REGULAR ARTICLE

Potential impact of CO2 leakage from Carbon Captureand Storage (CCS) systems on growth and yield in maize

Manal Al-Traboulsi & Sofie Sjögersten &

Jeremy Colls & Michael Steven & Colin Black

Received: 5 January 2012 /Accepted: 18 July 2012 /Published online: 31 July 2012# Springer Science+Business Media B.V. 2012

AbstractAims Anthropogenic release of CO2 is an importantfactor in the continuing rise in mean global tempera-ture. Carbon capture and storage (CCS) offers a prom-ising technology to capture and sequester CO2 in deepgeological reservoirs. In view of the possible impact ofleakage from CCS systems on vegetation, we exam-ined the effects of elevated soil [CO2] on growth andyield in Zea mays L.Methods Maize was exposed to elevated soil [CO2] byinjecting CO2 at controlled rates using a purpose-designed field exposure facility.Results Measurements of soil [CO2] and [O2] revealeda strong negative correlation. Plants in a 40–90 cmdiameter area centred on the injection point showedreduced growth and progressive development of se-vere stress symptoms during the gassing period. Allabove-ground vegetative (shoot, stem and leaf weightplant-1, chlorophyll content) and reproductive growthvariables examined (mature cob and seed numbers

plant-1) were negatively correlated with soil [CO2]and positively correlated with soil [O2]. Plants ex-posed to the highest [CO2] produced adventitiousroots, possibly as an adaptive response to hypoxic soilconditions.Conclusions Leakage from CCS transport or storagesites may have strong localised negative impacts onsurface vegetation, the extent of which differs greatlybetween species.

Keywords Carbon capture and storage (CCS) . Cropperformance . Elevated soil CO2

.Maize . Zea mays L.

Introduction

Increasing atmospheric concentrations of carbon diox-ide [CO2] and other greenhouse gases such as methaneand nitrous oxide are primary drivers of the predictedincreases in global surface temperature and associatedclimate change (IPCC 2007). Atmospheric [CO2] hasincreased at a rate of 1.9 %yr−1 to the current level ofc. 387 ppm, compared to 280 ppm before the indus-trial revolution (IPCC 2007). Carbon capture and stor-age (CCS) technology has been advocated as aneffective option for mitigating climate change as itwould reduce CO2 emissions whilst allowing contin-ued use of fossil fuels (Holloway 2005; Bäckstrand etal. 2011). CCS technology involves capturing andtransporting CO2 emitted from major industrial pointsources to deep geological or oceanic reservoirs where

Plant Soil (2013) 365:267–281DOI 10.1007/s11104-012-1390-5

Responsible Editor: Yong Chao Liang.

M. Al-Traboulsi : S. Sjögersten : J. Colls :C. Black (*)School of Biosciences, University of Nottingham,Sutton Bonington Campus,Loughborough LE12 5RD, UKe-mail: Colin.black@nottingham.ac.uk

M. StevenSchool of Geography, University of Nottingham,University Park,Nottingham NG7 2RD, UK

it can be stored securely for millions of years(Holloway 2001; Steven et al. 2010). It is anticipatedthat in the UK alone, sufficient CCS capacity will beneeded to capture and store CO2 produced by 20–30GW of power generation from fossil fuels in depletedoil and gas reservoirs in the North Sea and East IrishSea by 2030 (CCSA 2011). CCS technology is alreadywell established in North America, where 2,500 km ofpipelines transported 49 million t CO2 yr−1 from an-thropogenic and natural sources in 2002 (ICPP 2005);some transport pipelines in the USA are locatedabove-ground.

The most common concern is that CO2 leakingfrom underground pipelines or storage sites may mi-grate to the land surface (Klusman 2003; Gough andShackley 2005; Amonette and Barr 2010), poten-tially affecting groundwater, soil conditions andplant growth. Such leaks could occur at any stageof the CCS process and might range from abruptleakage following sudden failure of the geologicalstorage cap rock during an earthquake or volcaniceruption to more gradual leakage through fracturesand geological faults (IPCC 2005; Steven et al. 2010).To achieve safe and secure storage, Holloway (2007)recommended that geological characterisation of thestorage site and surrounding areas, simulation ofCO2 injection into the site, and studies of the long-term fate of the stored CO2 should be undertaken beforecommencing injection. Comprehensive studies ofpossible damage caused by leakage to terrestrialecosystems are essential to validate the safety of CCSsystems.

Numerous field and laboratory studies have exam-ined the impact of elevated soil [CO2] on plant growthwith the goal of elucidating responses to the naturalenrichment of CO2 that occurs in flooded or water-logged soil (Vartapetian and Jackson 1997; Smethurstand Shabala 2003; Pociecha et al. 2008), or to examinethe influence of irrigation with CO2-enriched water oncrop yield (Enoch and Olesen 1993; Aguilera et al.2001). Such conditions may provide a natural ana-logue for leakage of CO2 from CCS systems. Animportant response in some species, including maize,to hypoxia caused by flooding or waterlogging is thedevelopment of aerenchyma (Vartapetian and Jackson1997; Gunawardena et al. 2001; Chen et al. 2002;Vodnik et al. 2009; Colmer and Greenway 2011) toaccelerate the transfer of oxygen from the shoot to O2-deficient tissues at the stem base and within roots

(Armstrong 1979; Perata et al. 2011). Prolonged ex-posure to hypoxia is known to reduce shoot biomassand chlorophyll content (Bennicelli et al. 1998;Przywara and Stepniewski 1999), plant height and leafarea (Bragina et al. 2002) and photosynthetic rate,respiration and rooting depth in maize (Przywara andStepniewski 1999).

Understanding of the dynamic influence of abioticstress factors on root growth and functional efficiencyunder field conditions remains incomplete due thedifficulty of studying roots in situ (Norby 1994;Norby and Jackson 2000; Tracy et al. 2011, 2012a,b). Nevertheless, several studies have concluded thatelevated soil [CO2] reduces root elongation and pene-tration to depth (Grable and Danielson 1965; Geisler1965; Przywara and Stepniewski 1999) and influenceslateral root formation (Ranson and Parija 1955; Coultand Vallance 1958) and root respiration (Palta andNobel 1989; Maček et al. 2005; Matsui and Tsuchiya2006) in susceptible species.

There is almost no information regarding the po-tential impact of CO2 leakage from CCS facilities onthe gaseous soil environment and performance of ter-restrial vegetation. However, CO2 injection into soilwas found to reduce above- and below-ground growthin turf composed of mixed grass species (Pierce andSjögersten 2009) and in autumn and spring sown fieldbean crops (V. faba; Al-Traboulsi et al. 2012a, b). Inthe present study, experimentally-induced increases insoil [CO2] were used to simulate the impact of leakagefrom CCS facilities on sweet corn (Z. mays L.) underfield conditions to test the hypotheses that exposure toelevated soil [CO2]: (i) adversely affects plant survival,root and shoot growth and crop yield to an extent relatedto exposure concentration; and (ii) roots are more se-verely affected than shoots due to their direct exposureto hypoxic soil conditions.

Materials and methods

Site description

The study was carried out at the ASGARD (ArtificialSoil Gassing and Response Detection) field exposurefacility at the University of Nottingham SuttonBonington Campus (52.8°N, 1.2°W). ASGARD wasdesigned to expose vegetation to elevated soil [CO2]by injecting CO2 into undisturbed soil at controlled

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rates. The soil was a sandy loam to a depth of 60 cm,where a 20 cm thick gravel layer overlay clay (Ford2006). The study involved eight 2.5×2.5 m plotsseparated by 1 m wide grass walkways. CO2 (BritishOxygen Company, Windleham, UK) was injectedat a rate of 1 Lmin−1 into four plots (gassed plots)through a diffuser located 60 cm below the plotcentre; four ungassed plots were used as controls.This approach was chosen to generate the broadestpossible range of vertical and horizontal soil [CO2]gradients (5–75 %) to represent the full range ofleakage scenarios from CCS facilities and charac-terise the plant growth responses induced; [CO2]was greatest close to the injection point. Gas sup-ply was regulated and recorded using a computersoftware system (TVC, Great Yarmouth, UK) installedin 2006, 3 years before the experiment reported herebegan.

Soil gas measurements

Soil gas concentrations were measured using two ver-tical plastic sampling tubes (19 mm internal diameter)installed vertically to a depth of 30 cm at distances of15 and 70 cm from the centre of each gassed plot; onetube was installed 15 cm from the centre of controlplots. The tubes were sealed at the bottom, but 4.5 mmdiameter perforations near the base allowed gas ex-change with the surrounding soil. A valve at the top ofeach tube allowed soil [CO2] and [O2] to be measureddaily between 16 July and 9 September 2009 (72–127 days after sowing (DAS)) using a GA2000Landfill Gas Analyser (Geotechnical Instruments,Warwickshire, UK).

Barholing measurements of gas dispersion

Barholing measurements were used to map the disper-sion of [CO2] and [O2] in all plots. Each plot was sub-divided into 25 squares, each 50×50 cm in area,before inserting a purpose-designed steel spike (PeterWood & Co Ltd, Sheffield, UK) to a depth of 30 cm atthe corners of each square. The GA2000 probe wasimmediately inserted into the hole left after removingthe spike before recording [CO2]. Mean [CO2] for allcorners of each square was calculated and displayed ascontour maps using a grid-based graphics program,Surfer 07 (Golden Software Inc, Golden Co, USA).Measurements at the ASGARD site in 2006 showed a

strong negative linear correlation between soil [CO2]and [O2] (R²00.97; Steven and Smith 2010) i.e.:

O2½ � ¼ 20:078� 0:2147 CO2½ � ð1Þ

This equation was used to estimate [O2] from thecorresponding [CO2] values and construct O2 contourmaps for each plot.

Experimental treatments and measurements

A dwarf sweet corn variety (Zea mays L. cv. F1 Swift;Sutton Seeds, Devon, UK) was chosen to avoid lodg-ing and facilitate measurements. Seeds were sown on5 May 2009 in Levington F2S compost in modulartrays and germinated in a glasshouse; seedling emer-gence began 5 days later. The seedlings were placedoutside during the day from 19 May 2009 to hardenoff and transplanted to the field plots on 3 June. Allplots were cultivated manually before applying N:P:Kfertiliser according to local practice (25:5:5; 250 gplot−1). Seedlings were transplanted to provide fiverows per plot, each containing 10 plants, to give 50plants plot−1. Rows were spaced at 50 cm intervals andspacing within rows was 25 cm. CO2 injection beganon 16 July 2009 (72 DAS) to ensure the plants werewell established as exposure to elevated soil [CO2]from the time of sowing was found to inhibit germi-nation and seedling establishment in autumn-sownfield bean (V. faba L.; Al-Traboulsi et al. 2012a).

Plant height, leaf chlorophyll content and leaf, tillerand cob number plant−1 were recorded regularly forplants located 0, 50 and 100 cm from the centre of allplots. Chlorophyll content was determined using aSPAD 502 Chlorophyll Meter (Minolta, Chicago,USA) for three leaves located near the top, middleand base of each sampled plant. SPAD measurementsat five locations on each sampled leaf were used tocalculate mean values and calibrated against quantita-tive measurements of chlorophyll concentration forleaves for which SPAD values had been determined.Chlorophyll was extracted from 1 g fresh weight ofleaf tissue in 2 mL 80 % acetone using a mortar andpestle; an equivalent mass of tissue was dried at 85 °Cfor 24 h to allow chlorophyll content to be expressed ona dry weight basis. Absorbance of the extracts wasdetermined at wavelengths of 645 and 663 nm(Unicam SP 1,800 spectrophotometer, CambridgeScientific Instruments, UK); chlorophyll concentrations

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were calculated as described by Schaper and Chacko(1991).

At harvest (15 September 2009), all gassed plots weresub-divided into 25 squares, each 50×50 cm in area andthese were individually harvested. Six randomly selected50×50 cm squares were harvested in all control plots.Plant height was measured from the base to the tip of themain stem before dividing plants into leaves, stems,tillers and cobs and determining the fresh weight of eachcomponent. Sub-samples (c. 20 %) of leaves and stemsfrom each square were used to determine fresh and dryweight; cobs were divided into mature, semi-mature andjuvenile categories based on the degree of seed filling;the length and diameter of mature cobs, seed numbermature cob−1 and mature seed number plant−1 weredetermined. All plant components were dried at 100 °Cfor 48 h before determining dry weight.

Mean monthly values for air temperature and rela-tive humidity and total monthly rainfall and irradianceduring the experimental period and the preceding10 year period (1998–2008) were obtained fromSutton Bonington meteorological station.

Soil pH

Soil samples collected from all plots on 7 July 2009,before CO2 injection began, and on 27 October 2009,when the experiment ended, were tested to establisheffects on pH. Samples were collected 5 and 125 cmfrom the centre of all plots at depths of 10, 30 and80 cm. pH (water) was determined using a pH meter(pH 209, HANNA Instruments, Woonsocket, USA).

Root measurements

Minirhizotrons were used to examine rooting charac-teristics non-destructively during the exposure period.On 1 May 2008, two transparent access tubes (5 cmdiameter×125 cm long) were installed at an angle of45° to the soil surface to a depth of 70 cm in all gassedplots; one tube was installed in each control plot.Tubes in the gassed plots were inserted in two orien-tations; tube GA entered the soil 100 cm from the plotcentre, where soil [CO2] was relatively low, andsloped perpendicularly to the plant rows downwardstowards the plot centre, where [CO2] was greatest(Fig. 1a). Tube GB entered the soil 15 cm from theplot centre, where soil [CO2] was greatest and slopeddownwards parallel to the plant rows, towards the

edge of the plot, where [CO2] was lowest. Soil[CO2] therefore increased with depth for orientationGA but decreased with depth for orientation GB. Rootimages were recorded using a BTC-2 minirhizotronmicrovideo system (Bartz Technology Inc., SantaBarbara, CA, USA) inserted into the access tubes tocapture roots growing against their outer surface.Images recorded for all tubes (12.5 mm vertical×18 mm horizontal, area 2.43 cm²) on eight dates be-tween July and September 2009 were digitised usingthe BTC I-CAP Image Capture System. 63 imageswere analysed for each tube and sampling date, givinga total of 6,048 images (63 depths×12 tubes×8 dates).Images for the 0–10, 10–20, 20–30, 30–40, 40–50, 50–60 and 60–70 cm depth intervals were analysed usingthe RooTracker, V2.0.3 software package for root imageanalysis (Dave Tremmel, Duke University, Durham,NC, USA) to determine main and lateral root numbers,root length and root diameters for all images.

Statistical analysis

The effects of soil CO2 enrichment and location withinplots on plant height, chlorophyll content and tillerand cob numbers were tested by repeated measuresANOVA. Soil [CO2] was the main effect (independentfactor) with two levels, gassed and control, whilelocation (2, 50, 100 cm from the plot centre) and datewere analysed as repeated measures. Interactions weretested i.e. CO2*location, CO2*date, date*location,CO2*date*location. One-way ANOVA was used fordata obtained at harvest including stem, leaf, shoot andcob fresh and dry weights, tiller number plant−1, cobnumber plant−1 and seed number plant−1 from maturecobs. [CO2] was the main effect factor with two levels,control and gassed. Relationships between shoot dryweight plant−1 and soil [CO2] and [O2] provided bythe barholing measurements were tested for signifi-cance and linear relationships fitted. Effects of CO2

enrichment and soil depth on root number, length anddiameter were tested using repeated measures ANOVAwith [CO2] as the main effect (independent factor) withtwo levels; soil depth and date were analysed as repeatedmeasures. Interactions including CO2*depth, CO2*date,date*depth and CO2*date*depth were also tested. Leastsignificant difference (LSD) was calculated to aid com-parison between treatment effects and significance wasaccepted at P≤0.05. Soil pH values at the centre andedge of all plots were analysed by three-way ANOVA,

270 Plant Soil (2013) 365:267–281

with [CO2] (control and gassed), depth (10, 30, 80 cm)and date (before and after gassing) as independent var-iables. All analyses were performed using SPSS 16.0.

Results

Climatic conditions

Mean daily air temperature and relative humidity dur-ing the experimental period were comparable to valuesfor the preceding 10 year period (Table 1). Monthly

rainfall was much lower than the 10 year mean in Mayand September and higher in July, but total rainfall wassimilar to the long-term mean (257.6 vs. 279.5 mm).Total monthly irradiance was greater than the 10 yearmean for all months, giving a slightly higher cumulativetotal than the corresponding 10 year mean (2,463 vs.2,293 MJ m−2).

Soil CO2 and O2 concentrations

Mean soil [CO2] 15 cm from the centre of gassed plotswas much higher than at 70 cm during the injection

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Fig. 1 Spatial variation in(a) mean CO2 and mean O2

(b) concentrations at a depthof 30 cm in the CO2-enriched plots (n04). X andY axes represent total plotarea (2.5×2.5 m). N denotesNorth. The horizontal blackline and solid and dashedwhite line entering the plotfrom the North represent theCO2 supply line; white andstippled stars represent thesampling points located 15and 70 cm from the plotcentre; vertical hatched andhorizontal white arrows re-spectively represent the ori-entations of the Bartzminirhizotron tubes GA

and GB

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period (F0309; P<0.001) and values at both locationswere greater than in control plots (F0912; P<0.001;Fig. 1a). Conversely, [O2] was much lower 15 cmfrom the centre of the gassed plots than at 70 cm(F0260; P<0.001) and values for both locations werelower than in control plots (F0662; P<0.001;Fig. 1b). The concentric decline in soil [CO2] from aseasonal mean of 71 % close to the injection point to9.6 % near the plot margins was reflected by anincrease in soil [O2] from 5 % to 19.3 %, closelycomparable to the mean for control plots (19.4 %).

Soil pH

Soil pH at depths of 10 and 30 cm in the centre of theplots prior to the injection period increased with depthand was lower in the gassed (5.8 and 7.0 respectively)than in the control treatment (6.8 and 7.4; F03.60; P<0.001), reflecting the influence of soil gassing duringthe previous 3 years. No significant change in soil pHoccurred during the experimental period.

Plant growth

Shoot, stem and leaf dry weight plant−1, leaf chloro-phyll content, mature cob number plant−1 and matureseed number plant−1 were all lower in the gassed plots(Tables 2 and 3; Fig. 2). A zone of plants showingvisible stress symptoms developed close to the CO2

injection point in the gassed plots and expanded to 40–90 cm in diameter by 126 DAS. Chlorosis becameapparent 6 day after CO2 injection began and wasfollowed by premature senescence, leaf abscissionand plant death. No visible stress symptoms or mor-tality occurred in control plots.

Plant survival decreased by 25 % at the centre ofthe gassed plots after 35 day of exposure but thereafter

Table 1 Mean daily air temperature and relative humidity, total monthly rainfall and total irradiance during the 2009 growing seasonand mean values for the preceding 10 year period (1998/2008). Standard errors of the mean are shown for long term mean values

Month Air temperature (°C) Relative humidity (%) Rainfall (mm) Irradiance (MJ m−2)

1998/2008 2009 1998/2008 2009 1998/2008 2009 1998/2008 2009

May 11.8±0.2 12.3±0.4 81±1.3 82.6±1.7 56.8±7.2 34.4 501.1±9.6 563.0

June 15.1±0.2 15.0±0.5 79±1.4 82.3±1.7 54.4±13.4 60.6 534.2±9.9 583.5

July 16.6±0.5 16.2±0.3 80±1.4 84.3±1.4 58.2±9.9 87.4 514.8±19.1 531.9

August 16.7±0.1 16.9±0.3 81±1.4 82.7±1.4 64.1±18.4 58.2 440.2±9.3 449.8

September 14.5±0.3 14.1±0.2 83±1.6 83.1±0.8 46.0±6.4 17.0 303.0±10.3 333.6

Table 2 Summary of two−way repeated measures ANOVA todetermine the effect of elevated soil [CO2] on plant height, tillernumber plant−1, cob number plant−1 and leaf chlorophyll content

Variable Source F P

Plant height CO2 3.2 0.12

Date 1.3 <0.001

Location 1.3 0.28

CO2*Date 7.5 <0.05

CO2*Location 0.4 0.69

Date*Location 2.0 0.13

CO2*Date*Location 3.2 <0.05

Tiller number plant−1 CO2 0.0 0.10

Date 21.6 <0.001

Location 0.9 0.44

CO2*Date 1.2 0.28

CO2*Location 2.4 0.05

Date*Location 1.7 <0.05

CO2*Date*Location 2.8 <0.001

Total cob number plant-1 CO2 7.2 <0.05

Date 62.3 <0.001

Location 3.9 <0.05

CO2*Date 6.3 <0.001

CO2*Location 2.3 0.10

Date*Location 1.3 0.23

CO2*Date*Location 1.5 0.16

Chlorophyll content CO2 10.4 <0.05

Date 22.2 <0.001

Location 6.0 <0.05

CO2*Date 8.3 <0.05

CO2*Location 7.5 <0.05

Date*Location 4.0 <0.001

CO2*Date*Location 4.9 <0.001

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showed no further decline. By contrast, all plantslocated 50 and 100 cm from plot centre survived andcontinued to grow until harvest. The development ofsevere chlorosis prior to leaf abscission was reflectedby the progressive decline in chlorophyll content inthe gassed plots (Fig. 2a); this was much greater closeto the centre of gassed plots than at a distance of100 cm between 78 and 121 DAS. No equivalentdecline occurred in control plants. The sharp decreasein chlorophyll content and leaf abscission near thecentre of the gassed plots was not reflected by thetimecourses for tiller number plant−1, which werecomparable to control plants (Fig. 2b). Tiller numberplant−1 increased rapidly after 70 DAS in both treat-ments, but declined after cob formation began at 77DAS (Fig. 2c). Cob number plant−1 continued to in-crease in control plots but stabilised or decreased after90 DAS at distances of 0 and 50 cm from the centre ofthe gassed plots (Fig. 2c).

Growth parameters at harvest

Shoot, stem and leaf dry weight plant−1, mature cobnumber plant−1 and seed number plant−1 from maturecobs were greater in control than in gassed plants,which performed best near the plot margins and de-clined towards the centre (Fig. 3; Table 3). Only tillernumber plant−1, semi-mature cob number plant−1 andjuvenile cob number plant−1 did not differ significant-ly between treatments. Thus, plants which experiencedthe lowest [CO2] (9–20 %) and highest [O2] (17–19.5 %) performed better over a range of vegetativeand reproductive growth variables than those locatedclose to the injection point. Plants near the edge of the

gassed plots nevertheless showed large growth reduc-tions compared to control plants. Shoot dry weightplant−1 showed a strong negative linear correlationwith [CO2] (F096.8; P<0.001; Fig. 4a) and positivecorrelation with [O2] (F076.9; P<0.001; Fig. 4b).Similar effects were apparent for all growth variables.

Root growth

Root number was the only rooting characteristic to besignificantly affected by elevated soil [CO2] (P00.05),and none of the interactions involving CO2 was sig-nificant (Table 4). Main root number was greatest inthe 10–20 horizon of both treatments (Fig. 5a; Table 4)and generally declined with depth. Root length, diam-eter and surface area varied between depths and datesin both treatments but were unaffected by CO2 treat-ment (Table 4). The number and length of main rootsin the 0–10 cm horizon of the gassed plots declinedbetween 64 and 100 DAS (30 day of exposure), butincreased again by 126 DAS (56 day of exposure;Fig. 5); this effect was more pronounced for the GB

than the GA orientation. Main roots extended morerapidly and reached a greater maximum depth of70 cm by 100 DAS in control plants than in bothorientations in the gassed plots, for which maximumdepth was 60 cm (Fig. 5). Maximum rooting depththen declined to 50 cm by 126 DAS for the GB

orientation but remained at 60 cm for the GA orienta-tion. Lateral root number and length were consistentlylower than the corresponding values for main roots forall depths in both treatments, and were greater forcontrol plants than for both orientations in the gassedplots.

Table 3 ANOVA summary for growth characteristics at final harvest (mean±SEM) for plants in control and elevated soil [CO2]treatments (n04). Percentage changes for gassed plants relative to control plants are shown; ↑ and ↓ denote increases and decreases

Parameter Control Gassed F P Change (%)

Shoot dry weight (g plant−1) 342±7.1 235±6.09 32.5 <0.001 31.2↓

Stem dry weight (g plant−1) 24.7±0.7 19.5±0.8 21.9 <0.001 21.0↓

Leaf dry weight (g plant−1) 8.2±0.3 6.2±0.26 21.1 <0.001 24.3↓

Tiller number plant−1 0.66±0.13 0.77±0.07 0.5 ns 16.6↑

Seed number plant−1 467±18.1 376±18.8 12.0 <0.001 19.4↓

Mature cob number plant−1 1.0±0.00 0.75±0.04 33.4 <0.001 25.0↓

Semi-mature cob number plant−1 0.58±0.08 0.48±0.05 0.9 ns 17.2↓

Juvenile cob number plant−1 1.8±0.11 1.6±0.11 1.3 ns 11.1↓

Plant Soil (2013) 365:267–281 273

Discussion

The marked reduction in soil [O2] caused by CO2

injection (Fig. 1b) suggests direct displacement of O2

similar to that observed in previous studies (Vodnik etal. 2006; Steven and Smith 2010). The mean [CO2] of

71 % near the centre of gassed plots (Fig. 1a) greatlyexceeds typical values for well aerated soil (0.5–2 %;Russell 1973), while the corresponding [O2] values(Fig. 1b) were much lower than in well aerated soil(c. 20 %; Good and Patrick 1987; Bewley and Black1994). The gas dispersal patterns revealed that CO2

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migrated radially from the injection point to provideapproximately concentric reciprocal gradients for[CO2] and [O2] between the plot centre and margins.The roots of plants in the gassed plots were not entirelydeprived of O2 as the minimum mean concentration inthe soil atmosphere was 5 %, but nevertheless experi-enced hypoxia. The detrimental effect of gassing onmaize was proportionately greater below-ground as rootnumbers in the surface horizons were reduced by c.60 %, whereas the corresponding reduction in shootbiomass was c. 30 %. This observation suggests thatthe adverse effect of elevated soil [CO2] on shootgrowth and yield at harvest was a direct consequenceof the reduced size and impaired functioning of the rootsystem. These responses are in marked contrast to fieldbean (Vicia faba L.), in which responses to a similar soilgaseous environment imposed using the ASGARD ex-posure system were greater in the shoots than in theroots (Al-Traboulsi et al. 2012b). This contrast suggeststhat responses to leakage from CCS transport and

storage systems may differ greatly between species.Previous studies indicate that timing of exposure is alsocritical in determining the severity of the effects inducedas exposure from the time of sowing prevented seedlingemergence in V. faba in a large area surrounding theinjection point (Al-Traboulsi et al. 2012a).

Although soil pH near the centre of the plots wasslightly lower in gassed than in control plots (5.8 and7.0 at depths of 10 and 30 cm vs. 6.8 and 7.4 respec-tively) prior to the injection period, this is highlyunlikely to have impacted on crop performance as rootgrowth in maize is most rapid at soil pH values be-tween 5.5 and 6.5 (Islam et al. 1980), and ceases onlywhen pH is <3.5 (Yan et al. 1992).

Visible stress symptoms expressed in the form ofyellowing of the older leaves caused by chlorophylldegradation (Fig. 2a) followed by premature senes-cence and abscission initially appeared near the CO2

injection point before spreading outwards towards theplot margin; a similar pattern was observed for plant

a b

c d

Fig. 3 Spatial variation in a shoot dry weight plant−1, b leaf dry weight plant−1, c mature cob number plant−1 and d seed numberplant−1 in the gassed plots (n04). X and Y axes represent total plot area (2.5×2.5 m)

Plant Soil (2013) 365:267–281 275

mortality, reflecting the concentric variation in the soilgaseous environment (Fig. 1). These effects are con-sistent with the premature leaf senescence that is ofteninduced by soil-borne stress factors such as hypoxiaand anoxia (Dong et al. 1983; Vartapetian and Jackson1997); several studies have reported decreases in chlo-rophyll content in maize in response to increased soil[CO2] or reduced [O2] (Bennicelli et al. 1998;Przywara and Stepniewski 1999; Noomen andSkidmore 2009).

The pattern of gas concentrations in the gassedplots was reflected by the growth of surviving plants(Table 2; Figs. 2, 3 and 4). Thus, soil [CO2] of 55–75 % was lethal and 20–55 % [CO2] greatly reducedgrowth, whereas plants exposed to 9–20 % [CO2]showed no visible stress symptoms. These findingssubstantiate previous reports that naturally elevatedsoil [CO2] at Mammoth Mountain, California, inducedyellowing of leaves and caused trees to die by depriv-ing their roots of O2 (McGee and Gerlach 1998; Sorey

et al. 2000). In the present study, all above-groundvegetative and reproductive variables examined werenegatively correlated with soil [CO2] and positivelycorrelated with [O2] (Fig. 3); similar results have beenreported for maize grown at a site naturally enrichedwith CO2 (Vodnik et al. 2005). Moreover, hypoxic soilconditions induced by waterlogging reduced pod num-ber plant−1 and seed number plant−1 in winter oilseedrape (Brassica napus L.; Zhou and Lin 1995) andmungbean (Vigna radiata (L.) R. Wilczek; Laosuwanet al. 1994). The sharp decline in chlorophyll contentand the parallel decrease in cob number plant−1 to-wards the centre of the gassed plots (Fig. 2a, c) sug-gests that premature leaf senescence induced by theadverse soil gaseous environment severely restrictedassimilate supplies to support the initiation and growthof cobs as the timecourses for tiller number plant−1

were comparable in both control and gassed treat-ments (Fig. 2b).

The severity of the adverse effects on shoot growthand yield at harvest was much less than observed infield bean (V. faba) using the same exposure facilityand CO2 injection rate (Al-Traboulsi et al. 2012b), andwas more closely comparable to other graminoid spe-cies. For example, Pierce and Sjögersten (2009)reported that exposure of turf containing a mixture ofLolium perenne, Festuca rubra and Phleum pratenseto elevated soil [CO2] using the ASGARD facilityreduced above- and below-ground biomass by 21and 12 %, respectively after 10 weeks of exposure.By contrast, V. faba showed much greater plant mor-tality (75 %) than maize near the centre of the gassedplots and greater decreases in above-ground vegetative(49 %) and reproductive growth in terms of pod andseed number plant-1, which were reduced by 42 and46 % respectively (Al-Traboulsi et al. 2012b). Thiscontrast suggests that susceptibility to elevated soil[CO2] and severely depleted [O2] may vary greatlybetween graminoid and leguminous species.

The greater sensitivity of V. faba is likely to origi-nate from the absence of appropriate physiological andanatomical adaptations to survive hypoxic conditions(El-Beltagy and Hall 1974; Walter et al. 2004). Bycontrast, production of adventitious roots and forma-tion of aerenchyma are common responses of maize tohypoxia (Jackson et al. 1985; Atwell et al. 1988; He etal. 1994; Gunawardena et al. 2001; Mano et al. 2006;Colmer and Greenway 2011; Postma and Lynch2011). Roots experiencing the highest soil [CO2] and

y = 13.939x + 41.158R²= 0.40

0

50

100

150

200

250

300

350

400

450

500

0 5 10 15 20 25

Sh

oo

td

ryw

eig

ht(

gp

lan

t¯¹)

O2 concentration (%)

y = 3.3229x + 326.45R²= 0.46

0

50

100

150

200

250

300

350

400

450

500

0 20 40 60 80 100

Sh

oo

td

ryw

eig

ht(

gp

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CO2 concentration (%)

Gassed

Control

a

b

Fig. 4 Correlation between shoot dry weight at harvest and amean soil CO2 and b O2 concentration. Regression equationsand R2 values are shown

276 Plant Soil (2013) 365:267–281

lowest [O2] (GB orientation in the gassed plots;Fig. 1a) showed non-significant increases in adventi-tious root number and length in the surface soil hori-zons compared to plants experiencing less extremeconditions (GA orientation; Fig. 5a, b). Vodnik et al.(2009) also observed the formation of adventitiousroots when maize plants were exposed to hypoxia,while Drew et al. (1979) concluded that reduction ofsoil [O2] to 1 % promoted accumulation of ethyleneand production of adventitious roots containing aeren-chyma to enhance oxygen supplies.

It is therefore possible that formation of aerenchy-ma in response to hypoxia (Bailey-Serres andVoesenek 2008; Perata et al. 2011) in adventitious

roots produced during the injection period enabledaerobic metabolism to continue. This hypothesis mayprovide an explanation for the much greater resistanceof Z. mays to simulated leakage from CCS systemscompared to less tolerant species such as Vicia faba(Al-Traboulsi et al. 2012b). The reductions in rootnumber and maximum rooting depth in the gassedplots (Fig. 5) substantiate previous reports that deple-tion of soil [O2] and increased soil [CO2] reduce rootgrowth (Bengough et al. 2006; Visser and Pierik 2007)because increased ethylene biosynthesis in the celldivision and elongation zones under hypoxic condi-tions inhibits root elongation (Geisler-Lee et al. 2010).Ethylene biosynthesis is likely to have been greater inthe GB than in the GA orientation in gassed plots dueto the more severely hypoxic rooting environment,perhaps explaining the greater reduction of root elon-gation in view of the inhibitory influence of this stressplant growth regulator (Gallie et al. 2009). As chloro-sis, senescence and abscission of the older leavesincreased rapidly with time in the gassed treatment,reduced assimilate supply to the roots is likely to havecontributed to the observed reductions in root numberand rooting depth, as roots receive most of their as-similate from these leaves (Crisswell et al. 1974). Thesmaller root system in the gassed treatment may inturn have reduced O2 requirements for aerobic metab-olism (Geisler-Lee et al. 2010). However, the questionremains of whether the detrimental effects on plantsurvival, growth and yield in the gassed treatmentoriginated primarily from the potentially damaginginfluence of elevated soil [CO2] or the consequentdepletion of [O2].

In the context of leakage from CCS systems, thereare three scenarios, leakage from above-ground pipe-lines, buried pipelines or deep stores. The presentstudy is not relevant to leakage from above-groundpipelines as such leaks would not affect soil [CO2],although Mazzoldi et al. (2008) found that such leaksformed patches of frozen CO2, creating a secondaryhazard as they sublime. It is estimated that 1,300–2,000 km of new CCS pipelines will be needed inthe UK by 2030 (CCSA 2011). Although UK regula-tions may require these pipelines to be buried forreasons of aesthetics and security, they may be nodeeper than 1 m for financial reasons, potentiallyexposing vegetation to greatly increased soil [CO2]in the event of leakage. The present and previousstudies (Al-Traboulsi et al. 2012a, b) suggest that

Table 4 ANOVA summary of rooting characteristics in thecontrol and elevated soil [CO2] treatments for eight dates be-tween 62 and 127 days after sowing (n04)

Variable Source F P

Root number CO2 4.82 0.05

Date 3.43 0.05

Date*CO2 1.70 0.14

Depth 20.5 <0.001

Depth*CO2 1.40 0.25

Date*Depth 2.68 <0.001

Date*Depth*CO2 0.70 0.80

Root length CO2 1.12 0.38

Date 7.18 <0.001

Date*CO2 1.60 0.13

Depth 16.9 <0.001

Depth*CO2 1.41 0.20

Date*Depth 1.39 0.13

Date*Depth*CO2 0.67 0.91

Root diameter CO2 0.32 0.73

Date 5.21 ≤0.001Date*CO2 1.31 0.25

Depth 11.0 <0.001

Depth*CO2 1.23 0.29

Date*Depth 1.58 0.05

Date*Depth*CO2 1.00 0.47

Root surface area CO2 0.001 0.99

Date 2.31 ≤0.05Date*CO2 0.72 0.72

Depth 2.87 <0.05

Depth*CO2 1.19 0.32

Date*Depth 1.09 0.37

Date*Depth*CO2 0.94 0.55

Plant Soil (2013) 365:267–281 277

crops can tolerate soil [CO2] <20 %, but that lethaleffects are induced when [CO2] exceeds 55 %. Leaksfrom underground pipelines or deep storage might bothbe expected to generate values within this range.However, as damage caused by leaks from buried CCSpipelines will be confined to areas within 1–2 m of thepipeline, crop yield losses would be insignificant rela-tive to the total area of arable land in the UK andelsewhere in northern Europe, and also relative to thecost of installing and maintaining CCS pipelines. Amore pertinent implication of our findings is the poten-tial application of the responses of terrestrial vegetationto identify leaks from underground CCS systems. Leakdetection is critical for the viability of CCS schemes interms of accounting, safety and public acceptance.Remote sensing techniques focusing on the stress

responses of terrestrial vegetation have been shown tobe effective in detecting leaks from natural gas pipelines(Smith 2002), and there is evidence that this approachmay also be feasible for CO2 (Steven et al. 2010).

In conclusion, prolonged below-ground release ofCO2 caused plant mortality and increasingly reducedthe vegetative and reproductive growth of survivingplants towards the centre of the gassed plots. Beneficialeffects on the productivity of vegetation induced by in-creased atmospheric [CO2] are likely to be negligible dueto turbulent transfer of emitted CO2 to the bulk atmo-sphere, except perhaps in tall, dense vegetation commu-nities such as forests where understorey windspeed islow; indeed, measurements during subsequent experi-ments at the ASGARD site showed no detectable effecton atmospheric [CO2] (unpublished results). Maize

Fig. 5 a Mean total number and b total length of main andlateral roots in control plots (C) and the GA and GB orientationsin the gassed plots for depth intervals of 0–10, 10–20, 20–30,30–40, 40–50, 50–60 and 60–70 cm at (i) 64, (ii) 100 and (iii)126 days after sowing (DAS). The orientations of tubes GA and

GB and mean soil [CO2] and [O2] concentrations are shown inFig. 1. Single standard errors of the mean are shown (n04).Least significant differences (LSD) are shown for comparingtreatments

278 Plant Soil (2013) 365:267–281

exhibited much greater tolerance of simulated leakagefrom CCS transport and storage facilities than Vicia faba(Al-Traboulsi et al. 2012b). This contrast suggests thatsuch leakage may induce variable, potentially severe butspatially contained damage to terrestrial vegetationdepending on the species involved, providing a poten-tially important tool for assessing the integrity of CCSsystems.

Acknowledgments This research was supported by a grantfrom the HEFCE (Higher Education Council for England) throughthe University of Nottingham and a PhD scholarship from theLibyan Ministry of Education. We thank Sarah Macintosh, JimCraigon, Sacha Mooney, Mark Meacham, Jayalath De Silva,Matthew Tovey, John Alcock, John Corrie and Darren Hepworthfor professional advice and technical support.

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