Growth and marketable-yield responses of potato to increased CO2 and ozone

Europ. J. Agronomy 17 (2002) 273 /289 www.elsevier.com/locate/eja

Growth and marketable-yield responses of potato to increased CO2 and ozone J. Craigon a,*, A. Fangmeier b, M. Jones c, A. Donnelly a, M. Bindi d, L. De Temmerman e, K. Persson f, K. Ojanpera g b

a School of Biosciences, University of Nottingham, Sutton Bonington Campus, Leicester LE12 5RD, Loughbrough, UK Institute for Landscape and Plant Ecology, University of Hohenheim, Schloss Mittelbau (West), D-70599 Stuttgart, Germany c University of Dublin Trinity College (TCD), Dublin, Ireland d Center for Computer Science in Agriculture (CeSIA), P. Delle Cascine 18, I-50122 Florence, Italy e Veterinary and Agrochemical Research Centre (VAR), 3080 Tervuren, Belgium f Botanical Institute University of Go¨teborg, Carl Skottsbergs Gata 22 B, SE 413 19 Go¨teborg, Sweden g Resource Management Research, Agricultural Research Centre of Finland, 31600 Jokioinen, Finland

Abstract Central to the CHanging climate and potential Impacts on Potato yield and quality project (CHIP) was the consideration of the potential impacts of ozone and CO2 on growth and yield of future European Potato crops. Potato crops, cv. Bintje, were exposed to ambient or elevated ozone; targeted daily average, 60 nl l
1 for 8 h, and ambient or elevated CO2; targeted 680 ml l
1 averaged over the full growing season, in open top chambers (OTCs) at six European sites in 1998 and 1999, or to elevated CO2 (550 ml l
1) in Free Air Carbon dioxide Enrichment facilities (FACE) at two sites in both years. Some OTC experiments included 550 ml l
1. Above and below ground biomass were measured at two destructive harvests; at maximum leaf area (MLA) and at final-harvest. Final-harvest fresh weight yields of marketable-size tubers,
/35 mm diameter, from ambient conditions ranged from 1 to 12 kg m
2. There was no consistent (P
/0.1) CO2 /O3 interaction for growth or yield variables at either harvest. No consistent effects of ozone were detected at the maximum-leaf-area harvest. However, at final harvest, ozone had reduced both above-ground biomass and tuber dry weight (P B/0.05), particularly of the largest (
/50 mm) size class. These yield losses showed linear relationships both with accumulated ozone exposure; AOT40 expressed as nl l
1 h over 40 nl l
1, and with yields from chambered ambient-ozone treatments (P B/0.05) but, because of partial confounding between the treatment AOT40s and the ambient-ozone yields in the data, the two relationships were not completely independent. Yields from ambient-ozone treatments, however, explained a significant (P B/0.01) amount of the residual variation in ozone effects unexplained by AOT40. When averaged over all experiments, mean dry weights and tuber numbers from both harvests were increased by elevated CO2. Only green leaf number at the MLA harvest was reduced. The CO2 responses varied between sites and years. For marketable-size tubers, this variation was unrelated to variation in ambient-CO2 treatment yields. Yield increases resulting from the 680 ml l
1 and 550 ml l
1 treatments were similar. Thus elevating [CO2] from 550 to 680 ml l
1 was less effective than elevating [CO2] from ambient to 550 ml l
1. On average, CO2 elevation to 680 ml l
1 increased the dry weight of marketable-size tubers by about 17%, which far exceeded the average ozone-induced

* Corresponding author. Tel.: /44-115-9516-252; fax: /44-115-9516-334 E-mail address: [email protected] (J. Craigon). 1161-0301/02/$ - see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 1 1 6 1 - 0 3 0 1 ( 0 2 ) 0 0 0 6 6 - 7

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yield loss of about 5%. The net effect of raising CO2 and O3 concentrations on the European potato crop would be an increase marketable yield. # 2002 Elsevier Science B.V. All rights reserved. Keywords: CO2; Ozone; Potato; Solanum tuberosum L.; Growth; Yield

1. Introduction In terms of the tonnage produced, potato is the second most important crop in Europe after wheat and ranks fourth on a global scale after wheat, rice, and maize (FAO, 1996). It is used for a variety of industrial and food processing applications because of its high starch content. Fresh or stored tubers for direct consumption also form an important component of the human diet throughout much of Europe. Consequently, any environmental change that impacts upon the growth and yield of potato will have implications for European Agriculture. The atmospheric environment is changing throughout Europe. Amongst the ongoing changes are concurrent increases carbon dioxide (CO2) and ozone (O3). Mean atmospheric [CO2] has increased from 280 ml l
1 in pre-industrial times to c. 365 ml l
1 at present, and could exceed 700 ml l
1 by the end of the present century (IPCC, 1996). Tropospheric [O3] has increased substantially during the past 60 years (Anfossi et al., 1991) and is likely to continue increasing at an annual rate of 0.5 /2.5% in the Northern Hemisphere (Ashmore and Bell, 1991; Hertstein et al., 1995; Stockwell et al., 1997). Both gasses have been shown to affect plant growth and productivity. In general, elevated [CO2] results in increased growth and productivity in C3 species (Acock and Allen, 1985; Cure and Acock, 1986; Drake et al., 1997; Murray, 1997), with projected growth and yield increases of c. 30% if [CO2] rise to 700 ml l
1 (Kimball, 1983). Such increases in productivity in response to a doubling of present day [CO2] has been observed in the field (Miglietta et al., 1998) and in controlled environment experiments (Wheeler et al., 1994; Mackowiak and Wheeler, 1996) where potato has been exposed to elevated [CO2] for the entire growing season.

Ozone, both because of its increasing tropospheric concentrations and its damaging effects on plants, is regarded as one of the most important phytotoxic air pollutants (Ashmore and Bell, 1991). Indeed, growth and yield of economicallyimportant crops have been shown to be reduced by both ambient and experimentally-increased [O3] (Clarke et al., 1990): wheat (Fuhrer et al., 1989; Mulholland et al., 1998; Pleijel et al., 1991; Finnan et al., 1998; Ollerenshaw and Lyons, 1999; Donnelly et al., 1999); oil-seed rape (Bosac et al., 1998; Ollerenshaw et al., 1999) and potato (Foster et al., 1983a,b; Pell et al., 1988), though the effects may vary greatly within as well as between species (Barnes et al., 1999; Black et al., 2000). Thus, separate studies exploring the two gasses indicate that increases in the atmospheric concentrations of CO2 and O3 would have opposing effects on potato growth. However, there is little information on their combined effects on potato yields. The effects of simultaneous increases in [CO2] and [O3] may not be additive: ozonedamaged plants may be reduced in their capacity to make use of increased [CO2]; increased [CO2] may reduce O3 impacts through reduced stomatal aperture and/or effects on the supply of photoassimiliate to support repair and defence processes (Polle and Pell, 1999). Previous studies of the interactive effects of elevated [CO2] and [O3] on a number of crops: soybean (Mulchi et al., 1992; Fiscus et al., 1997), radish (Barnes and Pfirrman, 1992) and wheat (Balaguer et al., 1995; McKee et al., 1997; Mulholland et al., 1998; Donnelly et al., 1999) show that the severity of ozone-induced foliar injury is generally reduced under elevated [CO2]. However, the extent of such protection provided by elevated [CO2] varies and can depend upon the degree of stomatal closure induced by elevated [CO2], which differs between taxa (Barnes and Wellburn, 1998), and/or upon the timing and

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duration of ozone exposure (Mulholland et al., 1998; Donnelly et al., 1999; Black et al., 2000). Stomatal behaviour and thus the dose of O3 taken up by plants are highly dependent upon the prevailing meteorological conditions (Pleijel et al., 2002) as are the responses of photosynthesis to elevated [CO2]. Meteorological conditions vary within and between field seasons at the same site and also vary considerably across the potato growing regions of Europe. Therefore, whilst individual experiments can demonstrate the effects of elevated [CO2] and [O3] under a particular set of meteorological and soil conditions (Lawson et al., 2001; Donnelly et al., 2001a; Finnan et al., 2001), data from a range of representative regions are required if the potential effects are to be considered on a European scale. The CHIP project (De Temmerman et al., 2000), in which potatoes were grown under ambient and elevated [CO2] and/or [O3] in seven European countries, was designed to generate such data. In the work we report here, the growth and yield data from these experiments are analysed to determine what impacts the predicted increases in atmospheric [CO2] and [O3] may have on the European potato crop in the future.

2. Materials and methods 2.1. Sites, seasons and seed-stock Experimental potato crops were grown in two field seasons, 1998 and 1999, in seven countries: Belgium (Be); Finland (Fi); Germany (Ge); Ireland (Ir); Italy (It); Sweden (Sw) and the United Kingdom (UK). Details of the prevailing climatic conditions at each experimental site are given by De Temmerman et al. (2002a). Certified seed tubers (Solanum tuberosum cv. Bintje) from a common stock were obtained from the Netherlands in each year and used in all experiments. ‘Bintje’ was selected for this study because it is currently grown throughout mainland Europe, it is of commercial importance for processed food products, and preliminary controlled environment studies (B. Ko¨llner, pers comm.) suggested it may be susceptible to ozone-induced damage.

275

2.2. Experimental design 2.2.1. Open top chamber experiments At six sites: Tervuren (Belgium); Jokioinen (Finland); Giessen (Germany); Carlow (Ireland); Gothenburg (Sweden) and Sutton Bonington (UK), potato crops were grown in transparentwalled Open Top Chambers (OTCs). In Sweden in 1998 the chambers used were 1.24 m diameter / 1.6 m high but larger 3 m diameter /2.4 /2.8 m high chambers were used there in 1999 and in both seasons at the other five sites. To achieve the targetted gas concentrations, O3 and CO2 were added to unfiltered air blown into the OTCs and allowed to exit through the top of the chamber. The additions were controlled on the basis of continuously monitored levels within the chambers. The core Open Top Chamber (OTC) experiment in the CHIP project employed two CO2 concentrations [Ambient and Elevated; season long target 680 ml l
1 24 h daily mean] and two ozone treatments [Ambient and Elevated; season long target 60 nl l
1 8 h daily mean] replicated in a factorial design following a standard experimental protocol. An additional intermediate CO2 level was studied in the UK and Germany to match the target [CO2] (550 ml l
1) used in the CHIP FACE experiments in Germany and Italy. In Ireland, in 1998, the elevated CO2 treatment began on 25 June, 37 days after transferring the plants to the OTCs. No CO2 treatments were applied in Finland in 1998, when an intermediate O3 level was included, nor in Sweden in 1999. Additional charcoal-filtered treatments with no additional CO2 or O3 were included in Sweden in 1999 and in Belgium in 1998 and 1999. All OTC experiments employed three chamber replicates per treatment except in Germany (where two replicates were employed), Sweden (which had 6 in 1998 and 4 in 1999), and Finland in 1998 (which had 4). At most sites, crops were also grown in ambient conditions without chambers. 2.2.2. Free air CO2 enrichment (FACE) experiments In Italy and Germany in 1998 and 1999, crops were exposed to elevated CO2 in unchambered

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ambient air plots to achieve a target level of 550 ml l
1 by releasing CO2 from a ring of pipes surrounding the plots. In Germany there was one FACE ring and one control plot. In Italy there were three replicate FACE rings, three control rings releasing air without elevated CO2 and three ambient plots with no rings. 2.3. Seed preparation, planting and crop management To achieve single stemmed plants for OTC experimentation, seed tubers having been stored at 4 /5 8C were pre-sprouted in continuous light at 12 8C and either had surplus eyes removed or had single-sprouted cores excised which were then allowed to suberise. The resulting single sprouts with their attached parent tuber material were planted at a depth of 10 cm either in small ridges or in flat-ground in pre-prepared local field soil to achieve a density of 20 stems m
2 in 1998 and 13.33 stems m
2 in 1999. In Ireland, ten singlestemmed plants m
2 were grown in 1998. In the Italian FACE experiments seed tubers were planted using a conventional field planting machine in 1999 to achieve a density of c. 5.76 plants m
2 in ridges 73 cm apart. In 1998 the tubers were pre-sprouted and planted manually. In the German FACE experiment, and in the 1998 OTC experiment, plants were grown in large (90 dm3) plastic pots. In all experiments, the crops were irrigated to maintain soil moisture content above 75% of field capacity. Following soil analyses the crops were fertilised to locally-recommended levels for potato. In the OTCs, plants were supported by stakes to reduce lodging. The crops were sprayed against pests and diseases in keeping with the aim to study the effects of elevated [CO2] and [O3] on crops free from other stresses. Where possible, similar disease and pest control products were used at all sites and the use of chemicals thought to afford protection against ozone damage avoided. The products used for blight control were Shirlan (Fi, Sw, UK, Ir, Be); Radamil (Ir, Ge); Tattoo (Fi); Fubol (UK); Trimangol and Aviso (Be); Anthracol, Dithane Ultra, Maneb and Acrobat (Ge) and Copper Sulphate (It). For pest control the products

sprayed were Sumi-alpha and Pirimor (Sw); Metasystox and Dursban (Ir); Rapid, Cyperkill 10 and Metaphor (UK); Pirimor G, Pyretrex special, Unden and Actellic (Be); Neudosan (Ge) and in Italy, Linuron, Bacillus thuringiensis var Kurstaki to protect against colorado beetle. Some products were only used once e.g. Dursban in Ireland in 1998 to tackle stem borers whereas others, e.g. Shirlan, had multiple applications as part of routine spray programs to protect against blight. 2.4. Environmental monitoring Air and soil temperature, humidity, rainfall, irrigation and solar radiation were continuously monitored and recorded both outside and inside the treatment plots at all sites as were the concentrations of CO2 and O3. The levels of other pollutant gasses (NO2, NO and SO2) were also monitored at some sites including those which had potentially the highest ambient background levels of these pollutants. Their growing-season 24 h averages never exceeded 10 nl l
1 for any of the three gasses in either season; levels too low to have had a substantial effect the CO2 or O3 responses in these experiments. 2.5. Crop measurements Plants were destructively harvested at two times: (1) intermediate harvest, corresponding to the time of maximum leaf area and (2) final harvest, when the canopy had senesced to 50% of its maximum. These were considered to be the most important sampling times for testing and developing crop models. At the intermediate harvest the plant components were separated into above- and below-ground material; the above-ground material was further separated into stems, green and senescent leaves. These were then weighed to obtain their fresh weights before being oven-dried and weighed again to obtain dry weights. The number of tubers m
2 were determined and the weight of fresh and oven-dried tubers m
2 recorded. At the final harvest, the above-ground material was harvested 7 /14 days before the tubers, in line with commercial practice to allow the tuber skins

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to set before being harvested. The above-ground material was weighed before being oven-dried. Tuber fresh weight m
2 was determined for each plot, then the tubers were subdivided into three size classes B/35 mm, 35/50 mm and
/50 mm in diameter (i.e. those that would pass through a 35 mm sieve, those that were too large to pass through a 35 mm sieve but that could pass though a 50 mm sieve and those that could not pass through either). The fresh weight and number in each size class was recorded before a sample from each weight class from each plot was oven-dried to determine the tuber dry weight.

3. Statistical analyses The core OTC experiments were analysed individually to check that the within experiment residual variance did not differ substantially between sites and then pooled for overall analyses of variance. In this overall analysis there were consequently more than 20 replicates of the core factorial experiment for each variable analysed. These replicates were blocked between site/season combinations (experiments) and between the replicate blocks within an experiment. Treatment / experiment interactions were tested to determine whether any treatment effects varied between experiments. For variables which showed no ozone /CO2 interaction in the analysis of the core experiments, data for the experiments in which either O3 or CO2 were studied alone (e.g. the FACE experiments) were subsequently included in the analysis of the main effects of O3 or of CO2. Possible relationships between ozone effects on marketable yield; tubers in the
/35 mm category, and accumulated ozone exposure and/or background growing conditions were tested by stepwise regression. The effect of ozone was defined to be the average dry weight yield from the elevatedozone treatments minus the average yield from the chambered ambient-ozone treatments. Accumulated ozone exposure was expressed as the accumulated dose above 40 nl l
1 (AOT40, nl l
1 h) within a given time interval; emergence to harvest; tuber initiation to time of maximum leaf area

277

(MLA); MLA to final harvest. Marketable yields from the chambered ambient-ozone treatments were taken to represent the background growing conditions for the particular experiment. Data from all CO2 levels present for each O3 level in the particular experiment were included in the averages calculated for ambient and elevated ozone levels.

4. Results 4.1. Tuber yields from ambient plots Fig. 1 shows the mean fresh weight yields of tubers in the three size classes:
/35 mm; 35 /50 mm and
/50 mm, harvested from the ambient plots. The data illustrate that, despite the standard protocol followed, the background growing conditions varied considerably between sites and seasons. 4.2. Core OTC experiments Treatment means and analyses of variance summaries for the core OTC experiments, are presented in Tables 1 and 2 for the variables recorded at the intermediate harvest and in Tables 3 and 4 for the final harvest. The results from individual experiments where particular variables were recorded (i.e. from 1 year at one site) occupy successive rows in the tables, followed by the results of the combined analysis over all experiments, (for details see caption to Table 1). 4.3. CO2 /O3 interactions There were no CO2 /O3 interactions detected in the overall analyses for most variables and in general this was consistent across experiments and harvests. Only tuber number at the intermediate harvest showed a CO2 /O3 /Experiment interaction (P B/0.001); elevated ozone affected tuber number in the 1999 German and 1998 Belgian experiments, but only at ambient [CO2] in the former and at elevated [CO2] in the latter. In the analyses of individual experiments, only the 1998 Belgian experiment showed CO2 /O3 interactions

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Fig. 1. Fresh weight yields of marketable sized tubers (
/35 mm diameter) from open plots at each of the experimental sites in each year.

at the intermediate harvest: for above-ground biomass; green leaf and senesced leaf dry weights (P B/0.05). In these cases, weights were lower at elevated O3 than at ambient O3 but only when CO2 was also elevated. At final harvest, the only interaction of this nature was detected in the individual analyses for tuber weight from the Irish 1999 experiment (P B/0.01) in which elevated ozone reduced the yield but only at elevated CO2. 4.4. Ozone effects At the intermediate harvest, only tuber number and green leaf number showed an overall effect of O3 or any interaction between Experiment and O3 (Tables 1 and 2). The Experiment/O3 interaction for green leaf number was due to the data from the 1998 Belgian experiment */which showed a significant increase (P B/0.05) in the number of green leaves in response to elevated O3 (a finding not supported by any of the other sites’ data). The experiment /CO2 /O3 interaction described above for tuber number showed that the response was not consistent across experiments.

For final harvest, however, the overall analyses show that both above ground biomass and tuber dry weight were reduced by O3, despite there being no detectable (P
/0.1) effect in any of the individual analyses except for Ireland 1999 and Belgium 1999 (Table 3). The reduction in tuber weight was most evident in the largest size class (Table 4). There was no overall effect of O3 on tuber number though the individual analysis on data for UK 1998 showed an increase and Belgium 1998 data showed a decrease. Fig. 2a shows the effect of elevated ozone on the dry weight of marketable-size (
/35 mm) tubers plotted against the AOT40 from emergence to harvest for each of the experiments in which elevated ozone was applied, including the two ozone-only experiments; Sweden 1999 and Finland 1998. Regression analysis, omitting the data from Finland which had exceptionally large and contradictory ozone effects in the 2 years, showed there to be a significant negative linear relationship (P B/0.05) between ozone impacts and AOT40; the losses due to ozone tended to become greater as AOT40 increased. Adding chambered ambient-

Table 1 Intermediate harvest above-ground biomass and tuber yields, mean dry weights (g m
2), and tuber numbers (m
2) for the core CHIP OTC treatments: chambers with ambient air (CHA); with added ozone (Oz); with added CO2 (680) and with both ozone and CO2 added (Oz680) Year

Tuber dry weight (g m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments Tuber number (m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments

CHA

Oz

680

Oz680

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

390.1 242.8 192.9 130.7 160.0 352.6 215.1 348.9 495.5 298.5

413.1 234.5 227.2 121.4 205.5 327.1 212.2 311.3 471.8 296.8

438.3 250.4 216.1 114.6 168.1 376.6 218.7 265.5 635.8 319.0

336.3 231.0 304.5 100.1 173.7 431.5 231.5 294.2 637.8 327.0

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

210 245 190 215 275 657 347 498 317 340

215 278 407 213 433 631 322 453 267 366

372 457 324 250 410 882 410 810 513 516

308 451 480 190 476 942 387 664 498 514

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

214.7 104.9 132.4 126.6 116.2 173.3 110.2 143.0 121.7 140

214.7 100.4 126.2 136.9 221.3 135.3 128.9 137.0 122.6 144.8

329.3 123.5 124.4 150.6 184.9 135.3 98.6 152.3 117.3 156.8

234.7 140.4 120.0 119.8 180.7 153.0 98.6 153.0 133.3 149.2

CO2

O3

CO2 /O3

ns ns ns / ns ns ns ns ns ns ns

0.047 ns ns / ns ns ns ns ns ns ns

B/0.001 0.002 ns / 0.094 0.04 ns 0.008 0.039 B/0.001 ns

ns ns 0.053 / 0.055 ns ns ns ns ns ns

ns ns ns / ns ns ns ns ns ns ns

B/0.001 0.004 ns ns ns 0.035 ns ns 0.024 B/0.001

0.003 ns ns 0.048 ns ns ns ns ns 0.005

0.003 ns ns 0.039 ns ns ns ns ns 0.001

ns ns ns / ns ns ns 0.056 0.043 0.042 0.009

sed

df

35.6 15.1 57.0 / 21.7 58.0 30.2 30.1 84.8 17.1 68.5

6 6 8 / 3 6 6 6 6 47

30.1 53.0 116.5 / 52.0 144.9 47.4 93.7 114.9 32.9 131.7

6 6 8 / 3 6 6 6 6 47

14.33 9.03 24.43 21.97 27.02 10.85 17.24 13.82 6.42 25.66

6 6 8 3 6 6 6 6 47

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289

Above ground biomass dry weight (g m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments

Site

For an individual experiment, the ANOVA probability levels used to test the CO2 and O3 main effects and interactions are followed in the same row of the table by the standard error of difference between the means (sed) and its degrees of freedom (df); ns denotes non-significant, (P
/0.1); / denotes unreplicated data. For each variable, the ‘Overall’ rows present the means, probability levels and standard error of difference calculated over all experiments in a combined ANOVA. That ANOVA’s probability levels for testing the consistency of treatment effects across experiments are given in the subsequent row of the table. 279

280

Table 2 Intermediate harvest leaf dry weights and numbers for the core OTC treatments Year

Site

CHA

Oz

680

Oz680

CO2

O3

CO2 /O3

sed

df

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

236.0 182.7 168.8 311.4 216.8 222.0 242.9 214.9 166.4 210.3

274.7 200.4 188.8 256.6 250.0 199.0 235.9 216.7 162.3 216.2

232.0 188.0 182.2 232.7 220.8 209.3 246.5 195.1 156.6 204.3

244.0 173.8 195.5 242.9 236.7 204.3 243.8 190.9 148.4 204.9

ns ns ns / ns ns ns ns ns 0.012 0.078

0.035 ns ns / 0.084 0.094 ns ns ns ns 0.031

ns 0.079 ns / ns ns ns ns ns ns ns

13.20 10.68 15.94 / 13.42 9.97 9.36 16.93 14.62 4.68 18.73

6 6 8 / 3 6 6 6 6 47

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

193.0 101.5 123.4 89.5 96.8 157.0 131.5 122.0 207.0 141.2

213.8 109.3 150.9 86.9 122.4 158.3 132.0 107.0 195.5 147.2

233.0 124.5 142.2 80.0 98.6 190.0 135.7 91.4 272.9 160.3

180.0 109.4 204.0 71.6 106.8 207.9 142.1 106.9 254.3 162.5

ns ns ns / ns 0.059 ns 0.051 0.056 0.01 0.079

ns ns ns / ns ns ns ns ns ns ns

0.019 ns ns / ns ns ns 0.053 ns ns ns

16.34 10.45 41.40 / 13.06 25.08 17.93 8.95 37.30 9.05 36.21

6 6 8 / 3 6 6 6 6 47

Belgium Belgium Germany Germany UK UK

109.3 55.9 3.4 1.3 71.7 82.2 64.1

105.3 54.1 24.0 1.3 59.7 84.8 62.4

132.0 49.7 37.6 2.7 73.7 91.4 72.4

100.0 58.5 41.1 1.3 73.2 92.0 67.7

ns ns / ns ns ns 0.009 ns

ns ns / ns ns ns ns ns

ns ns / ns ns ns ns ns

15.67 5.94 / 2.37 7.16 8.98 3.39 13.57

6 6 / 3 6 6 27


2

Greenleaf dry weight (g m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments Senesced leaf number (m
2) 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments

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Greenleaf number (m ) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments

Year Senesced leaf dry weight (g m
2) 1998 1999 1998 1999 1999 1998 1999 Overall Interactions between experiments and treatments Format as for Table 1.

Site

Belgium Belgium Germany Germany Ireland UK UK

CHA

11.8 16.9 0.1 0.2 39.6 32.1 40.4 23.2

Oz

11.6 15.0 0.9 0.0 30.2 29.5 48.9 22.2

680

15.4 16.9 0.5 0.1 44.6 31.6 49.3 26.4

Oz680

9.8 23.6 2.8 0.1 56.6 34.8 65.3 32.5

CO2

O3

CO2 /O3

sed

df

ns ns / ns ns ns ns 0.003 ns

0.013 ns / ns ns ns ns ns ns

0.018 ns / ns ns ns ns ns ns

1.17 4.63 / 0.18 11.69 6.71 13.66 2.98 11.93

6 6 / 3 6 6 6 33

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289

Table 2 (Continued )

281

282

Table 3 Final harvest: dry weights (g) of above ground biomass, total tuber yield and number (m
2) Year

Total tuber dry weights (g m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1998 1999 Overall Interactions between experiments and treatments Total tuber numbers (m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1998 1999 Overall Interactions between experiments and treatments Format as for Table 1.

Belgium Belgium Finland Germany Germany Ireland Ireland UK UK

Belgium Belgium Finland Germany Germany Ireland Ireland Sweden UK UK

Belgium Belgium Finland Germany Germany Ireland Ireland Sweden UK UK

CHA

257.5 323.3 348.6 139.1 226.1 262.0 444.5 392.7 655.5 329.4

1610 1687 1696 1046 1740 1186 1238 1446 978 2273 1493

141.67 94.79 77.47 119.76 161.41 84.66 124.86 195.56 111.27 96.27 125.07

Oz

190.2 272.1 303.6 136.5 253.6 267.5 447.6 360.2 642.7 299.2

1476 1502 2062 914 1393 1254 1345 1301 905 2129 1416

128.33 87.09 85.07 129.17 145.31 95.10 110.64 180.74 124.30 101.60 121.4

680

148.0 240.3 312.0 122.4 193.2 330.8 428.7 385.2 841.3 306.1

1657 1838 2106 1145 1954 1658 1905 1340 1083 3208 1728

146.17 108.42 90.07 104.36 170.17 86.00 96.86 231.11 138.18 110.49 134.28

Oz680

150.7 231.2 314.8 109.1 185.5 293.4 395.8 368.1 787.2 288.7

1577 1727 2202 1138 2001 1593 1577 1346 1163 2949 1664

133.00 107.68 91.10 115.22 172.27 104.88 93.75 209.26 141.76 103.68 131.04

CO2

O3

CO2 /O3

0.051 ns ns / ns 0.048 ns ns 0.01 0.099 B/0.001

ns ns ns / ns ns ns ns ns 0.022 ns

ns ns ns / ns ns ns ns ns ns ns

ns 0.029 ns / 0.078 0.018 0.002 ns 0.092 0.01 B/0.001 B/0.001

ns 0.067 ns / ns ns ns ns ns ns 0.079 ns

ns ns ns / ns ns 0.052 ns ns ns ns ns

ns 0.019 ns / ns ns 0.025 0.008 B/0.001 ns 0.002 0.003

0.009 ns ns / ns 0.085 ns ns 0.017 ns ns ns

ns ns ns / ns ns ns ns ns ns ns ns

sed

43.3 50.4 31.3 / 50.0 27.0 53.2 43.2 63.1 14.15 51.0 98.9 93.6 314.7 / 176.7 127.4 117.0 128.3 336.3 55.9 142.0 4.93 7.64 10.03 / 25.45 10.07 10.70 15.52 3.61 13.62 4.18 10.65

df

6 6 8 / 3 6 6 6 6 47

6 6 8 / 3 6 6 20 6 6 67

6 6 8 / 3 6 6 20 6 6 67

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Above ground biomass dry weight (g m
2) 1998 1999 1999 1998 1999 1998 1999 1998 1999 Overall Interactions between experiments and treatments

Site

Table 4 Final harvest: dry weights of marketable size tubers (g m
2) Year

Tuber dry weights in the 35 /50 mm size class 1998 1999 1999 1998 1999 1998 1999 1998 1998 1999 Overall Interactions between experiments and treatments

CHA

Oz

680

Oz680

CO2

O3

CO2 /O3

sed

df

Belgium Belgium Finland Germany Germany Ireland Ireland Sweden UK UK

909 1259 1250 65 903 778 696 493 307 1903 842

803 1051 1589 146 556 780 769 358 266 1717 778

917 1212 1538 309 1054 1222 1553 360 324 2719 1035

814 1141 1551 285 1106 1087 1180 279 380 2510 946

ns ns ns / 0.028 0.038 B/0.001 ns ns 0.016 B/0.001 B/0.001

ns ns ns / ns ns 0.023 ns ns ns 0.044 ns

ns ns ns / ns ns 0.004 ns ns ns ns ns

103.5 116.3 271.1 / 123.4 200.4 70.0 107.8 108.4 341.2 52.6 134.0

6 6 8 / 3 6 6 20 6 6 67

ns ns ns / ns ns ns ns ns ns ns ns

ns ns ns / ns ns ns ns ns ns ns ns

Belgium Belgium Finland Germany Germany Ireland Ireland Sweden UK UK

543.2 357.6 414.8 761.5 641.6 313.4 453.4 880.3 532.4 336.9 542.7

530.7 391.2 434.2 582.4 648.9 368.7 498.1 837.3 467.1 380.6 528.9

566.9 536.1 521.9 681.4 675.3 361.2 287.1 856.3 570.4 459.7 575.2

622.3 498.6 605.4 668.3 683.7 383.7 334.4 942.4 584.1 409.3 599.3

0.051 0.005 0.042 / ns ns 0.022 ns 0.063 ns 0.003 0.02

33.6 46.3 81.3 / 76.8 66.8 75.6 78.2 48.0 91.7 23.33 84.13

6 6 8 / 3 6 6 20 6 6 67

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289

Tuber dry weights in the
/50 mm size class 1998 1999 1999 1998 1999 1998 1999 1998 1998 1999 Overall Interactions between experiments and treatments

Site

Format as for Table 1.

283

284

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Fig. 2. (a) Ozone effect, expressed as the difference between the dry weight (g m
2) of marketable sized tubers (
/35 mm) from elevated-ozone and ambient-ozone treatments, plotted against the accumulated ozone exposure above 40 nl l
1 from crop emergence to final harvest (AOT40) for the individual experiments. Data were averaged over all CO2 levels for both ozone levels. (b) Residual deviations about the fitted line in Fig. 2a plotted against the average yields for the ambient-ozone treatments from the individual experiments.

ozone yields into the stepwise regression significantly (P /0.002) improved the fit. This is illustrated in Fig. 2b which shows a significant linear relationship between the deviations about the line of best fit shown in Fig. 2a; i.e. the variation in ozone effect left unexplained by AOT40, and chambered ambient-ozone yields. When the order of fitting was reversed, chambered ambient-ozone yields explained a much larger proportion of the variation in ozone effects (83%) when fitted first than they did when fitted last (44%). Consequently AOT40 did not significantly improve the fit when it was fitted last. It was not possible to completely isolate the relationships with AOT40 and ambient yields because of their partial confounding in the data sets; experiments with high ambient-ozone yields tended coincidentally to be those that received the higher ozone doses. When the analyses were repeated using AOT40 values calculated over different time intervals, there were no clear relationships between ozone effects and AOT40

values calculated from early in the season; before the timing of maximum leaf area. Only for the period from maximum leaf area to final harvest did the calculated AOT40 values show similar relationships to those observed for the full season AOT40 values. 4.5. CO2 effects At both harvests, all variables responded to elevated [CO2] but the nature and extent of the response varied among the experiments. At the intermediate harvest, there was a suggestion that above-ground biomass was increased by elevated [CO2], largely due to the data from the UK 1999 experiment, but other experiments exhibited much smaller increases or even decreases. Of the other above-ground components recorded at the intermediate harvest, green leaf number was decreased (P B/0.05) and green leaf dry weight increased (P /0.01) by elevated [CO2] whereas both the

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289

number and weight of senesced leaves increased under elevated [CO2]. Overall, above-ground biomass at final harvest was reduced by elevated [CO2], reflecting the cumulative effect of observed decreases in five of the experiments, which were too small to be detected (P
/0.05) in the individual analyses. In contrast, UK data for 1999 showed a significant increase in above-ground biomass at final harvest. The overall means for tuber number at intermediate harvest suggest an increase in response to elevated [CO2], which though clearly the case in the Belgian data was not the case in Ireland 1999; this difference contributed to the significant variation in CO2 responses detected between experiments (P B/0.001). At the final harvest, total tuber numbers were increased by elevated CO2, all experiments except Ireland 1999 and Germany 1998 showing numerical increases-though many were again too small to be detected in the analyses of single experiments but contributed to the significant increase detected in the overall analysis. Intermediate-harvest tuber weight was increased by elevated CO2 (P B/0.001). At the final harvest, whilst total tuber dry-weight increased in response to elevated CO2, the response varied in direction and extent among the experiments. All sites except Sweden 1998 recorded a numerical increase (Table 3), though many were not large enough to be statistically significant (P
/0.1) in the individual analyses. A similar pattern was shown in marketable size classes (Table 4). Besides Germany 1998, which was not evaluated, low yields were obtained at Sweden 1998 and UK 1998. The difference between the yield of tubers
/35 mm at final harvest from the elevated and ambient CO2 treatments is plotted against the means from the ambient CO2 treatments in Fig. 3. Data from all experiments involving elevated CO2 are presented including the FACE experiments from Italy and Germany and 550 ml l
1 OTC treatments from Germany and the UK. There was considerable variation in the CO2 response. Points joined by straight lines are 2 years’ results from the same treatment at the same site for the FACE and the 680 ml l
1 OTC experiments. In all cases, both the ambient yields and CO2 effects were less in 1998 than in 1999 at the same site. Hence for every site

285

Fig. 3. CO2 effect, expressed as the difference between the dry weight of marketable sized tubers (
/35 mm) from elevatedCO2 and ambient-CO2 treatments, plotted against the average yield for the ambient CO2 treatments. For each CO2 level data were averaged over all ozone levels. The squares represent data for OTC 680 ml l
1 treatments, the diamonds data for OTC 550 ml l
1 treatments and the triangles data from FACE experiments. Points joined by straight lines are from the same treatment and location in each of the 2 years. The 1999 data invariably appears to the right of the 1998 data for a particular location. The locations are indicated by the text adjacent to the lines: Be Belgium; Fi Finland; Ge Germany; Ir Ireland; It Italy; Sw Sweden; UK United Kingdom.

with two season’s data the line joining the two season’s results ascends, suggesting that there is a correlation between the magnitude of the CO2 effect and the ambient-CO2 yield. However, within either season there is no evidence that variation in the CO2 effect across sites is related to the marketable yield of the ambient-CO2 treatments. The magnitude of the CO2 effects, considered in either absolute terms or relative to the ambient yield, varied substantially between locations. With the exception of the high yielding experiment conducted in the UK in 1999, the Italian FACE experiment showed a greater CO2 effect, particularly when considered in relative terms, than did the OTC experiments. In contrast the FACE results from Germany showed little or no effect of CO2 enrichment. The CO2 effects for the 550 ml l
1 OTC treatments did not differ significantly (P
/0.1) from those for the 680 ml l
1 OTC treatment at the same site. This indicates that the CO2 effect at those sites had saturated or was close to its maximum at 550 ml l
1.

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5. Discussion The core CHIP OTC experiment was designed to test whether elevated CO2 would protect potato growth and yield against the damaging effects of elevated O3 and also whether growth and yield enhancement induced by elevated CO2 is reduced by elevated O3. Elevated CO2 has been shown to reduce O3-induced effects on variables such as visible leaf injury in potato (De Temmerman et al., 2002b; Donnelly et al., 2001b) and green leaf area (Mulholland et al., 1997) and photoassimilation (McKee et al., 2000; Donnelly et al., 2000) in wheat, all of which would be expected to influence crop yields. However, in the data presented, the absence of any significant overall interaction between CO2 and O3 for any biomass or yield variable at either harvest indicates that either CO2 /O3 interactions did not occur consistently across experiments or that the interactive effects were too small to be detected despite the increased power of the pooled data analyses. Even the few interactions found within single experiments ran counter to the above hypotheses. When O3 had a detectable damaging effect on the intermediateharvest tuber numbers and above ground dry weights from Belgium 1998 and on the tuber yield at final harvest from Ireland 1999, the damage occurred only at elevated CO2. It would be impossible to demonstrate a protective effect of CO2 against ozone-induced damage if there was no significant ozone damage against which to protect. This may have been the case for the intermediate harvest in which little or no ozone effects on biomass and yield were detected. However, a clear overall reduction in biomass and tuber yield in response to elevated ozone was detected at the final harvest, particularly in the largest tuber size category, and there was no indication that the yield reduction due to ozone was any less under elevated CO2. For marketable tuber yield (i.e. those over 35 mm) the power of the combined analysis of all experiments enabled the average reduction of 4.8% of the ambient O3 yield to be detected (P B/0.05) although it was not detectable from the analyses of the individual experiments. These results agree with the findings of Pell et al. (1988) who found

that a seasonal 10 h per day mean of 51 nl l
1 O3 concentration reduced the yield of the largest size class,
/60 mm, of cv. Norchip. However, the losses reported here were considerably less than the 30% reported by Clarke et al. (1990) under ambient O3 conditions in the Eastern United States in potato crops which exhibited moderate to severe visible injury. Therefore, despite indications to the contrary, it would seem that cv. Bintje may be relatively insensitive to ozone. The strong relationship between the loss of marketable yield due to elevated ozone and the yield attained under ambient O3 conditions suggests that a major factor determining the scale of yield loss is the potential production at the particular site under the prevailing weather and management conditions. Of the variation in tuber yield responses induced by elevated ozone among the experiments, more could be explained by variation in yield potential than could be explained by variation in accumulated ozone exposure. Therefore, in attempting to model ozone-induced yield losses on a European scale, it is important that the models can account for the variation in potential potato yields across different sites and seasons. The causes of this variation are complex and still not wholly understood. Consequently current models cannot account fully for the variation between sites and seasons. An interesting feature of the relationship observed between ozone response and ambient ozone yield, whether or not AOT40 is included in the model, is that the proportional as well as the actual yield loss increases as potential yield increases. This implies that, for the same ozone conditions, more of the crop would be lost to ozone in good growing years than in poor growing years and is consistent with the fact that under low yielding conditions factors other than ozone would limit yield. This particularly could be the case for Sweden 1998 and UK 1998 where low tuber yields (Table 4) were harvested. CO2 enhanced mid-season above ground biomass and final harvest tuber yields to a greater extent than they were reduced by O3, resulting in net increases overall under the combined CO2 and O3 conditions that could occur in a future European climate. The increased weight of green

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289

leaves at the intermediate harvest represented the larger crop canopy, produced under elevated CO2; enhancing light capture and photoassimilation later in the season. It would also provide a larger area susceptible to damage by O3 which may have contributed to the few cases where losses due to elevated ozone were only detectable in treatments in which [CO2] was also elevated. Contrasting effects of elevated [CO2] were shown at the two FACE sites, with the Italian experiments showing much greater responses than did the German experiments. A possible cause of this may have been the use of pots in the German experiments as it has been shown that pots size can have both positive and negative effects on plant responses to elevated [CO2] (McConnaughay et al., 1993). Indeed, the German 1998 OTC experiment, which used similar pots, also showed little response to elevated [CO2]. However, it should be noted that plants in some of the other OTC experiments were similarly unresponsive. Also, plants in pots from the German 1999 FACE experiment produced one of the highest yields obtained under ambient [CO2], which supports the view that pots of the size used here, would not restrict growth responses. The greater [CO2] effects observed in 1999 compared with the effects in 1998 at the same sites could also have been due to a number of causes including the lower planting densities used at many sites in 1999. This may have enabled individual plants to perform better to the benefit of the whole crop, a fact exacerbated by the knowledge that 1999 was generally warmer and considered better for growth at many sites. Within a season, however, it is clear that the factors responsible for the variation in ambient yields were not the same as those that determined the responses to elevated CO2. Within either season there was no obvious relationship between ambient yields and CO2 effects. For a number of the individual experiments the CO2 effect on tuber yield, particularly when expressed as a proportion of the ambient yield, was less at the final harvest than at the intermediate harvest. If growth had been unrestricted, the CO2 effect would be expected to become greater because of the cumulative effect of earlier and enhanced canopy growth. This would suggest

287

that the growth of these particular crops was limited in some way towards the end of the season. The increase in tuber numbers at the finalharvest, in response to elevated CO2, was not sufficient to explain the observed increase in yield because tubers also grew larger on average under elevated CO2. Indeed, the high yields in the UK1999 experiment resulted from larger tubers than in 1998 and the fact that tubers were heavier in the elevated CO2 treatments (Donnelly et al., 2001a). This differs from the conclusions of Miglietta et al. (1998) who attributed the increased yield in their FACE experiments to the increase in tuber numbers under elevated CO2. The closeness of the yield increases at 550 and 680 ml l
1 suggests that the CO2 response was at, or approaching, saturation at 550 ml l
1. Mackowiak and Wheeler (1996) reported that tuber yield enhancement was maximum at 1000 ml l
1 but was reduced by higher concentrations, supporting the concept of their being an upper limit to the CO2 response. The response of potato to elevated [CO2] has been shown in laboratory experiments to depend upon environmental conditions (Wheeler et al., 1991). Therefore, it is possible that under the conditions of our experiments that the optimum [CO2] may be close to our experimental treatment levels. It also strengthens the comparability of the CO2 treatments in the OTC and FACE experiments. It should be noted, however, that Miglietta et al. (1998) concluded that the CO2 response was not saturated at 550 ml l
1 in their experiments.

6. Conclusions Anticipated future increases in ozone levels would reduce the yield of the European potato crop of cv. Bintje and the losses would be predicted to be greatest under high yielding conditions. Elevated [CO2] did not directly protect against yield losses in these experiments indicating that O3-induced losses of potato yield will still occur in a future climate even under elevated [CO2]. However, the yield increases observed in response to elevated [CO2] far exceeded ozoneinduced losses. Consequently, in a climate in which

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both [O3] and [CO2] are increased to the levels studied in these experiments, the positive effects of CO2 on yield would be predicted to more than compensate for the negative effects of ozone. This scenario would result in a net increase in the yield in the European potato crop.

Acknowledgements This work was partially-funded by EU Contract No. ENV4-CT-0498.

References Acock, B., Allen, L.H., 1985. Crop responses to elevated CO2 concentrations. In: Strain, B.R., Cure, J.D. (Eds.), Direct Effects of Increasing CO2 on Vegetation. USDOE, Washington, DC, pp. 55 /97. Anfossi, D., Sandroni, S., Viarengo, S., 1991. Tropospheric ozone in the 19th century: the Moncalieri series. J. Geophys. Res. 96D, 17349 /17352. Ashmore, M.R., Bell, J.N., 1991. The role of ozone in global change. Ann. Bot. 67, 39 /48. Balaguer, L., Barnes, J.D., Panicucci, A., Borland, A.M., 1995. Production and utilisation of assimilates in wheat (Triticum aestivum L.) leaves exposed to elevated O3 and/or CO2. New Phytol. 129, 557 /568. Barnes, J.D., Pfirrman, T., 1992. The influence of CO2 and O3 singly, and in combination, on gas exchange, growth and nutrient status of radish (Raphanus sativus L.). New Phytol. 121, 403 /412. Barnes, J.D., Wellburn, A., 1998. Air pollutant combinations. In: de Kok, L.J., Stuhlen, I. (Eds.), Responses of Plant Metabolism to Air Pollution and Global Change. Backhuys Publishers, Leiden, The Netherlands, pp. 147 /164. Barnes, J., Bender, J., Lyons, T., Borland, A., 1999. Natural and man-made selection for air pollution resistance. J. Exp. Bot. 50, 1423 /1435. Black, V.J., Black, C.R., Roberts, J.A., Stewart, C.A., 2000. Impact of ozone on the reproductive development of plants. New Phytol. 147, 421 /447. Bosac, C., Black, C.R., Roberts, J.A., Black, V.J., 1998. The impact of O3 on seed yield and quality in oilseed rape (Brassica napus L). J. Plant Physiol. 153, 127 /134. Clarke, B.B., Greenhalgh-Weidman, B., Brennan, E.G., 1990. An assessment of the impact of ambient ozone on field grown crops in New Jersey using the EDU method: part 1white potato (Solanum tuberosum ). Environ. Pollut. 66, 351 /360.

Cure, J.D., Acock, B., 1986. Crop responses to carbon dioxide doubling: a literature survey. Agric. For. Meteorol. 38, 127 /145. De Temmerman, L., Hacour, A., Vandermeiren, K., 2000. Changing climate and potential impacts on potato yield and quality ‘CHIP’. In: Proceedings of European Climate Science Conference, October 1998. Austrian Federal Ministry of Science and Transport, Vienna, Austria. De Temmerman, L., Wolf, J., Colls, J., Bindi, M., Fangmeier, A., Finnan, J., Ojanpera¨, K., Pleijel, H., 2002a. Effect of climatic conditions on tuber yield (Solanum tubersum L.) in the European ‘CHIP’ experiments. Eur. J. Agron., 17, 243 / 255. De Temmerman, L., Pihl-Karlsson, G., Donnelly, A., Ojanpera¨, K., Ja¨ger, H.-J., Finnan, J., Ball, G., 2002b. Factors influencing visible ozone injury on potato including their interaction with carbon dioxide. Eur. J. Agron., 17, 291 / 302. Donnelly, A., Jones, M.B., Burke, J.I., Schnieders, B., 1999. Does elevated CO2 protect grain yield of wheat from the effects of ozone stress. Zeitschr. Naturforsch. C-A J. Biosci. 54c, 802 /811. Donnelly, A., Jones, M.B., Burke, J.I., Schnieders, B., 2000. Elevated CO2 provides protection from O3 induced photosynthetic damage and chlorophyll loss in flag leaves of spring wheat (Triticum aestivum L., cv. ‘Minaret’). Agric. Ecosyst. Environ. 80, 159 /168. Donnelly, A., Craigon, J., Black, C.R., Colls, J.J., Landon, G., 2001a. Elevated CO2 increases biomass and tuber yield in potato even at high ozone concentrations. New Phytol. 149, 265 /274. Donnelly, A., Craigon, J., Black, C.R., Colls, J.J., Landon, G., 2001b. Does elevated CO2 ameliorate the impact of O3 on chlorophyll content and photosynthesis in potato (Solanum tuberosum L.). Physiol. Plant. 111, 501 /511. Drake, B.G., Gonza`lez-Meler, M.A., Long, S.P., 1997. More efficient plants: A consequence of rising atmospheric CO2. Ann. Rev. Plant Physiol. Plant Mol. Biol. 48, 609 /639. FAO, 1996. Food and Agriculture Organisation of the United Nations, Production Yearbook 50, 61. Finnan, J.M., Jones, M.B., Burke, J.I., 1998. A time-concentration study on the effect of ozone on spring wheat (Triticum aestivum L.). 3: Effects on leaf area and flag leaf senescence. Agric. Ecosyst. Environ. 69, 27 /35. Finnan, J.M, Donnelly, A., Burke, J.I., Jones, M.B., 2001. The effects of elevated concentrations of CO2 and O3 on potato (Solanum tuberosum L.) yield. Agric. Ecosyst. Environ. 1744, 1 /12. Fiscus, E.L., Reid, C.D., Miller, J.E., Heagle, A.S., 1997. Elevated CO2 reduces O3 flux and O3-induced yield losses in soybeans: possible implications for elevated CO2 studies. J. Exp. Bot. 48, 307 /313. Foster, K.W., Guerard, R.J., Oshima, R.J., Bishop, J.C., Timm, H., 1983a. Differential ozone susceptibility of centennial Russet and White Rose potato as demonstrated by fumigation and antioxidant treatments. Am. Potato J. 60, 127 /139.

J. Craigon et al. / Europ. J. Agronomy 17 (2002) 273 /289 Foster, K.W., Timm, H., Labanauskas, C.K., Oshima, R.J., 1983b. Effects of ozone and sulfur dioxide on tuber yield and quality of potatoes. J. Environ. Qual. 12, 75 /80. Fuhrer, J., Egger, A., Lehnherr, B., Grandjean, A., Tschannen, W., 1989. Effects of ozone on the yield of spring wheat (Triticum aestivum L. cv. Albis) grown in open-top field chambers. Environ. Pollut. 65, 181 /192. Hertstein, U., Gru¨nhage, L., Ja¨ger, H.-J., 1995. Assessment of past, present and future impacts of ozone and carbon dioxide on crop yields. Atmos. Environ. 29, 231 /239. IPCC, 1996. Climate change 1995. In: Houghton, J.T., Meira Filho, L.G., Callander, B.A., Harris, N., Kattenberg, A., Maskell, K. (Eds.), The Science of Climate Change, IPCC. Cambridge University Press, Cambridge, UK. Kimball, B.A., 1983. Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agron. J. 75, 779 /782. Lawson, T., Craigon, J., Black, C.R., Colls, J.J., Tulloch, A.M., Landon, G., 2001. Effects of elevated carbon dioxide and ozone on the growth and yield of (Solanum tuberosum L.) grown in open-top chambers. Environ. Pollut. 111, 479 / 491. Mackowiak, C.L., Wheeler, R.M., 1996. Growth and stomatal behavior of hydroponically cultured potato (Solanum tuberosum L.) at elevated and super-elevated CO2. J. Plant Physiol. 149, 205 /210. McConnaughay, K.D.M., Berntson, G.M., Bazzaz, F.A., 1993. Limitations to CO2-induced growth enhancement in pot studies. Oecologia 94, 550 /557. McKee, I.F., Bullimore, J.F., Long, S.P., 1997. Will elevated CO2 concentrations protect the yield of wheat from O3 damage. Plant Cell Environ. 20, 77 /84. McKee, I.F., Mulholland, B.J., Craigon, J., Black, C.R., Long, S.P., 2000. Elevated concentrations of atmospheric CO2 protect against and compensate for O3 damage to photosynthetic tissues of field-grown wheat. New Phytol. 146, 427 /435. Miglietta, F., Magliulo, V., Bindi, M., Cerio, L., Vaccari, F.P., Loduca, V., Peressottis, A., 1998. Face Air CO2 Enrichment of potato (Solanum tuberosum L.): development and yield. Glob. Change Biol. 4, 163 /172. Mulholland, B.J., Craigon, J., Black, C.J., Colls, J.J., Atherton, J.G., Landon, G., 1997. Effects of elevated carbon dioxide and ozone on the growth and yield of spring wheat (Triticum aestivum L.). J. Exp. Bot. 48, 113 /122.

289

Mulholland, B.J., Craigon, J., Black, C.J., Colls, J.J., Atherton, J.G., Landon, G., 1998. Growth, light interception and yield of spring wheat (Triticum aestivum L.) to elevated CO2 and O3 in open-top chambers. Glob. Change Biol. 4, 121 /130. Mulchi, C.L., Slaughter, L., Saleem, M., Lee, E.H., Pausch, R., Rowland, R., 1992. Growth and physiological characteristics of soybean in open-top chambers in response to ozone and increased atmospheric CO2. Agric. Ecosyst. Environ. 38, 107 /118. Murray, D.R., 1997. Carbon Dioxide and Plant responses. Research Studies Press, Taunton, UK. Ollerenshaw, J.H, Lyons, T., 1999. Impacts of ozone on the growth and yield of field grown winter wheat. Environ. Pollut. 106, 67 /72. Ollerenshaw, J.H., Lyons, T., Barnes, J.D., 1999. Impacts of ozone on the growth and yield of field-grown winter oilseed rape. Environ. Pollut. 104, 53 /59. Pell, E.J., Pearson, N.S., Vinten-Johansen, C., 1988. Qualitative and quantitative effects of ozone and/or sulfur dioxide on field-grown potato plants. Environ. Pollut. 53, 171 /186. Pleijel, H., Ska¨rby, L., Wallin, G., Se´llden, G., 1991. Yield and grain quality of spring wheat (Triticum aestivum L. cv. Drabant) exposed to different concentrations of ozone in open-top field chambers. Environ. Pollut. 69, 151 /168. Pleijel, H., Danielsson, H., Vandermeiren, K., Blum, C., Colls, ¨ janpera¨, K., 2002. Stomatal conductance and ozone J., O exposure in relation to potato tuber yield */results from the European CHIP programme. Eur. J. Agron., 17, 303 /317. Polle, A., Pell, E.J., 1999. Role of carbon dioxide in modifying plant responses to ozone. In: Luo, Y., Mooney, H.A. (Eds.), Carbon Dioxide and Environmental Stress. Academic Press, New York, USA, pp. 193 /213. Stockwell, W.R., Kramm, G., Scheel, H.-E., Mohnen, V.A., Seiler, W., 1997. Ozone formation, destruction and exposure in Europe and the United States. In: Sandermann, H., Wellburn, A.R., Heath, R.L. (Eds.), Forest Decline and Ozone , Springer, Berlin, Germany, Ecological Studies 127, 1 /38. Wheeler, R.M., Mackowiak, C.L., Sager, J.C., Knott, W.M., 1994. Growth of soybean and potato at high CO2 partial pressure. Adv. Space Res. 14, 251 /255. Wheeler, R.M., Tibbitts, T.W., Fitzpatrick, A.H., 1991. Carbon dioxide effects on potato growth under different photoperiods and irradiance. Crop Sci. 31, 1209 /1213.