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Swiss Federal Institute for Forest, Snow and Landscape Research, CH-8903 Birmensdorf, Switzerland
b
Bioenergetics Laboratory, University of Geneva, CH-1254 Jussy Geneva, Switzerland
Received 30 June 1999; accepted 5 January 2000
``Capsule'': A chlorophyll a performance index obtained from uorescence analysis correlates to visual injury and biomass
loss caused by ozone, and thus could be used for the large-scale monitoring of tree vitality.
Abstract
This paper describes a relationship between ozone exposure, biomass, visual symptoms and a chlorophyll a uorescence performance index for young beech trees (Fagus sylvatica). The plants were exposed to four levels of ozone in open-top fumigation
chambers (50, 85, 100% of ambient, and 50% of ambient+30 nl l1 ozone) that uctuated in parallel with ambient ozone during a
single growing season. The trees were fumigated in the four treatments with ozone levels corresponding to an AOT40 (accumulated
exposure above a threshold of 40 nl l1) of 0.01, 3.35, 7.06 and 19.70 ml l1 h, respectively. Highly signicant dierences were found
between the 50% of ambient+30 nl l1 ozone treatment and all other treatments, with a 70.5% reduction in primary photosynthetic performance, as measured with the PI index. The reduction of the PI values demonstrated a high correlation with visual
symptom development (r2=0.98), and by the end of September with biomass loss (r2=0.99). A signicant ozone exposureresponse
relationship was found between AOT40 and primary photochemistry (r2=0.97). Thus, analysis of PI provides an alternative
method for regional monitoring of tree health within the context of the currently employed AOT40. # 2000 Elsevier Science Ltd.
All rights reserved.
Keywords: Fluorescence; Ozone; Biomass; Performance index; Visual symptoms
1. Introduction
Current ozone levels remain a risk to European forests (Skarby et al., 1998). In the determination of an
appropriate ozone critical level, a two-tier approach was
suggested at the 1996 workshop under the UN/ECE
convention on Long-Range Transboundary Air Pollution for abatement strategies to protect vegetation from
ozone injuries. The Level I approach prescribed biomass
loss to be the appropriate biological response parameter
and that beech would be the most appropriate species to
monitor (Karenlampi and Skarby, 1996; Fuhrer et al.,
1997). The Level II approach proposed several additional environmental parameters to also be included due
to their modifying inuence on tree ozone responses. It
was also stated that there was a scarcity of data upon
* Corresponding author. Tel.: +41-22-7591944; fax: +41-227591945.
E-mail address: strasser@uni2a.unige.ch (R.J. Strasser).
0269-7491/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved.
PII: S0269-7491(00)00053-1
502
Table 1
The four ozone exposure treatments (IIV) used in the fumigation of beech trees in open-top chambers, their derivations in relation to the ambient
level of ozone, and measured ozone concentrations and cumulative ozone exposure (AOT40) from April to September 1997
Treatment
I
II
III
IV
a
Treatment type
Pre-industrial level
Reduced level
Level at low altitudes (400700 m a.s.l.)
Level at high altitudes (16001800 m a.s.l.)
S.D., 1 standard deviation.
S.D.a
Minimum
Maximum
50%
85%
100%
50%+30 nl l1
15.3
23.5
27.4
44.0
8.2
12.6
15.1
13.0
0.5
1.0
0.9
3.3
48.7
79.9
102.6
93.5
AOT40
(ml l1 h)
0.01
3.35
7.06
19.70
SFIP
ChlRC =Chltot
'Po
0
SFIN 1 ChlRC =Chltot 1 'Po 1 0
ChlRC
'Po
0
Chlantenna 1 'Po 1 0
PI
503
The index 0 refers to the state at the onset of illumination. The PI dened here refers to photochemical
events, an analogous expression denoted PIN can be
dened for non-photochemical events where:
PIN 1=PI:
or in experimental terms:
3. Results
RC FV 1 VJ
;
PI
VJ
ABS F0
where Chltot is the total quantity of Chl a, and
Chltot Chlantenna ChlRC . The ratio ChlRC/Chlantenna
can be replaced by the ratio RC/ABS, where RC is the
number of active PSII reaction centres, and ABS is
the quantity of light absorbed by the antenna. RC/ABS,
'Po and 0 can be calculated according to the JIP-test
using the experimentally collected parameters (Strasser
and Strasser, 1995; Strasser et al., 1995).
Maximum quantum yield of primary photochemistry:
'Po 1 F0 =FM TR0 =ABS
The ozone fumigation resulted in cumulative exposures (AOT40) of 0.01, 3.35, 7.06 and 19.7 ml l1 h for
the treatments IIV, respectively. AOT40 was calculated
for daylight hours (>50 Wm2) using 1-h mean concentrations in excess of 40 nl l1 ozone, in accordance
with the UN/ECE denition (Karenlampi and Skarby,
1996) (Table 1). Daily levels of hourly mean ozone
concentration in the 50% of ambient+50 nl l1 were
representative of those found at higher altitudes in the
Swiss Alps.
The repeated measures ANOVA calculated the eect
of ozone on the PI between the 50% ambient+50 nl l1
treatment and the other three treatments to be highly
signicant over the entire season (P>0.0026) (Table 2).
The PI values recorded from all plants remained indistinguishable until Day of Year 190, at which time the
50% ambient+30 nl l1 ozone treatment PI values
became increasingly reduced over time compared to the
three other treatments (Fig. 1). The treatment PI means
became signicantly dierent by the fourth measuring
event (P>0.009) (Day of Year 226), and remained so
for the rest of the season. By September, when the
plants had received close to the complete seasons exposure, mean PI was reduced by an average of 70.5, 15.3,
and 1% relative to the control (50% of ambient level).
The development of visual damage was scored from 1,
no visual symptom, to 5, large necrotic areas. The rst
visual symptoms developed at about the same time
as the mean PI value for trees in the 50% of ambient+
30 nl l1 treatment started to diverge from the other
504
Table 2
The results of a repeated measures ANOVA, testing the between and within treatment eects of four ozone treatments on beech trees from two
provenances using the primary photosynthetic performance index (PI) are showna
df
Between-treatment eects
Treatment (error = *)
Provenance (error = **)
Treatmentprovenance**
*Replication (Treatment) (error = **)
Tree (Treatmentreplication rovenance)
**Leaf
Within-treatment effects
Day of Year (DY)
DYtreatment
DYprovenance
DYtreatmentprovenance
DYreplication (Treatment)
DYtree (Treatmentreplicationprovenance)
Leaf (DY) error
Huynh-Feldt "
Mean square
P>F
3
1
3
15
15
150
21.586
0.106
1.041
2.855
2.53
0.082
0.0026
0.2577
0.0001
0.0001
0.0001
7
21
7
21
105
105
1050
21.223
2.187
0.759
0.166
0.44
0.372
0.086
0.0001
0.0001
0.0001
0.0069
0.0001
0.0001
1.0947
Replications refer to ve open-top chambers within each treatment. The degrees of freedom (df) and the mean square data are shown from
which the F-test probabilities were calculated (P>F ). Asterisks indicate the specic error terms used at each level of the model.
Fig. 2. The inverse of the mean performance index (PIN) versus mean
visual symptom score. PIN means were repeatedly measured during the
season as visual symptoms developed. Error bars are calculated as 1
S.E.
505
Fig. 4. Performance index (PI) and the inverse of the mean performance index (PIN) versus cumulative AOT40 ozone exposure. Data
points represent means repeatedly recorded during the 1997 season as
the trees exposure to the seasons cumulative ozone increased. All
ozone treatments are included. Error bars are calculated as 1 S.E.
4. Discussion
Exposure to ozone signicantly reduces the photosynthetic performance of beech over a single growing
season, as measured by the PI index. This response
demonstrated that the energy transduction process
around PSII lost performance, conrming previous
research using Chl a uorimetry (Mikkelsen, 1995;
Mikkelsen and Heide-Jorgensen, 1996; Clark et al.,
1998) and carbon dioxide gas exchange methods
506
Acknowledgement
This work was supported by the Swiss National
Science Foundation.
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