stomatal conductance and ozone exposure in relation to potato tuber yield—results from the...

Stomatal conductance and ozone exposure in relation topotato tuber yield*/results from the European CHIP

programme

H. Pleijel a,*, H. Danielsson a,b, K. Vandermeiren c, C. Blum d, J. Colls e,K. Ojanpera f

a Applied Environmental Science, Goteborg University, P.O. Box 464, SE-405 30 Goteborg, Swedenb Swedish Environmental Research Institute, P.O. Box 47086, SE-402 58 Goteborg, Sweden

c VAR, Leuvensesteenweg 17, B-3080 Tervuren, Belgiumd Institute for Plant Ecology, Justus-Liebig-University, Heinrich-Buff Ring 26-32, D-35392 Giessen, Germany

e Department of Physiology and Environmental Science, University of Nottingham, Sutton Bonnington Campus, Loughborough LE12

5RD, United Kingdomf Agricultural Research Centre of Finland, Institute of Resource Management, FIN-31600 Jokioinen, Finland

Abstract

Measurements of stomatal conductance on field-grown potato (Solanum tuberosum L.) cv. Bintje from the CHIP

programme were combined to study the response to environmental factors. 3274 data points were used. Data were

obtained from five sites: Jokioinen in Finland, Ostad in Sweden, Giessen in Germany, Tervuren in Belgium and Sutton

Bonnington in UK. Measurements were made in open-top chamber treatments with ozone and carbon dioxide exposure

and in the ambient air. A typical light response curve was obtained with light saturation at approximately 400

mmol m�2 s�1 photosynthetically active radiation (PAR). The leaf temperature optimum for stomatal conductance

was 29 8C. The stomatal conductance declined strongly at leaf-to-air vapour pressure differences �/20 hPa. An

elevated carbon dioxide concentration (680 ml l�1) reduced the stomatal conductance by up to approximately 20%.

Elevated ozone reduced the stomatal conductance towards the end of the growth period, in addition to the negative

effect by ordinary senescence on stomatal conductance. A multiplicative model, based on the boundary line technique,

was used to estimate the relationship between stomatal conductance and the environmental variables. Test with the data

sets from two sites providing sufficient data, Ostad and Giessen, showed that the multiplicative model had R2-values of

0.60 and 0.42, respectively, for the relationship between calculated and observed conductance. Test of the model with an

independent data set from an open-top chamber experiment with the potato cultivar Kardal showed an R2 of 0.59

between calculated and observed conductance. The conductance model was used to estimate the accumulated ozone

uptake (CUO3) by potato leaves from emergence to harvest. The relationship between CUO3 and relative yield loss,

using a threshold for the ozone uptake rate of 7 nmol m�2 s�1, provided a higher R2-value (0.45) than CUO3 without

any threshold and relationships based on the accumulated exposure over 40 nmol mol�1 (AOT40) or the sum of all

* Corresponding author. Tel.: �/46-31-773-2532; fax: �/46-31-773-2984

E-mail address: [email protected] (H. Pleijel).

Europ. J. Agronomy 17 (2002) 303�/317

www.elsevier.com/locate/eja

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 8 - 0

mailto:[email protected]

hourly average ozone concentrations exceeding 60 nmol mol�1 (SUM06). All four relationships were however

statistically significant.

# 2002 Elsevier Science B.V. All rights reserved.

Keywords: AOT40; Ozone; Ozone uptake; Potato; Stomatal conductance; SUM06; Tuber yield

1. Introduction

It is well established that ozone has the potential

to cause visible injury and yield loss in several

crops (Heck et al., 1988; Jager et al., 1992),

including potato (Solanum tuberosum L.) (Skarby

and Jonsson, 1988). Today, this kind of environ-

mental impact is considered to be very important

by policymakers (Borrell et al., 1997). As a result

there is a request for relationships between ozone

exposure and effects in order to accurately esti-

mate the extent of pollution induced damage and

the costs associated with this.

In Europe, the exposure index AOT40 (the

accumulated exposure over a threshold concentra-

tion of 40 nmol mol�1 ozone) has been widely

used during the last decade to obtain exposure�/

response relationships for primarily wheat (Triti-

cum aestivum ) and clover (Trifolium spp.) among

important crops (Karenlampi and Skarby, 1996).

When it was first introduced, AOT40 represented

an improvement in the development of exposure�/

response relationships (Fuhrer, 1994; Fuhrer et al.,

1997). At present, however, more and more

emphasis is being laid on ozone uptake by the

plants (Fuhrer, 2000), which takes place mainly

through the stomata (Fowler et al., 1991). Nowa-

days there is consensus within the scientific com-

munity that there should exist a closer relationship

between ozone uptake and effect than between the

ozone concentration outside the plants and effect

(e. g. Grunhage and Jager, 1994). For instance,

Pleijel et al. (2000) showed that the interexperi-

mental variation in ozone effects on spring wheat

yield associated with AOT40 was much reduced

when using an estimation of ozone uptake by the

flag leaves instead. The basis for that approach

was formed by Emberson et al. (1998), by intro-

ducing a multiplicative method for the estimation

of stomatal conductance and ozone effects, based

on phenology and environmental variables such as

solar radiation, temperature, leaf-to-air vapour

pressure difference (VPDLA) and soil moisture.

This modelling concept relied on earlier work by

e.g. Jarvis (1976), Korner (1994) and Gruters et al.

(1995).For potato no relationship between ozone

uptake and effects has been developed so far.

The EU-funded Changing Climate and Potential

Impacts on Potato Yield and Quality (CHIP)

programme, with several participating countries

offered an opportunity to explore a large data set

on potato, where stomatal conductance data were

derived in open-top chamber experiments. In theseexperiments also the influence of ozone on tuber

yield was studied.

The aims of the present investigation were (1) to

calibrate the multiplicative stomatal conductance

model for potato, (2) to test the conductance

model on an independent data set, and (3) to

derive relationships between ozone exposure, in-

cluding the estimated leaf uptake of ozone, andeffects on tuber yield.

2. Materials and methods

2.1. Sites and conductance measurements

Information concerning the experiments from

which data were taken is presented in Table 1.

Further details concerning climatic conditions and

pollutant exposure during the experiments can be

found in De Temmermann et al. (2002, this

volume). All studies were performed in 1998 and

1999. Data were obtained from open-top chamberexperiments using field-grown potato Solanum

tuberosum L. cv. Bintje and from measurements

in ambient air plots. In addition, data from

another experiment with the potato cultivar Kar-

dal, performed in Ostad, Sweden in 1999, were

included. The measurements of stomatal conduc-

H. Pleijel et al. / Europ. J. Agronomy 17 (2002) 303�/317304

Table 1

Sites and countries contributing data to the study in 1998 and 1999 (G , stomatal conductance data; Y , tuber yield data), equipment used for the measurements of stomatal

conductance and the different open-top chamber treatments used (CF, charcoal filtered air; NF, non-filtered air; NF�/, NF�/�/, non-filtered air with additional ozone;

680, 680 mmol mol�1 CO2) and the corresponding average ozone concentrations (8-h average 09.00�/17.00 GMT)

Site and country 1998 1999 Equipment Treatments 1998 Treatments 1999 Ozone

1998nmol mol�1

Ozone 1999

nmol mol�1

Irrigation�/rainfall

1998/1999, mm

Tervuren, BE G/Y G/Y CIRAS IRGA,

PP systems

CF, NF, NF�/,

NF680, NF�/680

CF, NF, NF�/,

NF680, NF�/680

6, 25, 47 7, 31, 63 532/417

Sutton Bonnington,

UK

G/�/ G/�/ CIRAS IRGA,

PP systems

NF, NF�/, NF680,

NF�/680

NF, NF�/, NF680,

NF�/680

19, 50 25, 65 262/296

Giessen, DE �//Y G/Y Li-Cor 6200 NF, NF�/, NF680,

NF�/680

NF, NF�/, NF680,

NF�/680

23, 51 22, 62 361/431

Jokioinen, FI �//Y G/�/ ADC LCA3 NF, NF�/, NF�/�/ NF, NF�/ 24, 36, 47 36, 56 182/266

Goteborg, SE �//Y G/Y Li-Cor 6200 NF, NF�/, NF680,

NF�/680

CF, NF, NF�/ 24, 42 11, 34, 59 480/630

Goteborg, SE inde-

pendent data set

�/ G Li-Cor 6200 �/ CF, NF, NF�/ 11, 34, 59 480/630

Irrigation�/rainfall data for the chambers were taken from De Temmermann et al. (2002).

H.

Pleijel

eta

l./

Eu

rop

.J

.A

gro

no

my

17

(2

00

2)

30

3�

/31

73

05

tance in that experiment were used as an indepen-

dent data set to test the calibration of the

conductance model. The equipment used for the

measurement of stomatal conductance varied

between the sites that contributed to the present

study (Table 1). Open-top chamber treatments

with both differing ozone concentrations and

elevated carbon dioxide concentrations were in-

cluded in the study. For the yield response study

also data sets without conductance measurements

were included, where sufficient data existed to

drive the conductance model.The measurement strategy in terms of the leaves

that were studied varied to some extent among the

experiments. The vast majority of the measure-

ments was however made on fully developed leaves

in the upper part of the canopy, and measurements

from lower leaves were excluded from the present

study. Most of the conductance measurements in

Giessen, Tervuren and Sutton Bonnington were

carried out using an artificial light source, while all

measurements in Ostad and Jokioinen were per-

formed in natural light.The average duration of the experiments from

emergence until haulm harvest, the period used for

integration of ozone exposure, was 103 days or

1553 8C days above 2 8C expressed as thermal

time.

2.2. The multiplicative stomatal conductance model

and the boundary line technique

The stomatal conductance model concept was

adopted from Emberson et al. (1998), which was

based on earlier work by e.g. Jarvis (1976) and

Korner (1994). In the model, the stomatal con-

ductance gs is assumed to be a multiplicative

function of a number of environmental factors

assumed to act independently:

gs�gmax(gphengO3gVPDgT gPARgtime) (1)

The highest value obtained in the study was

taken as gmax. All the other factors vary between 0

and 1. Thus, the factors either do not influence the

conductance if they are 1, or modify gmax nega-

tively. Since a minimum conductance could not be

identified from the data set no such level was

introduced to the model. The three factors, gVPD,

gT and gPAR, represent the instantaneous influence

exerted by the VPDLA, leaf temperature (TL) and

the PAR on the stomatal conductance, respec-

tively. For the model calibration, the data for these

three environmental factors were obtained from

the cuvette measurements.

Preliminary tests of the model showed that it

tended to overestimate conductance more and

more in the hours following noon. As a conse-

quence, similar to Livingston and Black (1987) a

gtime was introduced, reflecting the influence of the

time of day, which improved the performance of

the model considerably.

The phenological factor gphen is related to the

reduction of the stomatal conductance of senes-

cing leaves (e.g. Vos and Groenwold, 1989). It was

based on the accumulation of thermal time (Tsum,

temperature threshold 2 8C), which is considered

to be a better predictor of the developmental rate

than the number of days (Campbell and Norman,

1998). High ozone concentrations can induce cell

death and promote premature senescence of leaves

(Grandjean and Fuhrer, 1989), thus negatively

affecting the stomatal conductance. The factor

for ozone, gO3, was based on the accumulated

exposure of ozone concentrations (hourly

averages) from emergence until the time of mea-

surement using no concentrations threshold,

AOT0, expressed in mmol mol�1 h, like Gruters

et al. (1995). This was in accordance with the

finding that AOT0 accurately described the long-

term influence of ozone on conductance within the

CHIP programme (Vandermeiren et al., 2002, this

volume). Since the plants were kept well watered

(Table 1), and relevant soil moisture data were not

available, no factor for soil moisture was included

in the model.

The dependence of the different g factors on the

respective environmental variables was identified

using the boundary line technique (Jarvis, 1976;

Livingston and Black, 1987; Emberson et al.,

2000). Jones (1983) was used to find appropriate

mathematical functions for some of the boundary

lines.


2.3. Correction factor for elevated carbon dioxide

Because of the long-term character of the

influence of an elevated carbon dioxide concentra-

tion, and the fact that only two discrete levels of

CO2 (360 and 680 mmol mol�1) were used, a

slightly different approach had to be adopted for

this factor. Based on preliminary inspection of the

data, it was apparent that CO2 was more efficientin reducing the conductance in the higher range of

conductance. Also observed within the CHIP

programme was that the effect of CO2 on stomatal

conductance became manifest early in the season

and remained fairly constant over the entire

growth period (Vandermeiren et al., 2002, this

volume). In line with these two observations, a

time-independent, multiplicative correction factorfor elevated CO2, CCO

2, was added to Eq. (1) after

the influence of the other environmental factors on

conductance had been estimated. For the ambient

concentration of carbon dioxide CCO2

was always

1.

2.4. Calculations of ozone uptake by the leaves

In the present study it was assumed that the

ozone uptake by the leaves in the open-topchambers is determined by the chamber ozone

concentration and two resistances connected in

series: the leaf boundary layer resistance rb and the

stomatal resistance rs. It is normally assumed in

this type of calculations that the concentration of

ozone in the intercellular of the leaves is zero. This

assumption has empirical support (Laisk et al.,

1989). Application of the resistance analogueprinciple (Unsworth et al., 1984) then gives:

Uleaf �[O3]

rb � rs

(2)

where Uleaf is the ozone uptake rate to the leaf

interior per unit leaf area. The value for rb was setconstant, as the fans were operated continuously

at a constant rate. This value was taken from the

work by Unsworth et al. (1984) to be 25 s m�1 for

heat and was recalculated for ozone. The study by

Unsworth et al. (1984) was concerned with soy-

bean. For the present study it was assumed that

the open-top chambers used by Unsworth et al.

(1984) would be representative for the chambers

used in the CHIP programme and that the

boundary layer for potato leaves is close to that

for soybean, the leaf structure not being too

different between the two species. CUO3 denotes

the cumulative uptake of ozone per unit projected

leaf area from emergence until harvest. When an

ozone uptake rate threshold t , was used, the

corresponding cumulative uptake of ozone was

denoted CUO/t3:/

2.5. Tuber yield in relation to ozone exposure

Tuber yield was determined according to the

common protocol of the CHIP programme in all

the different experiments. For details see Craigon

et al. (2002 this volume). Since elevated carbon

dioxide concentrations can interact with the effect

of elevated ozone not only through the effect on

stomatal conductance, treatments with elevated

CO2 were not included in the calculated relation-

ships between ozone exposure and tuber yield.

Relationships between relative yield and external

(AOT40 and SUM06) or estimated internal

(CUO3) ozone exposure were based on the calcu-

lation principles introduced by Fuhrer (1994).

AOT40 is the accumulated ozone exposure over

a concentration threshold of 40 nmol mol�1 based

on hourly averages and SUM06 the sum of hourly

concentrations of ozone exceeding 60

nmol mol�1. The latter exposure index has been

used extensively for ozone in North America,

while AOT40 has mainly been used in Europe.

For CUO3 a test of different ozone uptake rate

thresholds, t , was made in order to find the

relationship with the highest R2 for the relation-

ship between relative yield and ozone exposure. In

the calculation of CUO3, TL was replaced by air

temperature (TA), and consequently VPDLA with

air vapour pressure deficit (VPDA), in Eq. (1),

which introduces a certain degree of systematic

error.

H. Pleijel et al. / Europ. J. Agronomy 17 (2002) 303�/317 307

Table 2

Maximum stomatal conductance, gmax, in the chamber (OTC) treatments and in the ambient air (AA) as well as the total number and number of data points used for the

determination of the different g factors for the stomatal conductance model in the different CHIP experiments

Site Number of data points used for calculations of the g factors

gmax PAR T VPD AOT0 Tsum Time of day CO2

OTC AA OTC AA OTC AA OTC AA OTC AA OTC AA OTC AA OTC AA

Tervuren 1998 640 596 433 27 433 27 433 27 361 0 433 27 433 0 360 0

Tervuren 1999 724 858 524 74 524 74 524 74 524 0 524 74 524 0 436 0

Sutton Bonington 1998 1087 1256 120 27 117 27 117 27 120 0 120 27 120 0 120 0

Sutton Bonington 1999 492 1226 298 76 298 76 298 76 298 0 298 76 298 0 298 0

Giessen 1999 1371 1037 613 27 613 27 613 27 613 0 613 27 613 0 613 0

Jokioinen 1999 810 1160 453 202 0 0 0 0 463 0 463 241 463 0 463 0

Goteborg 1999 1311 �/ 351 0 351 0 351 0 349 0 349 0 351 0 349 0

Sum: 3225 2567 2567 2728 3272 2802 2639

PAR, photosynthetically active radiation, T , leaf temperature, VPD, leaf-to-air vapour pressure difference, AOT0, accumulated exposure of ozone based on hourly

concentration averages, Tsum, thermal time accumulation �/2 8C.

H.

Pleijel

eta

l./

Eu

rop

.J

.A

gro

no

my

17

(2

00

2)

30

3�

/31

73

08

3. Results

3.1. Stomatal conductance in the CHIP

experiments

In Table 2 the maximum conductance obtained

in the different chamber experiments and in the

ambient air is presented along with information on

the number of data points used for the determina-tion of the different g factors. The total number of

conductance measurements used was 3274. The

highest conductance value obtained was 1371

mmol m�2 s�1 in Giessen, which was taken as

gmax for the multiplicative model. All conductance

values are given per unit projected leaf area.

3.1.1. Relationship with solar radiation, gPAR

Stomatal conductance in relation to PAR isshown in Fig. 1. The boundary line shows a rather

typical light saturation curve. Light saturation was

obtained at approximately 400 mmol m�2 s�1. A

majority of the leaf conductance measurements

were made using an artificial light source, mostly

having a PAR value of approximately 1000�/1200

mmol m�2 s�1, or higher. Mainly Swedish mea-

surements, which used natural light, contributewith boundary line points in the lower range of

PAR. The scarcity of measurements at low to

moderate light intensities was a limitation for the

derivation of the relationship between stomatal

conductance and PAR.

3.1.2. Relationship with leaf temperature, gT

The relationship between stomatal conductance

and leaf temperature is presented in Fig. 2. The

temperature optimum for stomatal conductance

was found at approximately 29 8C. The lack of

measurements below 16 8C consisted a limitationfor the calibration of the temperature function. A

mathematical function was used, which smoothly

approaches the x -axis at low and high tempera-

tures in order to obtain physiological realism.

3.1.3. Relationship with VPDLA, gVPD

High levels of VPDLA, in particular those larger

than approximately 20 hPa, induced stomatal

closure. The data and the boundary line are shown

in Fig. 3. Conductance measurements at low

Fig. 1. Stomatal conductance divided by gmax in relation to

PAR and boundary line for gPAR. Data from five different sites

within the CHIP programme. Open square, chamber treatment;

filled diamond, ambient air.

Fig. 2. Stomatal conductance divided by gmax in relation to leaf

temperature (T ) and boundary line for gT. Data from four

different sites within the CHIP programme. Open square,

chamber treatment; filled diamond, ambient air.


VPDLA and boundary line for gVPD. Data from four different

sites within the CHIP programme. Open square, chamber

treatment; filled diamond, ambient air.


VPDLA levels were strongly underrepresented in

the data set, partly due to the problems associated

with the measurement of stomatal conductance in

this range of VPDLA.

3.1.4. Relationship with thermal time, gphen

The phenological development of the plants was

described by the accumulation of thermal time

above a temperature of 2 8C (Tsum). As obvious

from Fig. 4, there was a clear developmental or

senescence effect on the stomatal conductance.

3.1.5. Relationship with cumulative ozone exposure,

gO3

For the conductance modelling, ozone exposure

was described using the accumulated ozone ex-

posure without a concentration threshold, AOT0,expressed in mmol mol�1 h (Fig. 5), which is the

simplest possible way to express ozone exposure

integrated over time. Large ozone exposures,

obtained mainly in the open-top chamber treat-

ments with elevated ozone, caused a decline in the

maximum stomatal conductance.

3.1.6. Relation to time of day, gtime

There was a reduction in the stomatal conduc-

tance during the afternoon, which could not beexplained by the influence of VPDLA, leaf tem-

perature or PAR. The factor representing this

effect, gtime, is presented in Fig. 6. It was based on

a non-linear function, having the value 1 before

noon.

3.1.7. Correction factor for elevated CO2

concentrations, CCO2

To evaluate the effect of elevated carbon dioxideconcentrations a different type of approach was

adopted compared to the g factors. The data from

treatments with elevated CO2 and the parallel

treatments with ambient CO2 concentrations was

sorted in ascending order and divided into 10%-

iles. The ratio between the elevated and ambient

CO2 treatments representing each percentile (first,

second etc.) was calculated. The result is presentedin Fig. 7. Each point represents the conductance

ratio between of the highest values in each 10%-ile

from elevated and ambient CO2. A clear pattern

was obtained where elevated carbon dioxide

reduced the stomatal conductance by approxi-


accumulation of thermal time above 2 8C (Tsum) and bound-

ary line for gphen. Data from five different sites within the CHIP

programme. Open square, chamber treatment; filled diamond,

ambient air.


accumulated ozone exposure expressed as AOT0 and boundary

line for gO3. Data from five different sites within the CHIP

programme.


time of day after noon and boundary line for gtime. Data from

five different sites within the CHIP programme.


mately 20% (i.e. CCO2�/0.8) in the upper range of

stomatal conductance, while in the lowest range of

conductance the CO2 effect was small.

3.2. Model tests

In Fig. 8 the multiplicative model has been run

using the environmental data associated with the

conductance measurements for the three data sets

which provided sufficient information and forwhich the model test regression was statistically

significant. For all three data sets R2 was larger

than 0.40. The highest R2-value (0.60) was ob-

tained for Ostad (Fig. 8B) for which the regression

was not significantly different from the 1:1-line at

P�/0.01 (analysis based on Underwood, 1997).

The regressions for Giessen and the independent

data set were significantly different from the 1:1-

line.

Jokioinen was excluded from this exercise be-

cause sufficient data was not present for all

environmental variables. Sutton Bonnington was

excluded from Fig. 8, and from the regressions in

Fig. 9, since there was no clear relationship

between predicted and observed conductance

(R2�/0.02). In Tervuren, PAR, TL and VPDLA

all had very narrow ranges of variation. Since the

short-term variation of the modelled conductance

is mainly driven by these variables, it is hard to

make a fair test of the model under these

circumstances. The model test for Tervuren was

however statistically significant (P B/0.001, R2�/

0.10), but the deviation from the 1:1-line was

substantial. Tervuren was included in the analysis

in Fig. 9.

The model tended to overestimate low-moderate

conductance, especially in Giessen, but also in the

other two data sets. The deviations from the 1:1

relationship was plotted against the different

environmental variables considered to be impor-

tant for stomatal conductance. It was not possible

to find a systematic variation in this exercise,

which could be used to improve the model

performance. On the contrary, further changes of

the boundary line functions lead to lower perfor-

mance of the model.

Fig. 7. The correction factor for elevated CO2, CCO2, i.e. the

conductance ratio between elevated and ambient CO2. The

points represent the ratio of the highest values for elevated and

ambient CO2 in each 10%-ile. Data from five different sites

within the CHIP programme.

Fig. 8. Calculated stomatal conductance using the multiplicative model plotted against the observed conductance values for all

measurements in (A) Giessen, (B) Ostad and (C) the independent data set from Ostad. The solid line represents the regression and the

broken line the theoretical 1:1 relationship.


3.3. Relationships between ozone exposure and

tuber yield loss for potato

In Fig. 9A�/D, the relationships between relative

tuber yield defined according to Fuhrer (1994) and

the cumulative ozone uptake (CUO/73; CUO/

03);

AOT40 and SUM06, respectively, are presented.

The highest R2 was obtained with CUO/73; which

was statistically significant at P�/0.01. The use of

a CUO3 index with a lower or higher ozone uptake

rate threshold than 7 nmol m�2 s�1 resulted in a

lower R2-value (Fig. 10). The linear regressions

with CUO/03; AOT40 and SUM06 were also statis-

Fig. 9. Relative yield of potato in relation to (A) the calculated ozone uptake by the potato leaves using an ozone uptake threshold of 7

nmol m�2 s�1 (CUO/73); (B) the calculated ozone uptake by the potato leaves using no ozone uptake threshold (CUO/

03); (C) the

accumulated ozone exposure above 40 nmol mol�1 based on hourly averages (AOT40), (D) the sum of all hourly concentrations

exceeding 60 nmol mol�1 (SUM06). Confidence limits for the regression lines are for the degree of significance indicated by the P -

values in the figures.

Fig. 10. R2-values for the regressions between relative yield and

CUO/t3 using different thresholds t for the ozone uptake rate.


tically significant. As evident from Fig. 11 the

threshold for the ozone uptake rate of 7

nmol m�2 s�1 on average corresponded to an

ozone concentration threshold of slightly below

20 nmol mol�1. This was fairly constant among

the four sites included in the yield regression study.

4. Discussion

In relation to the environmental variables in-

cluded in the multiplicative model, PAR, TL,

VPDLA, Thermal time, AOT0 and time-of-day,

the stomatal response pattern was well in accor-

dance with what can be expected from a physio-

logical perspective (Jones, 1983) and fairly similar

to what has been found with other crops such as

wheat (Gruters et al., 1995).

Gordon et al. (1997) obtained light saturation of

the stomatal conductance in potato at around 500

mmol m�2 s�1 PAR, similar to the present study.

Corresponding results in terms of stomatal light

response in potato were also found by Ku et al.

(1977) and Vos and Oyarzun (1987).

It should be noted that no conductance mea-

surements were made at leaf temperatures lower

than approximately 16 8C. This means that for

estimations of gs at lower temperatures in the

relationship between CUO3 and yield effects, the

use of the gT function represents extrapolation.

Since temperature, TL or TA, was used to calculate

VPDLA and VPDA, respectively, one may ask if

there was a strong correlation between gVPD and

Fig. 11. Hourly CUO37 values in relation to hourly ozone concentrations for the experiments in A. Giessen, B. Tervuren, C. Ostad and

D. Jokioinen.


gT. This was tested and turned out not to be thecase (R2 �/0.0087). Consequently, autocorrelation

between gVPD and gT seems to be a minor problem

in the present data set.

Also for the effects of senescence, represented by

thermal time accumulation, and the senescence

promoting effect by ozone there is in principle a

risk for a redundant interaction within the model

(Gruters et al., 1995). In practice this problem waslimited, since in the high ozone treatments gO

3

became limiting to stomatal conductance before

gphen indicated such a limitation in all sites except

Tervuren in 1998, where gphen tended to be more

important as a limiting factor for stomatal con-

ductance than gO3

during the growing season also

in elevated ozone treatments. The senescence effect

on stomatal conductance in the present study wassimilar to that found in potato by Vos and

Groenwold (1989).

For carbon dioxide, the largest effect was

obtained at high conductance. The influence by

carbon dioxide on stomatal conductance is nor-

mally suggested to be associated with a higher

internal carbon dioxide concentration of the leaf.

The result of the present investigation is consistentwith that mechanism. A similar reduction in

stomatal conductance of potato, associated with

elevated CO2, was found by Ku et al. (1977), which

resulted in improved water use efficiency in that

study.

As was the case also in Livingston and Black

(1987), it was necessary to introduce a boundary

line function for time of day after noon in ordernot to overestimate the conductance in the late

afternoon. The reason for this seems to be that the

decline in VPDLA, which typically occurred in the

late afternoon during many days, was not followed

by a stomatal opening of the magnitude suggested

by gVPD. This was probably related to the water

potential of the leaf (Livingston and Black, 1987).

A decline in stomatal conductance with increasingabsolute leaf water potential during the course of

the day was found to occur in potato by Vos and

Oyarzun (1987).

It should be noted in this context that there was

no factor included in the model for soil water

content, since soil water data were not available

and the plants were regularly irrigated. However,

different soils differ considerably in their capacityto store water and there may have existed differ-

ences in the soil water as well as the nutrient status

of the plants, which both are potentially important

to stomatal conductance, and which were not

covered by the model. Another point to consider

is that the equipment used for the measurement of

stomatal conductance was the same in Giessen and

Ostad but different from Tervuren, Jokioinen andSutton Bonnington. Since a detailed common

protocol for conductance measurements (which

existed for several other types of measurements)

was lacking within the CHIP programme, there

may have existed differences in the way measure-

ments were performed. It cannot be completely

excluded that differences in the instrumentation

and measurement practices caused some of thedifferences between the sites.

The maximum conductance values were fairly

high, in the upper range of or higher than what has

been generally reported for broadleaved crops in

the literature (Korner, 1994; Larcher, 1995).

However, a number of factors favouring stomatal

opening have to coincide in order to permit full

stomatal opening. In the field this is only rarely thecase (Korner, 1994). A group of data points from

Giessen fulfilled the requirements for maximum

conductance, the highest of which was chosen as

gmax. Thus, the gmax value did not represent a

single outlier. Considering both the measurements

in the open-top chambers and in the ambient air,

the differences in maximum observed conductance

between sites were not extremely large. In Tervu-ren the highest g values tended to be lower. It

should then be kept in mind that the model never

predicted higher conductance in Tervuren than

approximately 1000 mmol m�2 s�1. This was

related to the narrow variation of some important

environmental variables mentioned in Section 3.3.

The model resulted in a R2-value of 0.59 when

the calibrated model was applied the independentdata set. This is lower than the results found by

Livingston and Black (1987) in three tree species,

where R2 was as high as 0.84�/0.91. Like in the

present study, the model calibrations by these

authors tended to overestimate conductance for

two of the three species, while the deviation from

the 1:1 was very small for the third species.


Livingston and Black (1987), however, had a muchsmaller intercept in the model test regressions than

was the case in the present study. A possible

explanation for that is that many more points with

one or several factors strongly limiting stomatal

conductance, and where both predicted and ob-

served conductance were very low, were included

in the study by Livingston and Black (1987).

Ideally, a broad range of all important factorsshould be present in the data set behind the

calibration of multiplicative conductance model

(Jarvis, 1976).

A critical point for the CUO/73 relationship is the

use of air temperature for the gT and gVPD

functions. The influence of this simplification

was tested and it turned out not to be of a very

large importance. For instance, using air tempera-ture and VPDA instead of leaf temperature and

vapour pressure difference leaf-to-air in Eq. (1),

the regression for Giessen in Fig. 8A changed from

y�/315�/0.84x to y�/377�/0.72x . The corre-

sponding calculated average conductance changed

from 615 nmol m�2 s�1 to 633 nmol m�2 s�1.

An alternative to this approach would be to

calculate leaf temperature, which is also associatedwith a number of assumptions, data needs and

uncertainties.

The exposure index CUO/73 had a higher R2-value

than CUO/03; AOT40 and SUM06. This supports

the idea that ozone uptake related exposure indices

are better at explaining observed effect data than

the more descriptive concepts (Pleijel et al., 2000)

AOT40 and SUM06, which are only based on theconcentration of ozone in the air and thus have no

sensitivity at all to the factors which influence

stomatal conductance. Thus, the fact that no

perfect relationship between modelled and ob-

served conductance was obtained in the present

study has to be viewed from the perspective that

AOT40 and SUM06 basically assume constant

conductance. This is less realistic from a physio-logical point of view than using CUO3 based on

modelled conductance with a relatively high degree

correlation between calculated and observed con-

ductance, although the conductance model de-

viated to a certain extent from the 1:1-relationship.

Fig. 11 shows that the threshold 7 nmol

O3 m�2 s�1 on average started to cumulate quite

consistently at ozone concentrations slightly below20 nmol mol�1. It should be noted that this

should not be taken as a correspondence between

CUO/73 and AOT20. The CUO/

73 accumulation

above 20 nmol mol�1 only takes place to the

extent that stomatal conductance permits a certain

rate of ozone uptake, while the AOT20 exposure

index accumulates all concentrations above 20

nmol mol�1 in direct relation to the degree ofexceedance, regardless of stomatal conductance.

Based on an extensive compilation of existing

information, Borrell et al. (1997) concluded that

preindustrial concentrations of ozone were about

10�/15 nmol mol�1 at ground level. Plants may be

adapted to approximately the level of oxidative

stress imposed by such ozone concentrations.

Antioxidants such as ascorbate in the apoplast inthe leaf interior may be sufficient to completely

detoxify ozone up to a certain uptake rate (Castillo

and Greppin, 1988; Luwe and Heber, 1995). This

is consistent with the finding of the present study

that mainly concentrations above approximately

20 nmol mol�1 contribute to ozone induced yield

loss in potato. A similar conclusion, that concen-

trations from around 20 nmol mol�1 O3 have thepotential to cause adverse effects on plants, was

recently drawn by Grunhage et al. (2001), using a

compilation of toxicological information from a

large number of experiments.

To summarise, CUO3 should not be viewed as

an absolute ozone dose, which is very hard to

determine with high precision. Rather it is an

exposure index which is sensitive not only theconcentration of ozone in the air (like AOT40 and

SUM06), but also to those factors which influence

the stomatal ozone uptake from that concentra-

tion. The improvement obtained using a threshold

for the ozone uptake rate could represent the

biochemical resistance to ozone stress in the

apoplast inside the leaf, although the establish-

ment of such a relationship would have to betested in specific experiments.

Acknowledgements

All data used for the present analysis was

produced within the EU-funded CHIP pro-


gramme, with the exception of the independent

conductance data set from Ostad which was

funded by A.B. Solanum and Lyckeby Starkelse.

The data analysis made by Hakan Pleijel and

Helena Danielsson was funded by the ASTA

programme of the Mistra research foundation,

Sweden.

References

Borrell, P., Builtjes, P.J.H., Grennfelt, P., Hov, Ø. (Eds.),

Photo-oxidants, acidification and tools; policy applications

of EUROTRAC results. Springer, Berlin/Heidelberg/New

York 1997.

Campbell, G.S., Norman, J.M., 1998. An Introduction to

Environmental Biophysics. Springer, Berlin/Heidelberg/

New York.

Castillo, F.J., Greppin, H., 1988. Extracellular ascorbic acid

and enzyme activities related to ascorbic acid metabolism in

Sedum album L. leaves after ozone exposure. Environ. Exp.

Bot. 28, 231�/238.

Craigon, J., Fangmeier, A., Jones, M.H., Donnelly, A., Bindi,

M., De Temmermann, L., Persson, K., Ojanpera, K., 2002.

Growth and yield responses of potato to increasing CO2 and

ozone. Eur. J. Agron. 17, 273�/290.

De Temmermann, L., Wolf, J., Colls, J., Bindi, M., Fangmeier,

A., Finnan, J., Ojanpera, K., Pleijel, H., 2002. Effect of

climatic conditions on tuber yield (Solanum tuberosum L.)

in the European ‘CHIP’ experiments. Eur. J. Agron. 17,

243�/255.

Emberson, L.D., Ashmore, M.R., Cambridge, H.M., 1998.

Development of methodologies for Mapping Level II

Critical Levels of Ozone. DETR Report no. EPG 1/3/82.

Imperial College of London, London.

Emberson, L.D., Ashmore, M.R., Cambridge, H.M., Simpson,

D., Tuovinen, J.-P., 2000. Modelling stomatal ozone flux

across Europe. Environ. Pollut. 109, 403�/413.

Fowler, D., Duyzer, J.H., Baldocchi, D.D., 1991. Inputs of

trace gases particles and cloud droplets to terrestrial

surfaces. Proc. R. Soc. Edinburgh 97B, 35�/59.

Fuhrer, J., 1994. The critical level for ozone to protect

agricultural crops*/An assessment of data from European

open-top chamber experiments. In: Fuhrer, J., Achermann,

B. (Eds.) Critical levels for ozone. A UN-ECE workshop

report. Schriftenreihe der FAC Liebefeld, 16, 42�/57.

Fuhrer, J., 2000. Introduction to the special issue on ozone risk

analysis for vegetation in Europe. Environ. Pollut. 109,

359�/360.

Fuhrer, J., Skarby, L., Ashmore, M.R., 1997. Critical levels for

ozone effects on vegetation in Europe. Environ. Pollut. 97,

91�/106.

Gordon, R.J., Brown, D.M., Dixon, M.A., 1997. Stomatal

resistance of three potato cultivars as influenced by soil

water status, humidity and irradiance. Potato Res. 40, 47�/

57.

Grandjean, A., Fuhrer, J., 1989. Growth and leaf senescence in

spring wheat (Triticum aestivum ) grown at different ozone

concentrations in open-top field chambers. Physiol. Plant.

77, 389�/394.

Grunhage, L., Jager, H.-J., 1994. Influence of the atmospheric

conductivity on the ozone exposure of plants under ambient

conditions: considerations for establishing ozone standards

to protect vegetation. Environ. Pollut. 85, 125�/129.

Grunhage, L., Krause, G.H.M., Kollner, B., Bender, J.,

Weighel, H.-J., Jager, H.-J., Guderian, R., 2001. A new

flux-oriented concept to derive critical levels for ozone to

protect vegetation. Environ. Pollut. 111, 355�/362.

Gruters, U., Fangmeier, A., Jager, H.-J., 1995. Modelling

stomatal responses of spring wheat (Triticum aestivum L.

cv. Turbo) to ozone and different levels of water supply.

Environ. Pollut. 87, 141�/149.

Heck, W.W., Taylor, O.C., Tingey, D.T., 1988. Assessment of

Crop Loss from Air Pollutants. Elsevier Applied Science,

London and New York.

Jager, H.J., Unsworth, M.H., De Temmermann, L., Mathy, P.

(Eds.) 1992. Air Pollution Report 46. Effects of air pollution

on agricultural crops in Europe. Results of the European

Open-Top Chamber Project. Proceedings of the Final

Symposium of the European Open-Top Chamber Projects,

23�/25 November, Tervuren, Belgium. Commission of the

European Communities, Publication no. EUR 14975 EN.

Jarvis, P.G., 1976. The Interpretation of the Variations in Leaf

Water Potential and Stomatal Conductance Found in

Canopies in the Field. Philosophical Transactions of the

Royal Society, London, pp. 593�/610.

Jones, H.G., 1983. Plants and Microclimate. A Quantitative

Approach to Environmental Plant Physiology. Cambridge

University Press.

Karenlampi, L., Skarby, L. 1996. Critical Levels for Ozone in

Europe: Testing and Finalizing the Concepts. UN-ECE

Workshop Report, University of Kuopio.

Korner, C., 1994. Leaf diffusive conductances in the major

vegetation types of the globe. In: Schulze, E.D., Calwell,

M.M. (Eds.), Ecophysiology of Photosynthesis. Ecological

Studies, vol. 100. Springer, Berlin/Heidelberg/New York,

pp. 463�/490.

Ku, S.-B., Edwards, G.E., Tanner, C.B., 1977. Effects of light,

carbon dioxide, and temperature on photosynthesis, oxygen

inhibition of photosynthesis, and transpiration in Solanum

tuberosum . Plant Physiol. 59, 868�/872.

Laisk, A., Kull, O., Moldau, H., 1989. Ozone concentration in

leaf intercellular air space is close to zero. Plant Physiol. 90,

1163�/1167.

Larcher, W., 1995. Physiological Plant Ecology, Third ed..

Springer, Berlin/Heidelberg/New /New York.

Livingston, N.J., Black, T.A., 1987. Stomatal characteristics

and transpiration of three species of conifer seedlings


planted on a high elevation south-facing clear-cut. Can. J.

For. Res. 17, 1273�/1282.

Luwe, M., Heber, U., 1995. Ozone detoxification in the

apoplast and symplast of spinach, broad bean and beech

leaves at ambient and elevated concentrations of ozone in

air. Planta 197, 448�/455.

Pleijel, H., Danielsson, H., Pihl Karlsson, G., Gelang, J.,

Karlsson, P.E., Sellden, G., 2000. An ozone flux-response

relationship for wheat. Environ. Pollut. 109, 453�/462.

Skarby, L., Jonsson, B., 1988. Effects of ozone on crops in

Sweden. Environ. Pollut. 53, 461�/462.

Underwood, A.J., 1997. Experiments in ecology. Their logical

design and interpretation using analysis of variance. Cam-

bridge University Press, Cambridge.

Unsworth, M.H., Heagle, A.S., Heck, W.W., 1984. Gas

exchange in open-top field chambers-II. Resistances to

ozone uptake by soybeans. Atmos. Environ. 18, 381�/385.

Vandermeiren, K., Black, C., Lawson, T., Casanova, A.,

Ojanpera, K., 2002. Photosynthetic responses of potatoes

grown under elevated CO2 and/or ozone concentrations.

Eur. J. Agron 17, 337�/352.

Vos, J., Oyarzun, P.J., 1987. Photosynthesis and stomatal

conductance of potato leaves*/effects of leaf age, irradi-

ance, and leaf water potential. Photosynth. Res. 11, 253�/

264.

Vos, J., Groenwold, J., 1989. Genetic differences in water-use

efficiency, stomatal conductance and carbon isotope frac-

tionation in potato. Potato Res. 32, 113�/121.


stomatal conductance and ozone exposure in relation to potato tuber yield—results from the...

Documents