microbial Ecol 67:421–429
Liu J, Yang QP, Song QN, Yu DK, Yang GY et al (2013a) Strategy of fine root expansion of Phyllostachys pubescens population into evergreen broad-leaved forest. Chin J Plant Ecol 37:230–238
Liu L, Greaver TL (2010) A global perspective on belowground carbon dynamics under nitrogen enrichment. Ecol Lett 13:819–828
Liu XJ, Zhang Y, Han WX, Tang AH, Shen JL et al (2013b) Enhanced nitrogen deposition over China. Nature 494:459–462
Liu XZ, Wang L (2010) Scientific survey and study of biodiversity on the Lushan nature reserve in Jiangxi province. Science Press, Beijing
Lovett GM, Rueth H (1999) Soil nitrogen transformations in beech and maple stands along a nitrogen deposition gradient. Ecol Appl 9:1330–1344
Luo YQ, Wan SQ, Hui DF, Wallace LL (2001) Acclimatization of soil respiration to warming in a tall grass prairie. Nature 413:622–625
Martin-Olmedo P, Rees RM (1999) Short-term N availability in response to dissolved-organic-carbon from poultry manure, alone or in combination with cellulose. Biol Fertil Soils 29:386–393
Mo JM, Zhang W, Zhu WX, Gundersen P, Fang YT et al (2008) Nitrogen addition reduces soil respiration in a mature tropical forest in southern China. Glob Chang Biol 14:403–412
Mo QF, Li ZA, Zhu WX, Zou B, Li YW et al (2016) Reforestation in southern China: revisiting soil N mineralization and nitrification after 8 years restoration. Sci Rep 6:19770
Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978
Robertson GP, Coleman DC, Bledsoe CS, Sollins P (1999) Standard soil methods for long-term ecological research. Oxford University Press, New York
Schlesinger WH, Andrews JA (2000) Soil respiration and the global carbon cycle. Biogeochemistry 48:7–20
Song QN, Ouyang M, Yang QP, Lu H, Yang GY et al. (2016) Degradation of litter quality and decline of soil nitrogen mineralization after moso bamboo (Phyllostachys pubscens) expansion to neighboring broadleaved forest in subtropical China. Plant Soil 404:113–124
Song QN, Yang QP, Liu J, Yu DK, Fang K et al (2013) Effects of Phyllostachys edulis expansion on soil nitrogen mineralization and its availability in evergreen broadleaf forest. Chin J Appl Ecol 24:338–344
Song XZ, Jiang H, Zhang ZT, Zhou GM, Zhang SK et al (2014a) Interactive effects of elevated UV-B radiation and N deposition on decomposition of Moso bamboo litter. Soil Biol Biochem 69:11–16
Song XZ, Peng CH, Zhao ZY, Zhang ZT, Guo BH et al (2014b) Quantification of soil respiration in forest ecosystems across China. Atmos Environ 94:546–551
Song XZ, Zhou GM, Gu HH, Qi LH (2015) Management practices amplify the effects of N deposition on leaf litter decomposition of the Moso bamboo forest. Plant Soil 395:391–400
Stenberg B, Johansson M, Pell M, Sjödahl-Svensson K, Stenström J et al (1998) Microbial biomass and activities in soil as affected by frozen and cold storage. Soil Biol Biochem 30:393–402
Tang X, Xia M, Pérez-Cruzado C, Guan F, Fan S (2017) Spatial distribution of soil organic carbon stock in Moso bamboo forests in subtropical China. Sci Rep 7:42640
Tripathi SK, Sumida A, Shibata H, Ono K, Uemura S et al (2006) Leaf litterfall and decomposition of different above-and belowground parts of birch (Betula ermanii) trees and dwarf bamboo (Sasa kurilensis) shrubs in a young secondary forest in Northern Japan. Biol Fertil Soils 43:237–246
Tu LH, Peng Y, Chen G, Hu H, Xiao Y et al (2014) Direct and indirect effects of nitrogen additions on fine root decomposition in a subtropical bamboo forest. Plant Soil 389:273–288
Umemura M, Takenaka C (2015) Changes in chemical characteristics of surface soils in hinoki cypress (Chamaecyparis obtusa) forests induced by the invasion of exotic Moso bamboo (Phyllostachys pubescens) in central Japan. Plant Species Biol 30:72–79
Urakawa R, Ohte N, Shibata H, Isobe K, Tateno R et al (2016) Factors contributing to soil nitrogen mineralization and nitrification rates of forest soils in the Japanese archipelago. For Ecol Manag 361:382–396
Vitousek PM, D'Antonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Wardle DA (2002) Communities and ecosystems : linking the aboveground and belowground components. Princeton University Press, Princeton
Wolkovich EM, Lipson DA, Virginia RA, Cottingham KL, Bolger DT (2010) Grass invasion causes rapid increases in ecosystem carbon and nitrogen storage in a semiarid shrubland. Glob Chang Biol 16:1351–1365
Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732
Xu QF, Jiang PK, Wu JS, Zhou GM, Shen RF et al (2015) Bamboo invasion of native broadleaf forest modified soil microbial communities and diversity. Biol Invasions 17:433–444
Yan ER, Wang XH, Guo M (2009) Temporal patterns of net soil N mineralization and nitrification through secondary succession in the subtropical forests of eastern China. Plant Soil 320:181–194
Yan ER, Wang XH, Huang JJ, Li GY, Zhou W (2008) Decline of soil nitrogen mineralization and nitrification during forest conversion of evergreen broad-leaved forest to plantations in the subtropical area of Eastern China. Biogeochemistry 89:239–251
Zhang H, Zhuang S, Qian H, Wang F, Ji H (2015) Spatial variability of the topsoil organic carbon in the Moso bamboo forests of southern China in association with soil properties. PLoS One 10:e0119175
Zhang J, Sun W, Zhong W, Cai Z (2014a) The substrate is an important factor in controlling the significance of heterotrophic nitrification in acidic forest soils. Soil Biol Biochem 76:143–148
Zhang L, Wang H, Zou J, Rogers WE, Siemann E (2014b) Non-native plant litter enhances soil carbon dioxide emissions in an invaded annual grassland. PLoS One 9:e92301
Zhang L, Zhang Y, Wang H, Zou J, Siemann E (2013) Chinese tallow trees (Triadica sebifera) from the invasive range outperform those from the native range with an active soil community or phosphorus fertilization. PLoS One 8:e74233
Zhang L, Zhang Y, Zou J, Siemann E (2014c) Decomposition of Phragmites australis litter retarded by invasive Solidago canadensis in mixtures: an antagonistic non-additive effect. Sci Rep 4:05488
Zou J, Rogers WE, DeWalt SJ, Siemann E (2006) The effect of Chinese tallow tree (Sapium sebiferum) ecotype on soil–plant system carbon and nitrogen processes. Oecologia 150:272–281
Acknowledgments
This study was supported by the Gan-Po 555 Talent Project Funding of Jiangxi Province, the Research Foundation and Postdoctoral Science Foundation of Jiangxi Agricultural University (09005172 and 9232306047) and the High-end Foreign Experts Recruitment Program (GDW20157200307). We acknowledge the reviewers for their insightful comments and the Lushan National Forest Ecosystem Research Station and Lushan National Nature Reserve for the field work support.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
ESM 1
(DOCX 153 kb)
Rights and permissions
About this article
Cite this article
Li, Z., Zhang, L., Deng, B. et al. Effects of moso bamboo (Phyllostachys edulis) invasions on soil nitrogen cycles depend on invasion stage and warming. Environ Sci Pollut Res 24, 24989–24999 (2017). https://doi.org/10.1007/s11356-017-0186-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0186-9