*Corresponding author. Tel.: #44-1248-370045; fax: #44-1248-355365.E-mail address: gmi@ceh.ac.uk (G. Mills).�The United Nations Economic Commission for Europe.

Atmospheric Environment 35 (2001) 2583}2587

Short communication

Evidence of ozone-induced adverse e!ects on crops in theMediterranean region

Ivano Fumagalli�, Benjamin S. Gimeno�, Dimitris Velissariou�,Ludwig De Temmerman�, Gina Mills��*

�ENEL-Ricerca, via Reggio Emilia 39, 20090 Segrate (MI), Italy�ICP-Vegetation Steering Committee, CIEMAT, Avda Complutense 22, 28040 Madrid, Spain�Technological Educational Institute of Kalamata, Antikalamos 241 00, Kalamata, Greece

�ICP-Vegetation Steering Committee, Veterinary and Agrochemical Research Centre (VAR), B-3080 Tervuren, Belgium�ICP Vegetation Centre for Ecology and Hydrology, Bangor Research Unit, Deiniol Road, Bangor, LL57 2UP, UK

Received 1 March 2000; received in revised form 28 September 2000; accepted 4 October 2000

Abstract

The impacts of ambient ozone pollution on crops in the Mediterranean countries have been recorded regularly in theso-called `grey literaturea of UN/ECE Workshop Reports for the Convention on Long-range Transboundary AirPollution, and less frequently in the peer-reviewed literature. This short communication reviews such records and showsthat ambient ozone episodes have been reported to cause visible injury on 24 agricultural and horticultural crops grownin commercial "elds including three of the most important crops in the region (wheat, maize, and grapevine). On oneoccasion, the damage was so extensive that complete crop loss occurred in commercial glasshouses of Butterhead lettucein one area of Greece. Experiments with open-top chambers have indicated that ambient ozone caused 17}39% yield lossin crops such as wheat, bean, watermelon and tomato. The applicability of the long-term critical level of ozone describedby Fuhrer et al. (Environ. Pollut. 97 (1997) 91) for the Mediterranean areas is also considered. � 2001 Elsevier ScienceLtd. All rights reserved.

Keywords: Ambient ozone; Ozone injury; Agricultural crops; Horticultural crops; Yield reduction

1. Introduction

Recently, an article by FrancoDe Santis was publishedin the `New Directionsa section of this journal (De San-tis, 1999). The paper questions the scienti"c basis of thecritical level for ozone that has been adopted by theUN/ECE� and its applicability in Mediterranean areas.Ashmore and Fuhrer (2000) in reply to the De Santispaper have provided details on the scienti"c basis of thecritical level and the limitations of extrapolating yield

reductions from the O�dose}wheat response function

that was used to derive the critical level for O�(see

Fuhrer et al., 1997). De Santis (2000) has commentedfurther by reiterating that there needs to be scienti"cevidence of damage caused by ozone in Mediterraneanareas before policy makers could have the con"dence toimplement new control measures. The comments in thesepapers drew our attention to the shortage of informationon the e!ects of ambient ozone on crops in Mediterra-nean areas in the peer-reviewed literature, even thoughnumerous papers have been published in the so-calledgrey literature of UN/ECE Workshop Reports (e.g.KaK renlampi and SkaK rby, 1996; Fuhrer and Achermann,1999). In this paper, we summarise the published in-formation and report that O

�is actually a!ecting sensi-

tive receptors in the Mediterranean area. Most of thesestudies have been carried out under the framework of the

1352-2310/01/$ - see front matter � 2001 Elsevier Science Ltd. All rights reserved.PII: S 1 3 5 2 - 2 3 1 0 ( 0 0 ) 0 0 4 6 8 - 4

Table 1Reports of incidences of visible ozone injury on commercial agricultural and horticultural crops in the Mediterranean area

Agricultural crop Reference

Bean Phaseolus vulgaris Lorenzini et al. (1984); Panattoni et al. (1990); Elvira et al. (1992); Schenone etal. (1992); Gimeno et al. (1995a); Velissariou et al. (1996); Benton et al. (2000)

Clover Trifolium repens Fumagalli et al. (1997); Benton et al. (2000)Trifolium alexandrinum Velissariou and Kyriazi (1996)

Corn Zea mays Velissariou et al. (1996)Grapevine Vitis vinifera Lorenzini et al. (1984); Salleras et al. (1989); Gimeno et al. (1995a); Velissariou

et al. (1996)Peanut Arachis hypogea Gimeno et al. (1995a)Potato Solanum tuberosum Gimeno et al. (1995a); Velissariou et al. (1996)Soybean Glycine maxima Lorenzini et al. (1984); Salleras et al. (1989); Schenone (1993); Gimeno et al.

(1995a)Tobacco Nicotiana tabacum Gimeno et al. (1995a); Velissariou et al. (1996)Wheat Triticum aestivum Velissariou et al. (1996)

Triticum durumHorticultural crop Reference

Courgette Cucurbita pepo Schenone and Lorenzini (1992); Velissariou et al. (1996)Chicory Chicorium endiva Velissariou et al. (1996); Velissariou (1999)Lettuce Lactuca sativa Velissariou (1999)Muskmelon Cucumis melo Velissariou et al. (1996)Onion Allium cepa Gimeno et al. (1995a); Velissariou et al. (1996)Parsley Petroselinum sativum Velissariou et al. (1996)Peach Prunus persica Paolacci et al. (1995)Pepper Capiscum anuum Lorenzini and Panattoni (1986)Radish Raphanus sativus Lorenzini and Panattoni (1986)Red beetroot Beta vulgaris Velissariou et al. (1996); Velissariou (1999)Spinach Spinacea oleracea Lorenzini and Panattoni (1986)Tomato Lycopersicon esculentum Lorenzini et al. (1984); Gimeno et al. (1995a)Watermelon Citrullus lanatus Reinert et al. (1992); Gimeno et al. (1995b); Velissariou et al. (1996);

Gimeno et al. (1999a)

� International Cooperative Programme on E!ects of AirPollution on Natural Vegetation and Crops.

UN/ECE ICP Vegetation� (formerly ICP-Crops) for theConvention on Long-Range Transboundary Air Pollu-tion. We also make some comments on the applicabilityof the critical level to this region.

2. Records of ozone-induced visible injury in theMediterranean area

Ozone injury commonly appears as small #ecks orstipples on the interveinal areas of the upper surface ofleaves. The #ecks may be white, red, black or bronzedepending on species and may coalesce to form extensiveareas of chlorosis as the leaf ages. In 1996, Velissariou etal. compiled the references reporting the presence of suchinjury on 22 crop species grown in commercial "elds inItaly, Greece and Spain following ambient ozone epi-

sodes. The list has been updated in Table 1 and includesseveral of the most important commercial crops in thesecountries. For example, ozone injury has been detectedon commercial wheat, maize and grapevine which to-gether are grown on over one-third of the agriculturalareas of these three countries. Some reports have in-dicated the presence of visible injury on sensitive speciesover wide areas, for example, Gimeno et al. (1995a)reported ozone injury on watermelon grown in a600�40km area of eastern Spain. On a more localisedscale, e!ects can be catastrophic for farmers. Forexample, Velissariou (1999) reported 100% crop loss forlettuce and chicory in the Acharnes area of Greece (12 kmnorth of Athens) following an ozone episode in mid-October, 1998. The extensive reddening and necroticsymptoms meant that these two horticultural crops wereunsaleable. Financial losses as high as 12,500 ECU werereported for a single one-acre glasshouse of `Butterheadalettuce. Interestingly, the irrigated "eld crops of Chicorywere damaged by the episode whereas the drought-stressed crops were not. Thus, these "eld observationscon"rmed the experimental evidence that drought-stress

2584 I. Fumagalli et al. / Atmospheric Environment 35 (2001) 2583}2587

may protect crops from ozone injury by partial or com-plete stomatal closure leading to reduced uptake (Tingeyand Hogsett, 1985).The results of several bioindication/biomonitoring

studies involving the use of tobacco cultivars have re-ported the presence of visible O

�injury in the Po valley

(Mignanego et al., 1992) and Tuscany (Lorenzini et al.,1995; Toncelli and Lorenzini, 1999) in Italy, in easternSpain (Gimeno et al., 1995b; Ribas et al., 1998) and inGreece (Velissariou et al., 1992). Similarly, the ICP Veg-etation biomonitoring experiments performed in the re-gion in 1995 and 1996 have reported the presence ofvisible injury on bean, clover, watermelon, tomato andclover (Benton et al., 2000). Injury occurred on whiteclover at Italian sites near Milan, Naples and Rome on75}100% of the four to six 28-day harvest intervals peryear between 1994}1997 (UN/ECE, 1999) and 1998}1999(Mills, unpublished). In summary, both biomonitoringexperiments and "eld observations have indicated thatozone injury is widespread on numerous crops grown inthe Mediterranean region.

3. Reports of ozone-induced losses on yield and biomass ofagricultural crops of the Mediterranean region

There is experimental evidence (Schenone et al., 1992;Fumagalli and Mignanego, 1996; Fumagalli et al., 1999;Gimeno et al., 1996, 1999a) indicating that ambientO

�concentrations in the Mediterranean region induce

yield losses on crops such as wheat (20}27%), beans(17}31%), watermelon (19}39%) and tomatoes (17}24%). Reductions in the total dry weight of clover(20}40%) have also been described (Ball et al., 1998;Fumagalli et al., 1997; Mills et al., 2000). These yieldlosses have been reported for well-watered crops andcould potentially occur in the "eld where irrigation isextensively used during ozone episodes. Ozone-inducedlosses on horticultural crops can be greater than expectedas O

�e!ects might be more apparent in early harvests

when the crop value is the greatest (Gimeno et al., 1996,1999a) or O

�might enhance the sensitivity of plants to

pathogens such as viruses (Gimeno et al., 1999b). Recentpublished work of the experiments performed by the ICPVegetation throughout Europe has highlighted the in#u-ence of other environmental factors such as temperatureand NO

�on O

�phytotoxicity (Ball et al., 1998; Mills

et al., 2000; Pen� uelas et al., 1999).

4. The applicability of critical levels in the Mediterraneanregion

As the paper by Ashmore and Fuhrer (2000) haspointed out, the critical level for O

�(Level I) only indi-

cates the exposure above which risks to plant perfor-mance are expected. Therefore, the actual impact cannotbe derived from the dose}response function that wasconstructed for wheat grown in northern and centralEurope if the receptor and/or the conditions under whichthe receptor was grown are changed. The Mediterraneanscientists that attended the UN/ECE Ozone CriticalLevels Workshops were very keen to underline this fact(see Gimeno et al. (1994), and the report of the Cropsgroup in KaK renlampi and SkaK rby (1996)). In a "rst at-tempt to overcome this problem, Fumagalli et al. (1999)constructed a preliminary ozone dose}response curveinvolving a combination of yield losses reported in someexperiments that have been performed in Italy by ENEL.Interestingly, a linear regression "tted the data althoughthe slope of the regression was slightly smaller than thatreported for wheat in northern Europe (Fuhrer et al.,1997). The suitability of the ozone response function ofFuhrer et al. (1997) for use in southern European coun-tries, was also tested by Alonso et al. (1999) by analysingyield data and soil moisture conditions for ten years of"eld data from a site in Central Spain. It was concludedthat predicted yield losses for wheat grown in Mediterra-nean conditions would be about half of the losses in-dicated by the ozone response function of Fuhrer et al.(1997). Alonso et al. (1999) also derived a new correctionfactor for the in#uence of soil moisture content on durumwheat (Triticum durum) yield, and applied it to the wheat(Triticum aestivum) AOT40 response-function of Fuhreret al. (1997). For purposes of comparison, it was assumedthat T. durum was of equal sensitivity to ozone asT. aestivum. Using this approach, the estimated yieldlosses for T. durum at the site in Central Spain were15}80% of those predicted by Fuhrer et al. (1997) forirrigated wheat. E!ects on T. durum might be even lowerthan this as Reichenauer et al. (1998) found that theExtradur cultivar of this species was less sensitive toozone than the two cultivars of T. aestivum (Nando andPerlo) tested.

5. Conclusion

There is plenty of evidence that ambient O�concentra-

tions adversely a!ect Mediterranean crops of higheconomic value such as horticultural crops, which arenormally irrigated. Where ozone injury is extensive,complete commercial losses can occur in crops such aslettuce and chicory where value is dependent upon blem-ish-free appearance of the leaves. In irrigated conditions,ambient ozone concentrations in the Mediterraneanregion have been linked with yield losses in the range17}39% in crops such as wheat, bean, watermelon andtomato. However, O

�e!ects on the yield of wheat plants

grown under Mediterranean conditions (without irriga-tion) are undoubtedly lower than expected from the

I. Fumagalli et al. / Atmospheric Environment 35 (2001) 2583}2587 2585

equation presented in Fuhrer et al. (1997); further work isrequired before such e!ects can be accurately quanti"ed.The ICP Vegetation is now working to further address

the issues raised in this paper. Firstly, the ICP is perform-ing "eld-based experiments throughout Europe to assessthe in#uence of several environmental factors on O

�phytotoxicity. Secondly, models are being developed toassess O

�#ux to crops in the Mediterranean region

to assess how factors such as water availability couldmitigate O

�response in di!erent plant receptors. Finally,

the ICP is aiming to ascertain the role of O�on the

biodiversity of grasslands.

Acknowledgements

Financial support from the UK Department of theEnvironment, Transport, and the Regions for the coord-ination of the ICP Vegetation is gratefully acknowledged(Contracts EPG 1/3/96) and EPG (1/3/10).

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