A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe.

Ecology, 97(1), 2016, pp. 65–74 © 2016 by the Ecological Society of America A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe Q IUYING T IAN , 1,2 N ANA L IU , 1,3 W ENMING B AI , 1 L INGHAO L I , 1 J IQUAN C HEN , 4,5 P ETER B. R EICH , 6,7 Q IANG Y U , 8,9 D ALI G UO , 10 M ELINDA D. S MITH , 9 A LAN K. K NAPP , 9 W EIXIN C HENG , 8,11 P ENG L U , 1 Y AN G AO , 1 A N Y ANG , 1 T IANZUO W ANG , 1 X IN L I , 1 Z HENGWEN W ANG , 8 Y IBING M A , 12 X INGGUO H AN 1,8 AND W EN -H AO Z HANG 1,2,13 State Key Laboratory of Vegetation and Environmental Change , Institute of Botany , Chinese Academy of Sciences , Beijing 100093 , China Research Network of Global Change Biology , Beijing Institutes of Life Science , Chinese Academy of Sciences , Beijing 100101 , China University of Chinese Academy of Sciences , Beijing 100049 , China International Center for Ecology, Meteorology, and Environment (IceMe) , Nanjing 210044 , China CGCEO/Geography , Michigan State University , East Lansing , Michigan 48823 , USA Department of Forest Resources , University of Minnesota , St. Paul , Minnesota 55108 , USA Hawkesbury Institute for the Environment , University of Western Sydney , Penrith , New South Wales 2753 , Australia State Key Laboratory of Forest and Soil Ecology , Institute of Applied Ecology , Chinese Academy of Sciences , Shenyang 110164 , China Department of Biology and Graduate Degree Program in Ecology , Colorado State University , Fort Collins , Colorado 80523 , USA Key Laboratory of Ecosystem Network Observation and Modeling , Synthesis Research Center of Chinese Ecosystem Research Network , Institute of Geographic Sciences and Natural Resources Research , Chinese Academy of Sciences , Beijing 100101 , China Environmental Studies , University of California , Santa Cruz , California 95064 , USA National Soil Fertility and Fertilizer Effects Long-term Monitoring Network , Institute of Agricultural Resources and Regional Planning , Chinese Academy of Agricultural Sciences , Beijing 100081 , China Abstract . Loss of plant diversity with increased anthropogenic nitrogen (N) deposition in grasslands has occurred globally. In most cases, competitive exclusion driven by preemp- tion of light or space is invoked as a key mechanism. Here, we provide evidence from a 9- yr N- addition experiment for an alternative mechanism: differential sensitivity of forbs and grasses to increased soil manganese (Mn) levels. In Inner Mongolia steppes, increasing the N supply shifted plant community composition from grass–forb codominance (primarily Stipa krylovii and Artemisia frigida , respectively) to exclusive dominance by grass, with associated declines in overall species richness. Reduced abundance of forbs was linked to soil acidifi cation that increased mobilization of soil Mn, with a 10- fold greater accumulation of Mn in forbs than in grasses. The enhanced accumulation of Mn in forbs was correlated with reduced photosynthetic rates and growth, and is consistent with the loss of forb species. Differential accumulation of Mn between forbs and grasses can be linked to fun- damental differences between dicots and monocots in the biochemical pathways regulating metal transport. These fi ndings provide a mechanistic explanation for N- induced species loss in temperate grasslands by linking metal mobilization in soil to differential metal acquisition and impacts on key functional groups in these ecosystems. Key words: Artemisia frigida ; forbs and grasses ; Inner Mongolia, China ; manganese mobilization and acquisition ; nitrogen deposition ; photosynthesis ; soil acidifi cation ; species richness ; Stipa krylovii ; temperate steppe. I NTRODUCTION There has been a dramatic increase in atmospheric N deposition due to fossil fuel combustion and the use of N fertilizers in the past century (Clark and Tilman 2008 , Galloway et al. 2008 ), with 2010 values projected to increase >1.5- fold by 2030 (Bodirsky et al. 2014 ). This increase in N deposition is altering N cycling and the productivity and biodiversity of Manuscript received 24 December 2014 ; accepted 26 June 2015 . Corresponding Editor: S. D. frey E-mail: whzhang@ibcas.ac.cn terrestrial ecosystems globally (Galloway et al. 2008 , Bobbink et al. 2010 ). In grassland ecosystems in par- ticular, long- term N deposition has resulted in signif- icant reductions in plant species richness and altered ecosystem function (Stevens et al. 2004 , Clark et al. 2007 , Harpole and Tilman 2007 , Clark and Tilman 2008 , Bobbink et al. 2010 , Dupre et al. 2010 , Fang et al. 2012 , Isbell et al. 2013 ). Several mechanisms have been proposed to explain plant species loss with increased N deposition, but their relative importance is generally unknown (Suding et al. 2005 , Clark et al. 2007 , Harpole and Tilman 2007 , Hautier et al. 2009 , Borer et al. 2014 ). Competitive exclusion resulting from