Atmospheric CO2 Enrichment and Reactive Nitrogen Inputs

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Environmental Processes

Atmospheric CO2 enrichment and reactive nitrogen inputs interactively stimulate soil cation losses and acidification Li Zhang, Yunpeng Qiu, Lei Cheng, Yi Wang, Lingli Liu, Cong Tu, Dan C. Bowman, Kent O. Burkey, Xinmin Bian, Weijian Zhang, and Shuijin Hu Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b00495 • Publication Date (Web): 17 May 2018 Downloaded from http://pubs.acs.org on May 17, 2018

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Environmental Science & Technology

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Atmospheric CO2 enrichment and reactive nitrogen inputs interactively stimulate soil

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cation losses and acidification†

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Li Zhang&+//, Yunpeng Qiu&+⊥, Lei Cheng$, Yi Wang#, Lingli Liu%, Cong Tu∇, Dan C. Bowman§,

5

Kent O. Burkey§||, Xinmin Bian//, Weijian Zhang//, and Shuijin Hu*+⊥

6 7

+

8

27695, USA

9

//

Department of Entomology & Plant Pathology, North Carolina State University, Raleigh, NC

Institute of Applied Ecology, Nanjing Agricultural University, Nanjing 210095, China

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⊥ College

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210095, China

12

$

College of Life Sciences, Zhejiang University, Hangzhou 310058, China

13

#

State Key Laboratory of Loess and Quaternary Geology, Institute of Earth Environment,

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Chinese Academy of Sciences, Xi'an, 710061, China

15

%

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Academy of Sciences, Beijing 100093, China

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∇ Department

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Raleigh, NC 27695, USA,

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§

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USA,

21

||

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Research Unit, Raleigh, NC 27607, USA

of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing

State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese

of Biological and Agricultural Engineering, North Carolina State University,

Department of Crop and Soil Sciences, North Carolina State University, Raleigh, NC 27695,

United States Department of Agriculture, Agricultural Research Service, Plant Science

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†

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execution of the field experiment.

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&

This paper is dedicated to Dr. Fitzgerald L. Booker for his contribution to the design and

These authors contributed equally.

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ABSTRACT

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Reactive N inputs (Nr) may alleviate N-limitation of plant growth and are assumed to help

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sustain plant responses to the rising atmospheric CO2 (eCO2). However, Nr and eCO2 may elicit

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a cascade reaction that alters soil chemistry and nutrient availability, shifting the limiting factors

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of plant growth, particularly in acidic tropical and subtropical croplands with low organic matter

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and low nutrient cations. Yet, few have so far examined the interactive effects of Nr and eCO2 on

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the dynamics of soil cation nutrients and soil acidity. We investigated the cation dynamics in the

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plant-soil system with exposure to eCO2 and different N sources in a subtropical, acidic

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agricultural soil. eCO2 and Nr, alone and interactively, increased Ca2+ and Mg2+ in soil solutions

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or leachates in aerobic agroecosystems. eCO2 significantly reduced soil pH, and NH4+-N inputs

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amplified this effect, suggesting that eCO2-induced plant preference of NH4+-N and plant growth

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may facilitate soil acidification. This is, to our knowledge, the first direct demonstration of eCO2

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enhancement of soil acidity, although other studies have previously shown that eCO2 can

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increase cation release into soil solutions. Together, these findings provide new insights into the

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dynamics of cation nutrients and soil acidity under future climatic scenarios, highlighting the

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urgency for more studies on plant-soil responses to climate change in acidic tropical and

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subtropical ecosystems.

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TOC/Abstract art

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INTRODUCTION

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Rising reactive N inputs (Nr) and atmospheric CO2 concentrations (eCO2) are two concurrent

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factors that are believed to sustain the productivity of terrestrial ecosystems and promote

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ecosystem C sequestration.1-3 This assumption, however, has not taken the potential negative

94

effects of Nr and eCO2 into consideration. Simultaneously, ozone in the troposphere is a dynamic,

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short-lived air pollutant and is toxic to plant.4,5 Its concentration has more than doubled since

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1800.6 Elevated O3 (eO3) generally suppresses photosynthesis and reduces plant growth and

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subsequent C allocation belowground.7,8 Climate change (particularly eCO2) has elicited some

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fundamental changes in ocean biogeochemistry, resulting in globally ocean acidification with

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consequent impacts on both ocean life and marine resources.9-11 eCO2 and Nr may alter soil

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chemical properties and the relative availability of soil nutrients, shifting the limiting factors of

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ecosystem productivity. In particular, high Nr often cause cation losses and soil acidification.12-14

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Also, sporadic evidence suggests that eCO2 may enhance cation release from soil through

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stimulating carbonic acid formation, cation solubility, and weathering15,16 and cation losses

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through biomass removal and/or leaching.17,18 Yet, few have so far assessed the interactive

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effects of Nr and eCO2 on soil nutrient cations and soil acidity, especially in the humid

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subtropics and tropics where soil cations are low.19

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Soils in the warm and humid regions are generally acidic and infertile. The widespread

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existence of cation- and phosphorus-deficiency, Al toxicity and low available N co-limit their

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productivity.13,20 A soil pH of 5.0 appears to be a critical threshold value for many crop plants as

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Al toxicity intensifies below this value.21,22 Chemical N fertilizers are the major N source for

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many agricultural plants and are the primary agent of soil acidification in agroecosystems.23 5 ACS Paragon Plus Environment


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Fertilizer N usually enters the soil in the form of ammonium (NH4+) and nitrifying microbes

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rapidly convert NH4+ into NO3- (i.e., nitrification), generating proton ions (H+) and further

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facilitating soil acidification24,25. Also, eCO2 in general stimulates plant growth and

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photosynthate allocation belowground and enhances soil root and microbial activities.26,27

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Increased CO2 production due to higher biological activities generate soil H2CO3 that possesses

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soil acidifying potential28 and may stimulate cation release from soil. However, this effect has

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largely documented in anaerobic environments such as deep soils16,29 or rice paddies18 but not in

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the aerobic soils. Also, CO2-induced cation losses are cumulative and are irreversible. Despite

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the tight coupling between C and N cycles, few have ascertained how N fertilization and

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atmospheric CO2 enrichment may jointly affect soil chemistry and the dynamics of soil nutrient

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cations under future climate scenarios.19

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We conducted two independent but complementary experiments to investigate how eCO2

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and Nr interactively affect soil cation dynamics and soil acidity in surface soils of aerobic

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agroecosystems. In contrast, eO3 usually reduces plant growth5,8 and likely reduces root and

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microbial activities,7 and we therefore used it as a negative control. We hypothesized that (i)

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eCO2 and Nr interactively stimulate cation release from soil, plant cation uptake and cation

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leaching, facilitating soil acidification; (ii) eCO2-induced plant preference of NH4+-N may

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function as a primary driver of soil acidification.

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MATERIAL AND METHODS

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The field experiment

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This experiment was conducted in conjunction with a long-term CO2 and O3 study at the Lake

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Wheeler farm of North Carolina State University, Raleigh, NC, USA (35°43'N, 78°40'W;

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elevation 120 m). Annual mean temperature and precipitation are 15.2°C and 1050 mm,

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respectively. The soil is an Appling sandy loam (fine, kaolinitic, thermic Typic Kanhapludult),

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well drained with a pH(H2O) of 5.5, and contained 9.0 g C and 0.86 g N kg-1 soil when the

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experiment was initiated (May 2005).

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This experiment was conducted on a soybean-wheat system, using open-top chambers

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(OTC, 3.0 m diameter × 2.4 m tall; SI Figure S1).27 The experiment was a 2 × 2 factorial design

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with four treatments randomly assigned into each of four blocks. Four different trace-gas

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treatments were: (a) control, ambient CO2 in charcoal-filtered (CF) air; (b) eO3, CF air plus 1.4

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times ambient O3, (c) eCO2, CF air plus 180 µmol mol-1 CO2, and (d) eCO2 and eO3, CF air with

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1.4 times ambient O3 and 180 µmol mol-1 CO2. The 12-h daily (08:00-20:00 h) averaged CO2

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concentrations were 380 and 560 µmol mol-1 CO2 for ambient (a and b) and elevated (c and d)

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CO2 treatments, respectively. The daily averaged O3 concentrations for ambient (a and c) and

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elevated (b and d) O3 treatments were 21 and 59 nl l-1 O3, separately. Carbon dioxide was

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dispensed from a 14-ton liquid receiver 24 h daily and monitored at canopy height with an

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infrared CO2 analyzer (model 6252, LiCor Inc., Lincoln, NE, USA). Ozone was generated by

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electrostatic discharge in dry O2 (model GTC-1A, Ozonia North America, Elmwood Park, NJ,

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USA) and dispensed 12 h daily (08:00-20:00 h) in proportion to ambient O3 concentrations. It

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was monitored at canopy height using a UV photometric O3 analyzer (model 49, Thermo

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Environmental Instruments Co., Franklin, MA, USA).

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Soybean [Glycine max (L.) Merr.] was planted each spring followed by winter wheat (Triticum aestivum L.) in the fall using no-till practices. Plants were exposed to reciprocal 7 ACS Paragon Plus Environment


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combinations of CO2 and O3 within cylindrical OTCs from emergence to physiological maturity.

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N fertilizers of NH4NO3 were applied to wheat plants at a rate of 120 kg N ha-1 (24 and 96 kg N

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ha-1 at planting and in early March, respectively) and no additional N fertilizers were added to

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soybean plants. Dolomitic limestone was applied annually at a rate of 500 g per chamber

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(equivalent to 708 kg ha-1) in late October immediately before wheat planting according to soil

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test recommendations.

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Lysimeters and PRS probes

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Lysimeters (SoilMoisture, Inc., Santa Barbara, CA, USA) were installed at 20 cm soil depth in

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2007 at each chamber to examine cation nutrients in soil solutions.30 Soil solution samples were

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collected in response to a vacuum of 0.06mPa every two weeks using acid-washed vials and

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frozen at -20 °C. The cations in soil solutions from the lysimeters were determined with an ICP-

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Optical Emission Spectrometer (Perkin Elmer Co., Norwalk, CT, USA).

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Soil nutrient availability responses to plant-mediated effects of eCO2 and eO3 were

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measured using ion-exchange resins (Plant Root Simulator (PRS) probes, Western Ag

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Innovations Inc., Saskatoon, Saskatchewan) by the method described by Bengtson et al. (2007).31

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(PRS) probes were installed in the rooting zone (0-5cm depth) during late reproductive phase

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(November 2008) and mid-vegetative phase (July 2009) of the soybean rotation and during mid-

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vegetative growth of the wheat rotation (March 2009). For each burial period, three (PRS) probes

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for measuring soil available anions and three probes for measuring soil available cations were

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incubated in each chamber for two weeks. At the end of the burial period, the probes were

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removed and thoroughly washed with deionized water. Afterward, the cleaned (PRS) probes

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were sent to the Western Ag Innovations Inc. laboratory in Saskatoon, where they were analyzed

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for NH4+, NO3-, Ca2+, Mg2+, K+, Al3+, Fe2+, H2PO4-, and Mn2+. 8 ACS Paragon Plus Environment

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Cation nutrients in plant biomass

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Aboveground plant biomass and plant biomass Ca and Mg were quantified at the final plant

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harvest each year (except 2006). All aboveground plant biomass was harvested from each

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chamber. Soybean plants were separated into leaves, stems and seeds, while wheat plants were

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divided into straw and seeds. Plant materials were oven-dried at 65°C and weighed. Seed and

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residue subsamples were cut into pieces and ground into fine powder using an 8000-D Mixer

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Mill (SPEX CertiPrep Inc., Metuchen, NJ, USA) and prepared through dry ashing on a high

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temperature muffle furnace (500 °C). After the samples cooled down, 2 mL distilled water was

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added along with 4 ml of 6N hydrochloric acid. The solution was then warmed slightly (to ca.

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50 °C) on a steam plate and transferred into a 50 ml volumetric flask with distilled water. After

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that, the solution was mixed and filtered. The Ca, Mg and K concentrations of plant components

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were then analyzed on an ICP-Optical Emission Spectrometer (Perkin Elmer Co., Norwalk, CT,

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USA).32

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Soil pH

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Soil pH values were measured with an electrode and HI 9026 meter (Hanna Instruments,

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Woonsocket, RI, USA) using a soil/deionized water suspension of 1:2.5 (weight: volume).

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The microcosm experiment

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This microcosm experiment was conducted in the CO2 exposure facility at the USDA Air-

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Quality greenhouse at North Carolina State University (SI Figure S2). The facility consisted of

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20 continuously stirred tank reactor (CSTR) chambers designed for the exposure of plants to CO2

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and O3 gases.27, 33 For those chambers (1.2 m diameter × 1.4 m tall) assigned to an eCO2

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treatment, compressed CO2 was added to the air entering the CSTR using a rotometer to control 9 ACS Paragon Plus Environment


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flow so that CO2 concentration was maintained at target level. The air continuously moved out

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the CSTR and thus minimized the heating effect of chambers. To monitor CO2 concentrations, an

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infrared analyzer (model 6252, LiCor Inc., Lincoln, NE, USA) was used to measure CSTR

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chamber air CO2 concentrations, with a computer collecting and averaging CO2 and temperature

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data for analysis.

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This microcosm experiment was initiated to assess the interactive effects of eCO2 and the

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species and quantities of N inputs on soil acidity and soil nutrient cations. This was a split-split-

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plot experiment with whole-plots randomly assigned into each of four blocks. The whole-plot

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treatments were two atmospheric CO2 levels (ambient at 400 p.p.m.v. vs. elevated at 580

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p.p.m.v.) with four replicates (that is, four CSTR chambers for each CO2 level). The split-factors

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factors were two N species (NH4+-N vs. NO3--N) and the split-split-plot factors were two N

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levels (low at 62.5 vs. high at 125 kg N ha-1). While the high N level approximately corresponds

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to current N inputs in North Carolina, the low level intends to mimic N supplies in developing

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countries across the acidic soil regions in the future decades.34,35

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Mini-lysimeters

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We used mini-lysimeters (SI Figure S3),36 which were constructed from polyvinyl chloride

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columns (15 cm in diameter and 30 cm deep) with a cap at the bottom, to manipulate soil

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nutrient cation leaching. Each column was installed with one mini-lysimeter, which was

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equipped with two ceramic cups (2.2 cm diameter × 7.0 cm long) (SoilMoisture Inc., Santa

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Barbara, CA, USA) being embedded in 3-cm diatomaceous earth (Rising Sun Pools Inc., Raleigh,

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NC, USA), layered at the bottom of the column. The ceramic cups were connected with a ‘Y-

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Type’ connector (Thermo Fisher Scientific Inc., USA) in situ via tubing to a 250-mL collection

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bottle, which was connected to a manifold vacuum line and pump equipped with a pressure 10 ACS Paragon Plus Environment

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gauge. The soil was collected from the ‘field OTC study’ site in October 2012. The field soil

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was a low fertility sandy loam (fine, kaolinitic, thermic Typic Kanhapludult) with pH(H2O) of 5.2.

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Amount of 2.4 g dolomitic limestone (sieved through 2mm) (Winston Weaver Inc., Winston

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Salem, NC, USA) was mixed into 2.4 kg of soil (dry soil equivalent) to each microcosm to

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ensure healthy growth of wheat plants. Water was added to let the diatomaceous earth stabilize

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for 2 days, then the mixed soil was added on to the stabilized diatomaceous earth. The mixed soil

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was watered to 15% (w/w; ca. 75% WFC) and stabilized for 30 days. Five subsamples were

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obtained for determination of soil pH, and the averaged pH(H2O) was 5.6 at initiation of the

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experiment.

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Seed planting

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Ten seeds of winter wheat were sown into each column and thinned after emergence so that each

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column had six healthy plants. The CO2 fumigation started one week later after seed sowing. At

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the 4th week after seedling emergence, 50 ml of nutrient solution containing 32 mg N kg-1 soil of

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(NH4)2SO4 or KNO3 and 10 mg P kg-1 soil of NaH2PO4 was applied to the high-level N

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treatments, while half volume of the N nutrient solution and 10 mg P kg-1 soil of NaH2PO4 was

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applied to the low-level N treatments. During the growing season, nutrient solutions containing

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16 mg N kg-1 soil of (NH4)2SO4 or KNO3 (high N treatment) or half volume (low N treatment)

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and 5 mg P kg-1 soil of NaH2PO4 were added to the columns at the 8th, 10th and 12th week after

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seedling emergence. Equivalent K2SO4 was applied to balance K+. Columns were watered with

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deionized water daily.

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Soil nutrient leachates



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During the growing season, a vacuum of 0.010 MPa was connected to the ceramic cups for 30

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min to promote complete drainage into collection bottles after watering. Soil nutrient leachates

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were collected from the collection bottles using acid-washed vials and stored at 4°C. Leachate

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samples were collected two weeks after each N fertilization and 1d before plant harvest, and

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were subsampled and analyzed for NH4+-N, NO3--N, Ca2+, Mg2+ and Al3+ concentrations. The

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concentrations of Ca2+ and Mg2+ were analyzed using an ICP-Optical Emission Spectrometer

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(Perkin Elmer Co., Norwalk, CT, USA). NH4+- and NO3--N were measured using a Lachat

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QC8000 Flow Injection Analyzer. Total leaching losses of NH4+-N, NO3--N, Ca2+ and Mg2+ were

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calculated with leachate volume and cation concentrations. Cumulative NH4+-N, NO3--N, Ca2+,

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Mg2+ and Al3+ referred to the sum of NH4+-N, NO3--N, Ca2+, Mg2+ and Al3+ contents in soil

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solutions, respectively.

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Plant biomass and cation uptake

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At the plant physiological maturity, all aboveground plant parts were harvested at the soil surface

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and carefully separated into seeds and residue components (stems and leaves). Roots were

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carefully separated from the soil and washed thoroughly with tap water. Seed, residue and root

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weights were determined after being oven dried at 65°C for 48 hours. Subsamples of seeds and

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residues were ground into fine powder using an 8000-D Mixer Mill (SPEX CertiPrep Inc.,

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Metuchen, NJ, USA) and prepared using dry ashing procedure by a high temperature muffle

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furnace (500 °C). The Ca and Mg concentrations of plant components were analyzed on an ICP-

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Optical Emission Spectrometer (Perkin Elmer Co., Norwalk, CT, USA).

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Soil pH

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Soils were collected immediately after moving aboveground plant parts and separated from

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diatomaceous earth. Soil pH values were measured with an electrode and HI 9026 meter (Hanna 12 ACS Paragon Plus Environment

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Instruments, Woonsocket, RI, USA) using a soil/deionized water suspension of 1:2.5 (weight:

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volume).

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Statistical analysis

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For the field experiment, the effects of eCO2 on the response variables (soil cations and pH, plant

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biomass and plant biomass Ca and Mg) for the entire period from 2005 to 2009 were valued

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using the repeated-measures analysis of variance (ANOVA). For the microcosm study, the

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effects and interactions of eCO2 and Nr on soil and plant parameters (soil pH, plant biomass, and

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plant biomass Ca and Mg) were analyzed using a split-split plot model. Repeated-measures

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ANOVA was performed to examine the effects of eCO2 and Nr on the leaching dynamics of soil

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solution chemistry. All statistical analyses were performed using the SAS 9.3 (SAS Institute, Inc.,

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Cary, NC, USA). For all tests, P< 0.05 was considered to indicate a statistically significant

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difference.

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RESULTS

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The impact of eCO2 on plant biomass and cation nutrients in plant biomass and soil

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solutions in the field experiment

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Elevated CO2 on average increased soybean biomass by 33.4%, increasing biomass Ca and Mg

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by 36.9% and 28.9%, respectively (SI Table S4 and S6). It also increased aboveground wheat

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biomass by 16.3% (P < 0.05) but did not significantly affect biomass Ca and Mg (SI Table S5

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and S6).



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eCO2 significantly and consistently increased Ca2+ and Mg2+ in soil solutions (Figure 1)

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Similarly, eCO2 increased Fe2+ and Mn2+ in solutions though statistically significant only for

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Mn2+ in 2009 (SI TableS2 and S3). In contrast, eCO2 significantly reduced K+ concentration

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under soybean (November 2008 and July 2009; SI Table S1 and S3) but increased it under wheat

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(March 2009; SI Table S2). In addition, eCO2 did not affect soil pH and Al3+ in soil solutions

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(Figure 2a, SI Table S1, S2 and S3) and neither eO3 nor eCO2 × eO3 had a significant effect on

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Ca2+, Mg2+ and Al3+ in soil solutions (Figure 1, SI Table S1, S2 and S3).

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Interactive effects of eCO2, N species and N level on cation nutrients in soil leachates and

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plant biomass in the microcosm experiment

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Both CO2 concentrations and N inputs affected Ca2+ and Mg2+ in soil leachates and plant

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biomass. Across all the 5 sampling dates, eCO2 alone increased Ca2+ and Mg2+ in soil leachates

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by 132% and 95%, respectively, and eCO2 and reactive N had significant interactive effects on

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Ca2+ and Mg2+ in soil leachates (Figure 3 and SI Table S7). Also, eCO2 effect on Ca2+ and Mg2+

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was only significant when NH4+-N was applied (Figure 3). However, eCO2 did not significantly

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affect plant biomass Ca (P = 0.89) and Mg (P = 0.09) at the final harvest (SI Figure S4 and Table

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S7). N species significantly affected plant biomass, Ca2+ and Mg2+ in soil leachates and plant

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biomass Mg (SI Figure S4, S5 and Table S7). Total biomass was 12.9% higher under NH4+-N

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than NO3--N (SI Figure S5). Soil leachate Ca2+ and Mg2+ was almost 4 times and 7 times higher

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with NH4+-N than NO3--N inputs, respectively (P < 0.01; Figure 3), suggesting that proton

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produced by nitrification may play a dominant role in promoting cation release from soil. High N

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inputs increased plant biomass by 44.7% (SI Figure S5), and biomass Ca and Mg by 42.0% and

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33%, respectively (SI Figure S4). Also, Al concentration in the soil leachates was significantly 14 ACS Paragon Plus Environment

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higher under NH4+-N than NO3--N input (SI Figure S6). However, no significant CO2 or CO2 × N

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effects were observed. The Ca2+ and Mg2+ dynamics exhibited a very similar pattern under two N

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levels (Figure 3), and plant uptake was higher with high than low N inputs (SI Figure S4). In

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addition, NH4+- and NO3--N concentrations in the leachates were close to detection limits and

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exhibited no differences among the treatments (data not shown).

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As expected, the species and quantity of N inputs differently affected soil pH: soil pH

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remained statistically unchanged at 5.64 with NO3--N inputs but significantly reduced to 5.20

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with NH4+-N inputs (Figure 2b). However, the significant effect of eCO2 on soil pH was

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surprising (Figure 2b). Averaged across different N treatments, eCO2 induced a small, but

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significant decrease in soil pH (by 0.18 units; P < 0.01; Figure 2b and SI Table S7). eCO2

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significantly interacted with NH4+-N in reducing soil pH, leading to different soil pH responses

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under two NH4+-N levels. In contrast, it did not interact with NO3--N as eCO2 reduced soil pH by

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about 0.22 units at both NO3--N levels (Figure 2b).

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DISCUSSION

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Rising atmospheric CO2 (eCO2) and reactive N inputs (Nr) may alter cation dynamics and

333

enhance soil acidity through different mechanisms and/or processes. We proposed a unifying

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framework of eCO2 and Nr interactive effects on soil cation losses and acidity. While Nr

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primarily modify microbial processes that generate protons via nitrification to alter the dynamics

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of cations, eCO2 increases protons largely through plant-mediated processes (Figure 4). Two N

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species also have profound differences in their impacts on proton production and soil pH. NH4+-

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N inputs can potentially enhance proton production through three pathways: microbial H+ 15 ACS Paragon Plus Environment


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production during nitrification,13 plant H+ excretion to maintain cation-anion balance in response

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to plant NH4+ uptake,37 and increased plant growth and the resulting root and microbial activities

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(Figure 4 and SI Figure S5).38 eCO2 may enhance soluble cations in soil solutions through H+

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replacement of Ca2+ and Mg2+ from exchange sites over the short term18 and weathering over the

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long-term.16 Significant interactive effects on soil pH between eCO2 and NH4+-N inputs (Figure

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2b) suggest that plant H+ excretion following CO2-enhancement of NH4+ uptake may play a

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major role in shaping long-term impacts of eCO2 on soil cations and soil acidity. In contrast, the

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possible pathway through which NO3- may stimulate H+ generation is through enhancing plant

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growth and root activity. Despite increasing plant biomass by 46.8% (SI Figure S5), high NO3--N

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inputs did not affect soil pH (Figure 2b), suggesting that plant excretion of hydroxyl ions (OH-)

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to maintain cation-anion balance may have partially offset H+ generation of a larger plant root

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system. The effects of Nr on soil acidity may be further amplified under eCO2 at least through

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two mechanisms. First, eCO2 increases CO2 availability for plants and thus reduces stomatal

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conductance and leaf transpiration,39,40 reducing plant NO3- uptake because NO3- reaches to roots

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mainly through mass flow.41 Also, eCO2 reduces plant photorespiration that produces

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intermediates needed for plant nitrate assimilation.42, 43 Consequently, plants have to increase

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NH4+ uptake to meet plant C intake, further enhancing H+ release. Second, CO2-enhancement of

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plant water use efficiency improves soil water availability44 and likely increases leaching of soil

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cations and NO3-, facilitating acidification.

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CO2-enhancement of cations in soil solutions has previously been demonstrated.29,45

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eCO2 often stimulates carbonic acid formation, cation solubility, and weathering, potentially

360

enhancing soil cation availability.16,18 Yet, our results provide the first direct evidence showing

361

that eCO2 promotes soil acidity in upland surface soils. Soil acidification is a worldwide 16 ACS Paragon Plus Environment

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362

phenomenon and has been largely attributed to acid rain and reactive N inputs.46 Yet, significant

363

acidification has occurred in recent decades in remote areas such as Inner Mongolia where acid

364

deposition was relatively low.47 Our results suggest that the rising atmospheric CO2 might have

365

contributed to this process through stimulating plant growth and H+ release from plants.19,48,49

366

The lysimeter system employed in our experiment optimizes the leaching of cations from soil

367

and may overestimate the short-term impact. Yet, CO2-enhancement of cations in soil solutions

368

has been shown in the deep soils of a subtropical forest,16 which may facilitate cation losses in

369

tropical and subtropical regions where nitrogen input (either deposition or fertilization) is high.

370

In a previous microcosm study where leaching was minimized, no significant CO2 effects on soil

371

pH were observed,19 suggesting that losses of cations and NO3- were the key leading to soil

372

acidification. Also, the N input rate (at 62.5 kg N ha-1) used in our microcosm experiment was at

373

the low end for agricultural soils and is likely to increase in many tropical and subtropical

374

regions.50 More importantly, the effect on cation losses and acidity accumulates over time. It

375

magnifies over the long term as stimulated assimilation of cations including Ca2+, Mg2+, and

376

NH4+ by plant biomass under eCO2 increases the removal of base cations due to crop harvest.51

377

Taken together, these results may permit valid inferences about the interactive effects of eCO2

378

and Nr on soil acidity over time.

379

Our results may have some major implications for the N management. Marked soil pH

380

decrease under high NH4+-N inputs and eCO2 (Figure 2b) is particularly alarming because Al

381

toxicity can quickly increase when soil pH decreases below 5.0.13,21,22 Higher Al concentrations

382

under these treatments (Figure S6) provided direct evidence of increased Al solubility. The

383

buffering mechanisms for soil pH differ at different soil pH: when soil pH is above 5.0, soils are

384

buffered by base cations; when soil pH falls below 4.5, soils are buffered by Al3+ and cations 17 ACS Paragon Plus Environment


385

play a minor role as they are mostly depleted.13, 24 In acidic soils with a pH less than 5.0, Al3+ is

386

solubilized into soil solution and leads to the displacement of other cations, resulting in decreases

387

in the storage and availability of base cations.52 Consequently, high Al3+, in combination with

388

base cation deficiency, negatively affect root growth and function, leading to a decrease in

389

nutrient uptake and crop health and production.52,53 Therefore, maintaining soil pH above 5.0 is

390

critically important for crop production and cations play a major role around the pH level.

391

Agricultural soils in the humid subtropics and tropics (Oxisols in South America and Africa or

392

Ultisols in Southeast Asia and Southeast US) (USDA–NRCS 2005) have low soil pH and cation

393

contents, and are likely most vulnerable to cation losses. Much of our knowledge on N dynamics

394

and eCO2 effect is from the temperate world,13,50 preventing any generalization about the tropics

395

and/or other areas where the most dramatic increases in Nr will occur over the next few

396

decades.54-56 Our results suggest that high N inputs under a rising CO2 climate may exacerbate

397

chemical constraints on crop productivity in acidic soils, raising new challenges for food

398

production and quality.57 Also, liming is the most effective approach amending soil acidity for

399

agricultural soils.25 However, because lime materials are often physically unavailable and/or

400

financially too costly, farmers have few other options to amend soil acidity, highlighting the

401

urgency to identify the alternative N management regimes that are practically feasible and are

402

conducive to sustaining the productivity.

403 404

ASSOCIATED CONTENT

405 406

Supporting Information

407

The following Supporting Information is available for this article: 18 ACS Paragon Plus Environment

Page 18 of 31

Page 19 of 31

408


Six figures and seven tables.

409 410

AUTHOR INFORMATION

411 412

Corresponding Author

413

*Phone: 1-919-515-2097; e-mail: [email protected]

414

Author Contributions

415

The manuscript was written through contributions of all authors. All authors have given approval

416

to the final version of the manuscript. &These authors contributed equally.

417

Notes

418

The authors declare no competing financial interest.

419 420

ACKNOWLEDGMENTS

421 422

We thank D. Coleman and Y. Luo for valuable comments, and J. Barton, W. Pursley, J. Wang, Y.

423

Zhang, and E. Silva for technical assistance. L.Z., Y.W. and Y.Q were primarily supported by

424

fellowships from China Scholarship Council. The field experiment was primarily supported by

425

U.S. Department of Agriculture (USDA)–Agricultural Research Service Plant Science Research

426

Unit (Raleigh, NC) and the microcosm experiment was supported in part by CALS, NCSU and a

427

USDA grant to S.H. (2009-35101-05351).

428 429

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430 19 ACS Paragon Plus Environment


431 432 433 434

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FIGURES

16

(a)

12

Ca 2+

Ca 2+ (mg L -1 )

14

10 8 6

(mg 10 cm -2 2 weeks-1 )

613

Page 28 of 31

1000

4

800 600 400 200

(b)

6

4

(mg 10 cm -2 2 weeks-1 )

0

Mg 2+

Mg 2+ (mg L -1 )

8

Control CO2 O3 CO2+O3

1400 (c) 1200

400

(d)

300 200 100

2 Control CO2

O3

0

CO2+O3

11/2008

614

03/2009

07/2009

Month/Year

615

Figure 1. The impact of elevated CO2 on cations in soil solutions in the field experiment. (a) Soil

616

Ca2+ and (b) Mg2+ in lysimeter solutions in 2007. (c) Soil Ca2+ and (d) Mg2+ in the PRS probes in

617

the year 2008-2009. Treatments include ambient CO2 (Control), elevated CO2 (CO2), elevated O3

618

(O3), and combinations of elevated CO2 and O3 (CO2+O3). Data shown are mean ± SE (n=4).

619 620 621 622 623 624 625


Page 29 of 31


5.6

6.3

(a)

Ambient CO2

6.0

5.4

Elevated CO2

5.7

5.2

Soil pH

Soil pH

(b)

5.0

5.4 5.1

4.8 4.8 4.6 Control

CO2

O3

CO2+O3

Low

High

NH4+

626

Low

High

NO3-

627

Figure 2. Soil pH responses to atmospheric CO2 enrichment in the field experiment in 2009 (a).

628

Treatments include ambient CO2 (Control), elevated CO2 (CO2), elevated O3 (O3), and

629

combinations of elevated CO2 and O3 (CO2+O3). And soil pH responses to atmospheric CO2

630

enrichment and reactive N inputs in the microcosm experiment (b). Data shown are mean ± SE

631

(n=4).

632



(a)

aCO2 low NH4 aCO2 low NO3

Ca2+ (g m-2)

10

eCO2 low NH4

8

eCO2 low NO3

10

+

(c)

-

8

-

6 4

0 4

eCO2 high NH4

6

eCO2 high NO3

+ -

4

0 4 (d)

(b) 3

Mg2+ (g m-2)

3

Mg2+ (g m-2)

aCO2 high NO3

+

2

2

2

1

2

1

0

0 44

633

aCO2 high NH4

+

Ca2+ (g m-2)

12

Page 30 of 31

69

97

124

158

44

Days after germination

69

97

124

158

Days after germination

634

Figure 3. Cumulative soil leachate cations as affected by CO2 concentrations and N species in

635

the microcosm study. (a) Ca2+ and (b) Mg2+ in soil leachates under the low N level. (c) Ca2+ and

636

(d) Mg2+ in soil leachates under the high N level. Soil leachates were collected using mini-

637

lysimeters: at ambient (dashed line) and elevated CO2 (solid line). Data shown are mean ± SE

638

(n=4).

639 640 641 642


Page 31 of 31


643 644

Figure 4. A unifying framework of plant-mediated proton (H+) production under elevated CO2

645

and different N species. Solid lines indicate positive effects on plant/microbial proton production,

646

but a dashed line indicates a negative effect on proton production. Plant NO3- uptake increases

647

plant excretion of hydroxyl ions (OH-) to maintain cation-anion balance, partially offsetting H+

648

generation.


Atmospheric CO2 Enrichment and Reactive Nitrogen Inputs

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