Environmental and Experimental Botany 44 2000 69 – 82
Impacts of urban levels of ozone on Pinus halepensis foliage
Costanza Soda
a
, Filippo Bussotti
a,
, Paolo Grossoni
a
, Jeremy Barnes
b
, Bruno Mori
a
, Corrado Tani
a
a
Department of Plant Biology, Uni6ersity of Florence, Piazzale delle Cascine
28
, I-
50144
Firenze, Italy
b
Air Pollution Laboratory, Department of Agricultural and En6ironmental Science, Ridley Building, The Uni6ersity of Newcastle Upon Tyne, Newcastle NE
1 7
RU, UK Received 4 February 2000; received in revised form 10 April 2000; accepted 13 April 2000
Abstract
Between May and September, 1996, seedlings of Pinus halepensis were placed at a site adjacent to an automated air pollution monitoring station within the urban area of Florence. Additional ‘control’ plants were placed in chambers
ventilated with charcoalPurafil
®
-filtered air. All trees were well watered throughout the whole experimental period. During the exposure period, ambient levels of sulphur dioxide were very low, whilst the accumulated hourly exposure
to ozone above 40 ppb i.e. AOT40 exceeded 20 000 ppb h
− 1
— peak hourly ozone concentrations rising to levels above 100 ppb. Trees exposed to ambient levels of air pollution exhibited typical symptoms of ozone damage
chlorotic mottle on previous year needles toward the end of the summer. Similar symptoms were not observed on equivalent trees exposed to filtered-air, nor were visible symptoms accompanied by insect or pest infestation.
Anatomical and ultrastructural observations made on symptomatic needles revealed degeneration in mesophyll cells bordering sub-stomatal cavities and alterations in chloroplast ultrastructure fat accumulation, starch and tannin
pattern modifications. These observations are consistent with the known effects of air pollutants namely ozone recorded in the literature. Findings are discussed in relation to the impacts of ozone on P. halepensis in the
Mediterranean region. © 2000 Elsevier Science B.V. All rights reserved.
Keywords
:
Cell ultrastructure; Mediterranean; Sulphur dioxide; Symptomatology; Urban air www.elsevier.comlocateenvexpbot
1. Introduction
Visible symptoms attributed to the pervasive photochemical air pollutant ozone have been
recorded for many years on the needles of several pine species in California and the South-Eastern
United States Miller et al., 1963; Miller and Millecan, 1971; Evans and Miller, 1972a,b; Miller
and Evans, 1974; Fox and Mickler, 1995; Ar- baugh et al., 1998; Chappelka and Samuelson,
1998, as well as in the mountains bordering Mexico City Hernandez Tejeda and Nieto de
Pascual, 1996; Alvarez et al., 1998. In Europe, among coniferous trees, visible symptoms of foliar
injury appear to be restricted to a single species, Aleppo pine Pinus halepensis, the most common
landscape tree of the Mediterranean littoral. The
Corresponding author. E-mail address
:
filippo.bussottiunifi.it F. Bussotti. S0098-847200 - see front matter © 2000 Elsevier Science B.V. All rights reserved.
PII: S 0 0 9 8 - 8 4 7 2 0 0 0 0 0 5 5 - 1
question of whether this species is particularly sensitive to ozone remains to be established see
Barnes et al., 1999. However, ambient concentra- tions of the pollutant are known to be particularly
high in the Mediterranean region Gimeno et al., 1994 because of the high summer temperatures
and radiations, and the natural distribution of this species is coincident with the highest ground level
ozone
concentrations experienced
in Europe
Butkovic et al., 1990; Milla´n et al., 1996. Ac- cording to the UN-ECE standards Ka¨renlampi
and Ska¨rbi, 1996; Fuhrer et al., 1997; Fuhrer and Achermann, 1999, risks for forests are currently
evaluated in Europe with the index AOT40 accu- mulated hourly ozone exposure above 40 ppb
threshold. AOT40 values exceeding 10 000 ppb.h are considered dangerous for forest vegetation
Level I Critical Levels. The threshold of 40 ppb was chosen to exclude the non-anthropogenic
ozone, but this threshold has been seriously ques- tioned. Sutinen et al. 1990, for example, found
that considerably lower ambient ozone concentra- tions about 30 ppb caused ultrastructural alter-
ations on Picea abies needles.
Typical visible symptoms of ozone injury on the needles of P. halepensis have been observed in
California Ka¨renlampi, 1987 and in several parts of Southern Europe Gimeno et al., 1992; Velis-
sariou et al., 1992; Davison et al., 1995; Gimeno et al., 1995; Velissariou et al., 1996. These symp-
toms comprise chlorotic mottling that becomes visible towards the end of summer or early winter
Velissariou et al., 1996. Previous year C + 1 needles are primarily affected Ka¨renlampi, 1987;
Davison et al., 1995, though current year C needles can be affected if trees are exposed to
particularly high levels of the pollutant see Barnes et al. 1999. In the most severe cases, the
symptoms degenerate into necrosis and are associ- ated with premature needle loss. The chlorotic
mottle observed is considered a specific symptom of ozone injury, since the same symptoms have
been reproduced during several controlled or semi-controlled exposures of P. halepensis to
ozone Gimeno et al., 1992; Wellburn and Well- burn, 1994; Elvira et al., 1995; Anttonen et al.,
1998. Several ultrastructural studies have been car-
ried-out on symptomatic needles of P. halepensis in order to characterize the histological changes
induced by ozone Ka¨renlampi, 1986, 1987; Anttonen et al., 1994; Wellburn and Wellburn,
1994. Most of these studies have been performed on plant material exposed to ozone under con-
trolled or semi-controlled conditions Anttonen et al., 1994; Wellburn and Wellburn, 1994, although
one study was conducted on trees exposed in the field Ka¨renlampi, 1986, 1987. Findings have
been variable, presumably because of differences in the way in which trees have been exposed to
the pollutant cf. Anttonen et al., 1998 and the fact that several studies have focused on the ef-
fects on juvenile needles on young seedlings rather than effects on mature needles of forest trees
Kelly et al., 1995; Kolb et al., 1998.
In this study, we examined i the relationship between ambient concentrations of ozone at an
urban Mediterranean location and the appearance of visible symptoms on the needles of P. halepen-
sis, ii the impacts of ambient levels of ozone on needle ultrastructure and iii compared the ob-
served ultrastructural modifications with those de- scribed in the literature as typical of ozone
damage in this species.
2. Materials and methods
