ARTICLE IN PRESS
DTD 5
Environmental Pollution
--
(2005)
---e---
www.elsevier.com/locate/envpol
UV-B radiation and acclimation in timberline plants
Minna Turunen a,*, Kirsi Latola b
a
Arctic Centre, University of Lapland, PO Box 122, FI-96101 Rovaniemi, Finland
b
Thule Institute, PO Box 7300, FI-90014 University of Oulu, Oulu, Finland
Received 10 December 2004; accepted 31 January 2005
More long-term field research is needed to assess the interaction of climate, soil and UV-B on timberline plants.
Abstract
Research has shown that some plants respond to enhanced UV-B radiation by producing smaller and thicker leaves, by
increasing the thickness of epidermis and concentration of UV-B absorbing compounds of their surface layers and activation of the
antioxidant defence system. The response of high-altitude plants to UV-B radiation in controlled conditions is often less pronounced
compared to low-altitude plants, which shows that the alpine timberline plants are adapted to UV-B. These plants may have
a simultaneous co-tolerance for several stress factors: acclimation or adaptation to the harsh climate can also increase tolerance to
UV-B radiation, and vice versa. On the other hand, alpine timberline plants of northern latitudes may be less protected against
increasing UV-B radiation than plants from more southern latitudes and higher elevations due to harsh conditions and weaker
preadaptation resulting from lower UV-B radiation exposure. It is evident that more long-term experimental field research is needed
in order to study the interaction of climate, soil and UV-B irradiance on the timberline plants.
Ó 2005 Elsevier Ltd. All rights reserved.
Keywords: UV-B irradiance; Northern timberline; Alpine timberline; Woody plants; Conifers; Acclimation; Adaptation; UV defence mechanisms;
Co-tolerance
1. Introduction
The timberline ecotone is a latitudinal or altitudinal
transition zone between continuous forest and treeless
terrain, where trees struggle to survive by attempting to
adapt their regeneration, growth forms, statures and
physiological and genetic properties to the extreme
conditions. Many theories and hypotheses have been
suggested that climate is a determinant for the location of
the timberline, or treeline, i.e. the extreme limit at which
trees still achieve arboreal form and size (Stevens and
* Corresponding author. Tel.: C358 16 341 2774; fax: C358 16 341
2777.
E-mail address: minna.turunen@ulapland.fi (M. Turunen).
0269-7491/$ - see front matter Ó 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envpol.2005.01.030
Fox, 1991; AMAP, 1998; Veijola, 1998; Tuhkanen, 1999;
Gervais et al., 2002). Theories also stress the significance
of frosts, frost desiccation, wind and irradiance in the
formation of this ecotone. In addition, topographic and
edaphic factors, forest fires, plant diseases, insect
infestations and human activities can be locally important (Tranquillini, 1979; Körner, 1998, 1999; Veijola,
1998; Wardle, 1998; Tuhkanen, 1999; Karlsson and
Weih, 2001; Boyce et al., 2002; Vostral et al., 2002). The
timberline is a heterogeneous boundary in both an
ecological and a taxonomic sense, and therefore different
tree species constitute the latitudinal and altitudinal
timberlines in different parts of the world. Polar
timberline is encountered in the Northern Hemisphere,
and therefore terms like arctic or northern timberline
are used. The northern timberline between the boreal
ARTICLE IN PRESS
DTD 5
2
M. Turunen, K. Latola / Environmental Pollution
coniferous forest and tundra zone is formed by about ten
species of evergreen and deciduous conifers, especially in
continental areas, and by ten broad-leaved species in
oceanic areas (Apps et al., 1993; Veijola, 1998; Tuhkanen, 1999). Taxonomically the trees forming the northern timberline are different on the two sides of the
Atlantic, although the habitats of the northern species
and their responses to the environment are very similar.
Latitudinal and altitudinal timberlines coincide in Polar
Regions, so the timberlines in high latitudes can be
characterized by the ecological factors of both high
altitudes and arctic climates (AMAP, 1998; Veijola,
1998; Tuhkanen, 1999).
The climatic and edaphic conditions of the alpine
timberline vary greatly depending on latitudinal location, topography, exposition and altitude, but in general,
low temperatures, rapid temperature changes, poor soil,
strong winds and extended periods of high irradiance
levels are often characteristic of alpine timberline
habitats. Alpine timberline vegetation is characterised
by decreasing plant species diversity and abundance with
increasing altitude (Körner, 1999). On the other hand,
the biodiversity of the alpine timberline itself is wider
than that in either of the ecosystems adjoining the
ecotone. Isolated trees or small stands of trees on the
alpine timberline are characterized by shapes ranging
from tall and erect to short and thick trunks, to flagging
crowns, and to hedge-like and prostate krummholz in
response to increased exposure, and above the treeline
they can often persist only as shrubs or thickets. Most
importantly, alpine plant groups are of low stature or
prostative woody shrubs, graminoids such as grasses and
sedges that mostly form tussocks, herbaceous perennials
that often form rosettes and cushion plants of various
types. In these ecosystems, plants are often adapted to
harsh conditions by perennial, dwarfed, slow-growing
characteristics, and by developing small and thick
evergreen leaves. Cryptograms, bryophytes, lichens,
algae and fungi may also play an important role (Baig
and Tranquillini, 1976; Tranquillini, 1979; AMAP, 1998;
Körner, 1998, 1999).
The amount of UV-B irradiance (ultraviolet-B,
280e315 nm) reaching the Earth’s surface is influenced
by latitudinal gradients in total atmospheric ozone
column thickness, solar zenith angles, elevation above
sea level, albedo (surface reflectivity) clouds and aerosols
(Blumthaler et al., 1997; Webb, 1997; AMAP, 1998;
Björn et al., 1998; Gröbner et al., 2000). Due to high
altitude, unshaded environments with sparsely-growing
small trees and albedo from the long lasting snow cover
and glaciers, irradiance levels on the alpine timberline
during clear sky conditions can be high and stressful for
plant life (Jokela et al., 1993; Blumthaler et al., 1997;
Gröbner et al., 2000). The values for many irradiance
parameters, e.g. annual global net radiation, UV-B,
UV-A (ultraviolet-A, 315e400 nm), visible and PAR
--
(2005)
---e---
(photosynthetically active radiation) rise on many alpine
timberlines and are associated with the zonation of the
boreal and arctic vegetation (Blumthaler et al., 1997;
Björn et al., 1998). The UV-B contribution to total solar
radiation tends to increase with altitude because of
a thinner, relatively unpolluted and more transparent
atmosphere in many mountainous regions. Air pressure,
i.e. the mass of air above, decreases in a vertical direction
by about 125 millibar for one kilometre, which corresponds to about an 8% per km increase in PAR under
summer conditions in Northern Scandinavia. For the
first kilometre above sea level, the increase in biologically
effective radiation is 15e20% depending on how clean
the air is, and assuming there are no clouds below this
elevation. However, the long-term means of UV-B
radiation are strongly dampened by cloudiness, which
also tends to increase with altitude (Körner, 1999). The
combination of latitudinal and altitudinal trends yields
maximum UV-exposure in tropical-alpine and minimum
in arctic lowland plants. In arctic regions, UV-B
radiation levels are lower than at temperate latitudes,
but the relative ozone depletion and the relative increase
in UV-B anticipated in the arctic are larger than at lower
latitudes and this is probably more important for the
timberline plant life than absolute radiation levels
(Webb, 1997; AMAP, 1998; Björn et al., 1998). Recent
overviews have been published on the research projects
studying the response of terrestrial ecosystems to UV-B
radiation from various climatic and geographical zones
including the arctic and subarctic (Gwynn-Jones et al.,
1999; Björn, 2002), grassland (Rozema et al., 1999;
Campbell et al., 1999), Mediterranean (Manetas, 1999;
Musil and Wand, 1999), South American (Ballare et al.,
1999, 2001) and Antarctic ecosystems (Huiskes et al.,
1999; Robinson et al., 2003). A number of reviews have
discussed the direct and indirect effects of enhanced and
ambient UV-B radiation on vascular plants (Jansen
et al., 1998; Laakso and Huttunen, 1998; Searles et al.,
2001; Day, 2001; Day and Neale, 2002), some paying
special attention to plant defence mechanisms against
UV-B radiation (Jones and Hartley, 1998; Bornman,
1999; Cockell and Knowland, 1999; Meijkamp et al.,
1999; Jordan, 2002). This work discusses the effects of
UV-B radiation on the woody plants of the alpine
timberlines, with special emphasis on the northern
latitudes.1 We briefly review earlier research on UV-B
transmittance and oxidative stress defence and then
discuss the sensitivity of timberline plants to UV-B
radiation and their possible co-tolerance with other
stress factors.
1
The term ‘‘timberline’’ is used in a general sense to refer to the
transition belt from forests to treeless vegetation, ‘‘northern timberline’’ referring to polar latitudinal timberline of the Northern
Hemisphere and ‘‘alpine timberline’’ referring to timberline in
accordance with increasing elevation.
ARTICLE IN PRESS
DTD 5
M. Turunen, K. Latola / Environmental Pollution
2. UV-B transmittance in timberline plants
Timberline plants can avoid solar UV-B-irradiance
stress by increased leaf-surface reflectance, thickness of
the epidermis, the concentration and type of UV-Babsorbing compounds located in leaf epidermal cells,
cuticle, waxes or hairs, by placing developing sensitive
tissue below ground or enveloping it with bud scales or
by phenological timing related to reproductive effort
and biomass production (Caldwell, 1968; Ziska et al.,
1992; Yang et al., 1995; Schnitzler et al., 1996; Lavola,
1998; Turunen et al., 1999a,b; Körner, 1999; Kinnunen
et al., 2001; Jordan, 2002; Lavola et al., 2003). When
UV-B radiation has penetrated through the epidermis
into the photosynthesizing mesophyll, antioxidant systems (see ‘‘Oxidative stress defence’’) and DNA repair
processes play an important role in the defence against
UV-B damage (Foyer et al., 1994; Jordan, 2002).
It has been shown that UV reflectance from the leaf
surfaces depends on the optical properties of the surface,
which is largely determined by the structure of the
leaves, epicuticular wax and leaf hairs (Robberecht
et al., 1980; Vogelmann, 1993; Holmes and Keiller,
2002). The reflectance of UV radiation from the leaf
surface of most plant species studied so far has generally
been below 10%, and therefore it is considered a less
important defence mechanism against UV-B irradiance
when compared to UV-B absorption (Caldwell, 1968;
Robberecht et al., 1980; Vogelmann, 1993; Yang et al.,
1995; Hoque and Remus, 1999; Holmes and Keiller,
2002). In an early work, Caldwell (1968) studied UV-A
reflectance of 13 mountain and 18 alpine species in the
Rocky Mountains of the United States, 1800 and 3750
m a.s.l. respectively, and found no difference between
these two groups with reflectance ranging from 1.5 to
7%. In conifer species with a bluish appearance in the
needles (glaucous blue due to epicuticular wax), e.g. in
blue spruce (Picea pungens), UV-B radiation is reflected
more effectively from the needle surface than in species
with greenish appearance (Clark and Lister, 1975;
Vogelmann, 1993). Reflectivity from Scots pine (Pinus
sylvestris) needles was 5.5% at 315 nm, and it decreased
slightly with increasing wavelength, being 3.3% at
400 nm (Hoque and Remus, 1999). Holmes and Keiller
(2002) recently studied the total reflectance of ultraviolet
(330 nm) and photosynthetically effective (680 nm)
wavelengths for a range of different leaf types and
concluded that both pubescence (presence of hairs) and
glaucousness (presence of a thick epicuticular wax layer)
had a marked effects on total reflectance. Glaucous
leaves were very effective reflectors of both UV and
longer wavelength radiation, whereas pubescent leaves
tended to be more effective in reflecting longer wavelengths than ultraviolet radiation.
The epidermal transmittance of UV-B radiation
correlates with plant life forms, but it is still uncertain
--
(2005)
---e---
3
how well it is related to UV-B-mediated damage or
damage-repair mechanisms (Day et al., 1992; Sullivan
et al., 1996; Bilger et al., 2001). The UV-B-transmittance
of Rocky Mountain plants varied from zero to 40%,
being lower in the most typical timberline plants, e.g.
conifers than in herbaceous dicots. In conifer needles,
UV-B transmittance has varied in the range of
0.5e2.5%, depending on the altitude, age of the needles
and trees, species and measurement techniques (Day
et al., 1992, 1994; Sullivan et al., 1996; Turunen et al.,
1999a). It has been shown that removal of epicuticular
waxes does not significantly increase UV-B transmittance into needle mesophyll (Bornman and Vogelmann,
1988; Day et al., 1992). The reason for the low UV-Btransmittance in conifer needles is that the UV-B
absorbing compounds are located in vacuoles as well
as within epidermal cell walls, whereas in herbaceous
dicots they are located primarily in the vacuole of the
epidermal cell. The two primary groups of UV-B
absorbing compounds, identified as soluble flavonoids
and insoluble phenyl-propanoids of hydroxycinnamic
acids, both have major absorption bands in the range of
304e350 nm and 352e385 nm respectively. Although
these compounds absorb UV wavelengths effectively,
they transmit visible or PAR into the mesophyll cells.
Soluble flavonoids can be actively and rapidly mediated
by UV-B exposure whereas cell-wall bound insoluble
phenyl-propanoids represent a more passive UV screening mechanism (Schnitzler et al., 1996; Hoque and
Remus, 1999; Turunen et al., 1999a,b; Jordan, 2002;
Lavola et al., 2003). It is also possible that UV radiation
could be converted into PAR by the epidermis (Hoque
and Remus, 1999).
Tables 1 and 2 show that the increased UV-B
absorption of plant foliage is often related to increased
altitude and that different species, and populations of
the same species and genus, can exhibit wide UV-B
acclimation potential (Larson et al., 1990; Ziska et al.,
1992; Sullivan et al., 1992; Wand, 1995; Rau and
Hofmann, 1996). For example, significant altitudedependent relationship with the UV-B absorbance of
foliage was found in Hunsruck of Rhineland Palatinate
(131e816 m a.s.l.) in Germany for the wood anemone
(Anemone nemorosa), a spring geophyte, but for
blueberry (Vaccinium myrtillus) and Fuchs grounsel
(Senecio fuchsii), which are forest under storey species,
no such relationship could be seen (Neitzke, 2002).
Correspondingly, in the same region, the UV-B absorbance of the sun leaves of beech (Fagus sylvatica)
increased with elevation but no such relationship could
be seen in shade leaves (Neitzke and Therburg, 2000).
In addition, the composition of flavonoids can vary
according to altitude and latitude. For example, the
Scots pine populations growing at high altitudes and
latitudes were rich in prodelphinidin, whilst low-altitude
and low-latitude populations were rich in taxifolin
4
Table 1
Studies on the adaptive characteristics of plants at the timberline
Response to altitude
Reference
Nederland, Colorado, Rocky
Mountains, USA (40N, 10W)
1800 and 3750
Growing
season
UV exclusion over the
alpine tundra community
No difference in reflectance
of the species from two
altitudes
Caldwell, 1968
Patscherkofer Mountain (near
Innsbruck), Austria (47N, 11E)
1000e2140
Winter
Picea abies, Pinus
cembra samples
collected from
wind-exposed and
wind-protected branches
from sun-exposed side
Thickness of cuticle decreased
at higher altitudes
Baig and
Tranquillini, 1976
Peru (10S)
Venezuela (10N)
Maui, Hawaii (20N)
Barrow and Atkasook, Alaska (71N)
3000e4000
3000e4000
2500e3000
2
Spring and
early summer
All species were collected
from exposed habitats
(43 species)
At higher latitudes, mean epidermal
transmittance exceeded 5%, at low latitudes
transmittance was less than 2%
Robberecht
et al., 1980
Mt. Mooselauke (44N, 71E)
732e1455
Winter
Abies balsamea,
samples collected
Thickness of cuticle decreased in high
altitude
DeLucia and
Berlyn, 1983
Melcheben, Stubalpe (47N, 14E)
and Tullnerbach near Vienna
(48N, 16E)
400e1700
January and
February
Picea abies
No difference in thiol content, but the sulfhydryl
content was higher at high altitude. Higher
wintertime values of thiol content and glutatione
reductase activity were recorded at high altitude
Grill et al., 1988
Most northern location above
Polar Circle in Sweden and most
southern in Sierra Nevada Spain
Survey from
different
locations from
170 to 1700
Not mentioned
Pinus sylvestris needles
collected from nature or
from plantations
Two flavonoid chemomorphs were found. The
high altitude or latitude populations were almost
entirely made up prodelphinidin at low altitude
exhibits o-dihydroxylated flavonoids (quercetin
and taxifolin)
Laracine-Pittet
and Lebreton, 1988
Southern Appalachian Mountains,
USA (37N, 80E)
Not mentioned
Plants potted
in early spring
Phytotron studies on
species from NE and SW
slopes. Rhododendron
maximum (valley),
R. periclymenoides
(NE slopes), Kalmia
latifolia (SW slopes)
R. maximum was the most sensitive
to high radiation. Both
R. periclymenoides and Kalmia
latifolia improved their photosynthetic
performance at high irradiance
Lipscomb and
Nilsen, 1990
Mt. Mooselauke (44N, 71E)
760e1140
March 1989
Picea rubens, samples
collected from east and
west sides
Cuticular resistance to water loss decreased
with elevation. Sun-exposed shoots lost more
water than shaded shoots
Herrick and
Friedland, 1991
Wank mountain in the Bavarian
Calcareous Alps
870e1700
May, mid-June,
mid-September,
early November
and January
90 to 140-years-old
Picea abies
Ascorbate, GSH, GR, SOD levels
were higher in needles obtained from
high altitude
Polle and
Rennenberg, 1992
Kleinrivier Mountains South
Africa (34S, 19E)
100e824
From February
towards the end
of the summer
Sun and shade leaves
collected from 38 species
representing 17 families
UV-B absorbance (280 to 320 nm)
was higher in leaves collected from
high elevation
Wand, 1995
(2005)
ARTICLE IN PRESS
Origin of material
--
Sampling
time
DTD 5
Altitude (m a.s.l.)
M. Turunen, K. Latola / Environmental Pollution
Location
---e---
ARTICLE IN PRESS
DTD 5
Neitzke, 2002
UV-B absorbance of the
Anemone nemorosa leaves increased
with increasing elevation; no effect in
Vaccinium myrtillus or Senecio fuchsia
Wood anemone
(Anemone nemorosa),
Blueberry (Vaccinium
myrtillus), Fuchs grounsel
(Senecio fuchsia)
1050e2170
131e816
Dolomites (NE Italian Alps),
Italy (46N, 12E)
Hunsruck, Rhineland-Palatinate,
Germany
Not mentioned
Anfodillo
et al., 2002
In both species the cuticle was thicker and contact
angles were higher in high altitude trees
131e816
Hunsruck, Rhineland-Palatinate,
Germany
Dec -93, Feb -94,
May -94, Aug -94
Picea abies, Pinus cembra,
samples collected from
windward north-side and
leeward south-side
Neitzke and
Therburg, 2000
UV-B absorbance of sun leaves of Beech (Fagus
sylvatica) increased with increasing elevation
Beech (Fagus sylvatica)
450e3030
Not mentioned
--
(2005)
---e---
5
(Laracine-Pittet and Lebreton, 1988). In addition, two
other studies have reported significant differences in the
characteristics of UV absorbing compounds among
Pinus and Betula populations of different geographical
origins (Kaundun et al., 1998; Lavola, 1998).
3. Oxidative stress defence
Ötztal/Obergurgl, Austria
July and August 1992,
mostly between 1100 and
1600 h
Samples collected from
nine species
A strong correlation between
antioxidant content, particularly
ascorbic acid, and elevation
Wildi and Lutz, 1996
M. Turunen, K. Latola / Environmental Pollution
Plants normally increase several components of the
antioxidative system simultaneously in response to
naturally occurring stresses such as stress at high
altitude, chilling, drought, or nutrient deficiencies (Polle
and Rennenberg, 1994; Tausz et al., 2003) (Table 1).
However, there is no consensus about whether different
stresses that generate active oxygen species (AOS) would
cause a similar activation of AOS scavenging systems
(Rao et al., 1996). Recently, Tegischer et al. (2002)
found that the needles of mature trees had less photoprotective potential, but higher antioxidative potentials
when compared with seedlings and saplings. A decreased capacity for photoprotection might impose
a higher oxidative load on the radical scavenger systems
because the production rate of AOS would increase and
it must be counteracted with increased antioxidative
defence involving glutathione, ascorbate and tocopherols (Tegischer et al., 2002).
In conifers, the glutathione (GSH) levels follow the
diurnal and seasonal cycle (Polle and Rennenberg, 1994;
Wildi and Lutz, 1996). A light-dependent increase in the
GSH concentration of Norway spruce needles causes
a diurnal cycle with high concentrations during the day
and low concentrations at night (Schupp and Rennenberg, 1988). High wintertime levels of GSH (Esterbauer
and Grill, 1978; Schupp and Rennenberg, 1988; Polle
and Rennenberg, 1992) could mean that glutathione
plays a role in the winter hardiness of the foliage of
evergreen plant by protecting it against winter injury.
Thus, in the colder environment on the timberline,
glutathione may have an even more important role in
protection against the harsh climate. Streb et al. (1998)
indicated that the leaves of high-mountain plants were
highly resistant to photoinhibitory damage at low
temperature and exhibited divergent strategies of
photosynthetic adaptation. This could be due to higher
levels of antioxidants observed in high altitude plants.
For example, Norway spruces growing at high altitude
have higher levels of GSH and higher glutathione
reductase (GR) activities compared to ones growing at
low altitudes (Grill et al., 1988; Polle and Rennenberg,
1992). The high levels of GSH and the high GR activity
during periods of high light intensity around noon and
at high altitudes could protect plants against UV-B
radiation (Bielawski and Joy, 1986; Noctor et al., 1997).
On the other hand, a low background UV-B level might
stimulate the antioxidative systems and thereby mediate
6
Table 2
Studies on the response of plants from different altitudes to UV-B irradiance
0e1524
Seven species of seed-grown conifer seedlings
of high, intermediate and low altitude
exposed to UV-BDNA (0, 2.34, 4.78, 7.17,
9,56 Wmÿ2, 11 wk) in phytotron
Biomass production of high altitude species
were least influenced by UV-B radiation
Kossuth and Biggs, 1980
36e41N (WY, NC, MD, USA)
30e3000
Ten species of seed-grown
conifer seedlings of high,
intermediate and low altitude
exposed to UV-BBE (0, 12.4,
19.1 kJmÿ2, 22 wk) in
greenhouse
Effects of supplemental UV-B
dose were less for growth and
stress symptoms of species
native to higher elevations
Sullivan and Teramura, 1988
Not mentioned, probably
Urbana, Illinois, USA
Alpine and
non-alpine
region
Seed-grown seedlings of alpine (Aquilegia
caerulea) and non-alpine (Aquilegia canadensis)
species of Colombine exposed to UV-BBE
(19 kJmÿ2, 14 wk) in controlled conditions
Height growth was inhibited more in non-alpine
species while the number of leaves increased faster
in alpine species. No UV-B effects in photosynthetic
capacity and stomatal conductance was found, but
flavonoid contents increased
Larson et al., 1990
20N Maui, Hawaii, USA
0e3000
Seeds of 33 species collected, germinated and
grown in greenhouse, 0, 15.5 or 23.1 kJmÿ2
UV-BBE, 12 wk
Large differences between species, but in general,
high elevation species showed smaller response
in plant height and biomass
Sullivan et al., 1992
20N Maui, Hawaii, USA
0e3000
Seeds of 33 species were collected, germinated
and grown in greenhouse, 0, 15.5 or
23.1 kJmÿ2 UV-BBE for 12 weeks
UV-B resulted in e.g. earlier reproductive effort and
increased photosynthesis in plants from high elevations.
Increases in UV-B absorbing compounds for low
elevation species, but not for high elevation species which
had larger amounts even in the absence of UV-B
Ziska et al., 1992
52 N 4E Hoogezand, Netherlands
47N 15E Vorarlberg, Austria
0e2
1600
Seed-grown Silene vulgaris seedlings
and mature plants exposed to UV-B
in greenhouse (0, 10, 16.2 kJmÿ2
UV-BBE, 18e20 d, two experiments)
Growth rates, gas exchange rates, transpiration and
biochemical parameters did not show a difference in
the response to enhanced UV-B
Van de Staaij et al., 1995
52 N 4E Hoogezand, Netherlands
47N 15E Vorarlberg, Austria
0e2
1600
Seed-grown Silene vulgaris seedlings
and mature plants exposed to UV-B
in greenhouse (0, 6, 16.2 kJmÿ2 UV-BBE)
Lowland population showed a decrease in the number
of seed producing flowers and the number of seeds per
plant under elevated UV-B. Individual seed mass, seed
germination percentages were unaffected
Van de Staaij et al., 1997
European Alps
>1200
ÿ1000
ÿ500
Seed-grown plants from species pairs or
triplets of 5 genera grown with
(150 mWmÿ2) or without UV-B, then
exposed to UV-B (600, 1000 mWmÿ2)
15 hdÿ1 in growth chambers, many
experiments during 3 yrs
In 2 genera the alpine species exhibited a better
adaptation to UV-B pre-irrigation
Rau and Hofmann, 1996
Rocky Mountains,
SE Wyoming, USA
2488
3567
Potted seedlings (2488 m a.s.l) and natural
field saplings (3567 m a.s.l.) of lodgepole
pine (Pinus contorta ssp. latifolia) grown
under UV-exclusion 10 and 13 wk,
respectively
No treatment effects in epidermal transmittance for
naturally grown saplings at 3567 elevation
Turunen et al., 1999a
ARTICLE IN PRESS
North Carolina, Oregon,
Florida, Washington, USA
---e---
Reference
(2005)
Response
--
Species and origin of material
DTD 5
Altitude
(m a.s.l.)
M. Turunen, K. Latola / Environmental Pollution
Location
ARTICLE IN PRESS
DTD 5
37N, 101E Qinghai-Tibet Plateu,
China
3200
Saussurea superba, Gentiana straminea
in an alpine meadow were exposed to
UV-BBE (15,80 kJ dÿ1, one growing
season from May -99 onwards)
No treatment effects in photosynthetic
CO2 uptake or photosynthetic O2
evolution rate, photosynthetic pigments
on area basis increased, leaf thickness
increased
Shi et al., 2004
M. Turunen, K. Latola / Environmental Pollution
--
(2005)
---e---
7
enhanced cross-tolerance to other environmental stress
factors (Polle, 1997).
More attention has been paid over the past five years
to the effects of UV-B radiation on oxidative stress as
well as to the role of phenylpropanoids as antioxidants
in plants. UV-B radiation may produce such extreme
stress in terms of active oxygen production that the local
antioxidative systems are overwhelmed (Foyer et al.,
1994). In laboratories, UV-B exposure can increase the
activity of several oxidative stress defence systems, but
the effect is less clear under field conditions (Day, 2001;
Tausz et al., 2003). Enhanced UV-B exposure has
increased oxidative stress in crop plants (Takeuchi
et al., 1996; Dai et al., 1997; Kalbin et al., 1997),
herbaceous plants (Hideg and Vass, 1996; Rao et al.,
1996; Hideg et al., 1997) and aquatic organisms
(Malanga and Puntarulo, 1995; Jansen et al., 1996) in
laboratories. A phytochamber study on the interactive
effects of ozone (O3) and UV-B on oxidative stress in
Norway spruce and Scots pine (Pinus sylvestris) indicated that pine needles exposed to UV-B and elevated
O3 levels had elevated lipid peroxidation and a 5-fold
increase in dehydroascorbate, suggesting that pine was
less protected and suffered greater oxidative stress than
spruce. UV-B radiation with ambient O3 levels increased
the total superoxide dismutase activity in spruce, but no
changes in superoxide dismutase, ascorbate, glutathione
or peroxidase activities were seen in pine (Baumbusch
et al., 1998). As shown by several authors (i.e. Mirecki
and Teramura, 1984; Flint et al., 1985; Cen and
Bornman, 1990; Fernbach and Mohr, 1992; Jordan
et al., 1992; Mackerness et al., 1996) the effects of UV-B
in laboratory experiments are more pronounced and not
relevant to natural environments.
A long-term UV-B field experiment was established
in Oulu, Northern Finland to study more realistic
responses of the oxidative stress of mature Scots pines to
UV-B radiation. In this study, UV-B stress was observed
in the two-year-old needles of mature Scots pines as
a degradation of total glutathione, and a bigger proportion of oxidized glutathione in July during the third
UV-B exposure season. In current-year needles, no
increase in oxidized glutathione was seen in either the
first or the third season. After the third experimental
season in September, the total glutathione levels decreased in UV-B-treated current-year needles. These
results suggested that the effect of UV-B on the
oxidative stress of mature Scots pines could be
duration-dependent and cumulative (Laakso et al.,
2001). This is consistent with previous short-term
experiments on Norway spruce and Scots pine needles
(Baumbusch et al., 1998) and pear shoots (Predieri et al.,
1995), which did not show any UV-B effects on
glutathione status. No evidence for cumulative UV-B
effects on oxidative stress was found in the deciduous
dwarf shrub bilberry (Vaccinium myrtillus L.) after seven
ARTICLE IN PRESS
DTD 5
8
M. Turunen, K. Latola / Environmental Pollution
growing seasons of UV-B exposure at Abisko, Swedish
Lapland, where it was shown that there was scarcely any
response in the oxidative stress in ascorbate and
glutathione concentrations, and activities of the closely
related enzymes ascorbate peroxidase and glutathione
reductase (Taulavuori et al., 1998). More field studies
are needed to find out the long-term effects of UV-B
radiation on oxidative stress of the plants, particularly
in the stressful environment of the timberline.
4. Is UV-B radiation stressful to timberline plants?
A meta-analysis of 62 field-based research papers
published over 20 years indicated that the effects of
enhanced UV-B were most apparent for UV-B absorbing compounds, with an increase in concentration of
approximately 10% across all studies when comparing
ambient solar UV-B control to treatment (ambient
UV-B plus supplemental UV-B), but little or no
response was found for plant height and leaf mass per
area (Searles et al., 2001). Another recent meta-analysis
reviewed 36 arctic field studies, and concluded that
arctic plants are not affected in the short term by
increases in UV-B radiation e instead, temperature
elevation, increases in nutrient availability and major
decreases in light availability were more meaningful
for plant-growth and nutrient cycling (Dormann and
Woodin, 2002). However, how will timberline plants
react to increasing UV-B radiation? It has been shown
that natural plant populations exhibit wide variation
in UV-B radiation sensitivity, which is related to the
ambient UV environment in which these plants grow
and therefore reflects the long-term adaptation of plants
to radiation conditions (Larson et al., 1990; Sullivan
et al., 1992; Van de Staaij et al., 1997).
Table 2 indicates that enhanced UV-B radiation in
controlled conditions has resulted in less pronounced
effects of UV-B irradiance on high-altitude plant species
versus low-altitude species, which shows that alpine
plants are adapted to higher UV-B levels. This was
shown by Larson et al. (1990), who exposed seedlings of
alpine (Aquilegia caerulea) and non-alpine (Aquilegia
canadensis) species of Aquilegia to enhanced UV-B
radiation in controlled conditions. They found that
height growth was inhibited more in non-alpine species
while the number of leaves increased faster in alpine
species. No UV-B effects in photosynthetic capacity and
stomatal conductance were found, but flavonoid contents increased. Sullivan et al. (1992) collected seeds of
33 species along a 3000 m a.s.l. altitudinal gradient in
Hawaii, exposed seedlings to UV-BBE (15.5 or 23.1
kJmÿ2 for 12 weeks weighted with the generalized plant
response action spectrum) in controlled conditions, and
found that the response to UV-B varied among species.
--
(2005)
---e---
In general, high elevation provenances again showed
smaller response in plant height and biomass.
The response of lodgepole pine (Pinus contorta ssp.
latifolia Engelm.) needles to natural sunlight was studied
by employing two different UV-exclusion experiments at
high elevation field sites in the Rocky Mountains
(potted seedlings at 2488 m a.s.l, and natural field
saplings at 3567 m a.s.l.). No differences among treatments were found in epidermal transmittance (!2.5%)
for naturally-grown saplings at 3567 elevation (Turunen
et al., 1999a), which agrees with earlier research
reporting an increase in UV-B absorbing compounds
after exposure to supplemental UV-B radiation in plants
grown at low elevation but not in those grown at high
elevation (Larson et al., 1990; Sullivan et al., 1992; Van
de Staaij et al., 1997).
Probably the most stressful time for the timberline
plants is the spring, when the solar radiation dose, and
particularly the UV dose received by conifers and alpine
plants emerging from the snow cover, may be particularly high. The plants may experience strong, but often
short radiation stress at the start of their growing season
due to reflectance of irradiance from the surrounding
snow cover (albedo) and are therefore exposed to the
direct effects of UV-B radiation. UV-B albedos for most
ground covers are !0.1, but much higher values can be
encountered for snow, typically 0.8 for fresh and dry
snow, and lower values for old, wet and dirty snow. On
a clear day, new snow can reflect over 90% of all the
incoming UV radiation on vertical surfaces, and thin
cloud cover can cause the multiple reflections of UV rays
between snow and clouds, increasing the UV dose in all
directions (DeLucia et al., 1991; Jokela et al., 1993;
Björn et al., 1998; Körner, 1999; Gröbner et al., 2000).
Within two days, or within a few hours, when snow
melts, plant tissue may become exposed to high
intensities of solar radiation. It is likely that mature
and hardened evergreen conifers and alpine plants can
defend their photosynthesis from direct radiation stress
by increasing concentrations of compounds absorbing
visible UV-A and/or UV-B radiation, or by increasing
the thickness of their leaves. Recently, Shi et al. (2004)
exposed Saussurea superba and Gentiana straminea to
UV-BBE radiation for one growing season (15.80 kJmÿ2
dÿ1), at an alpine meadow on the Qinghai-Tibet Plateau
in China (3200 m a.s.l) and found evidence that the
increase in leaf thickness in both species could compensate for the photodestruction of photosynthetic pigments when light passes through the leaf.
It is not known, however, if still dormant and/or
premature tissue with undeveloped epidermis, cuticle or
epicuticular wax, due to a short and cold growing
season, suddenly released from snow, can defend against
radiation stress. During the spring, undeveloped epidermal cells in expanding conifer needles are not sufficiently
able to absorb UV radiation and it can therefore
ARTICLE IN PRESS
DTD 5
M. Turunen, K. Latola / Environmental Pollution
penetrate into the mesophyll (DeLucia et al., 1992). The
fascicular sheath protects the developing needle but it
probably does not block all gas exchange and the
penetration of PAR and UV-B radiation (Chabot and
Chabot, 1975; Dvorák and Stokrová, 1993). It has been
suggested that mesophyll cells may become photosynthetically active while they are still within the fascicular
sheaths, since the chlorophyll (aCb) content was high
and the necessary gas exchange was possible due to
the well-developed stomatal complexes (Chabot and
Chabot, 1975; Dvorák and Stokrová, 1993). Thus, particularly in emerging and expanding leaves, increased
penetration of UV-B radiation into the mesophyll may
disrupt physiological and developmental processes
(DeLucia et al., 1992).
5. Co-tolerance for several stress factors?
It is interesting to speculate whether structural and
physiological acclimation or adaptation to the harsh
climate, particularly drought and low temperatures,
and poor soil also provide protection against increasing
UV-B radiation. On the other hand, are the plants in
the northern timberline environment more sensitive to
UV-B radiation due to harsh conditions and weaker
preadaptation due to naturally lower UV-B radiation
compared to plants from more southern latitudes and
elevations? And vice versa: does defence against increased UV-B radiation, such as thicker epidermal layer
and cutin, increased concentration of UV-B absorbing
compounds in the epidermal cells, and higher levels of
glutathione (Laakso et al., 2000, 2001; Turunen et al.,
1999a,b; Kinnunen et al., 2001), increase the plants’
tolerance against another environmental stresses such as
drought and low temperatures? Most probably all these
statements are true.
Many xerophytic plants with thick leaves and an
epidermal cell layer are adapted to both water stress and
high irradiance. It has been shown that many drought
tolerators are generally resistant to UV-B damage and
that enhanced UV-B radiation can induce xeromorphic
characteristics, such as a thicker cutin layer, in northern
conifers (Laakso et al., 2000) or in Mediterranean species
(Manetas, 1999). Latola et al. (2001) found that increased
UV-B decreased the cross-sectional needle area of fullygrown fascicle needles of Scots pines. Since no decrease in
needle length was seen, it was suggested that the smaller
cross-sectional area was due to the more xeromorphic
structure of UV-B-treated needles. In primary needles of
Scots pine seedlings, UV-B increased the thickness of the
cutin layer and the outer and inner periclinal walls and
the anticlinal wall thickened to fill cell lumen, which are
common features in xeromorphic needles (Laakso et al.,
2000). Thus, the xeromorphic structure might give better
protection also against UV-B radiation and on the other
--
(2005)
---e---
9
hand, the enhanced UV-B radiation may cause a more
xeromorphic structure in evergreens.
There are several other examples of the existing cotolerance to UV-B radiation and drought, UV-B
radiation, and low temperatures. The fact that UV-B
radiation can act as an environmental signal to induce
tolerance to high light and drought stress in Douglas fir
(Pseudotsuga menziesii) seedlings was demonstrated by
Poulson et al. (2002). They investigated the effects of an
ambient dose of UV-B radiation on chamber-grown
seedlings and found that the presence of ambient UV-B
radiation in the growth light regime induced the
production of UV-B absorbing pigments and that the
seedlings had 30% fewer stomata per unit leaf area
compared with control seedlings. Reduced stomatal
frequency in response to UV-B radiation may limit
water loss by seedlings and/or decrease the potential for
leaf cooling through evapotranspiration. UV-B radiation has also been reported to increase cold tolerance in
the plant species typical to timberline regions (Dunning
et al., 1994; Mendez et al., 1999). Both cold stress and
UV-B exposure are known to increase synthesis and the
accumulation of phenolic compounds (Bäck et al., 1993;
Jones and Hartley, 1998) and, for example, increased
anthocyanin concentrations may play a role in protection against photoinhibition, UV-B radiation, desiccation and freezing resistance (Chalker-Scott, 1999;
Hoch et al., 2001).
Timberline plants may be poorly protected against
UV-B radiation due to the harsh climate. Table 1 shows
that, depending on microclimatic and edaphic conditions, cuticle thickness, the amount of epicuticular waxes
and wettability of alpine timberline plants, particularly
conifer needles, either decrease, increase or remain
unchanged with increasing altitude. A decrease in cuticle
thickness with increasing altitude has been reported for
Balsam fir (Abies balsamea) Norway spruce (Picea abies)
and Stone pine (Pinus cembra). Gunthardt and Wanner
(1982) found an increase in the total amount of waxes in
high-elevation Stone pine and Norway spruce trees and
Sase et al. (1998) showed a similar trend in Japanesecedar (Cryptomeria japonica). On the other hand,
Anfodillo et al. (2002) studied minimum cuticular
conductance and cuticle features of Norway spruce and
Stone pine needles along an altitudinal gradient of 1050e
2170 m a.s.l. of the Dolomites (NE Italian Alps), where
the treeline is seldom subjected to strong winds. They
found no effect of altitude in minimum cuticular
conductance in either species. In this study, the
wettability of the needle surface was lower in highaltitude needles than it was in low-altitude needles, the
cuticle was thicker in needles of high-altitude trees than
in needles of low-altitude trees, and there was no
correlation between minimum cuticular conductance
and cuticle thickness, meaning that the desiccation
resistance did not decrease with altitude in either species.
ARTICLE IN PRESS
DTD 5
10
M. Turunen, K. Latola / Environmental Pollution
Short and cool growing seasons may delay the
development of protective epidermis, cuticles and the
epicuticular wax of evergreen foliage (Turunen and
Huttunen, 1990, 1991, 1996; Kinnunen et al., 2001),
which may then contain less UV-B-absorbing compounds, and at the same time, low temperatures may
slow down the enzymatic and non-enzymatic UV-B
repair processes (Foyer et al., 1994). This may predispose timberline plants to additional stresses particularly during the early spring, such as photoinhibition
due to high irradiance levels and winter desiccation
(Tranquillini, 1979; Strand and Öquist, 1985; Ottander
and Öquist, 1991). Classical studies in Europe and the
USA have showed that the role of protective surface
layers in woody plants may be vitally important in
alpine timberline conditions. The decreased cuticular
transport of water vapour in conifer needles due to the
reduced allocation of carbon for the development of
cuticle increased the risk of winter desiccation in the
Alps of Central Europe (Baig and Tranquillini, 1976;
Tranquillini, 1979), and direct mechanical damage to the
surface layers and stomatal dysfunction due to windblown snow and ice contributed more to conifer winter
deaths in the alpine treeline in Scotland (Grace, 1990)
and the Rocky Mountains of the United States (Hadley
and Smith, 1990). Thin cuticles and the low amount of
wax in timberline plants could also mean less protection
against UV-B radiation. Epicuticular wax itself may not
play a major role in the UV-B screening of the
timberline plants, however. The cuticular layer has been
found to thicken due to increased UV-B radiation, thus
protecting photosynhetical tissue, mesophyll, against
harmful radiation. In Scots pine for example, both the
well-developed wax layer and thick epidermis prevent
UV-B penetration. Kinnunen et al. (2001) found that
young developing Scots pine needles with undeveloped
epicuticular waxes had a higher amount of UVabsorbing compounds than fully-grown needles with
well-developed wax indicating that the defence mechanisms vary with the needle age. This shows that if one
protection mechanism is unable to function then other
mechanisms take over.
6. Conclusions
It has been shown that many plants respond to
enhanced UV-B radiation by producing smaller and
thicker leaves, by increasing the thickness of the cutin
layer and the epidermal wall, and by increasing
concentrations of UV-B absorbing compounds in the
epidermal cells, waxes and leaf hairs, and activation of
the antioxidant defence system. Alpine timberline plants
may have a simultaneous co-tolerance for several stress
factors, such as drought, high UV-B, UV-A, PAR or
low temperatures. On the other hand, they may be worst
protected against increasing UV-B radiation than plants
--
(2005)
---e---
from southern latitudes and higher elevations due to
harsh conditions and weaker preadaptation resulting
from comparatively lower UV-B radiation exposure.
This review suggests that more long-term experimental
field research is needed in order to study the interaction
of harsh climate, poor soil and UV-B irradiance on the
ecophysiology and defence mechanisms of timberline
plants.
Acknowledgments
This work was funded by the Thule Institute of the
University of Oulu.
References
AMAP, 1998. AMAP Assessment Report: Arctic Pollution Issues.
Arctic Monitoring and Assessment Programme (AMAP). Oslo,
Norway.
Anfodillo, T., Di Bisceglie, D.P., Urso, T., 2002. Minimum cuticular
conductance and cuticle features of Picea abies and Pinus cembra
needles along an altitudinal gradient in the Dolomites (NE Italian
Alps). Tree Physiology 22, 479e487.
Apps, M.J., Kurz, W.A., Luxmoore, R.J., Nilsson, L.O., Sedjo, R.A.,
Schmidt, R., Simpson, L.G., Vinson, T.S., 1993. Boreal forests and
tundra. Water, Air and Soil Pollution 70, 39e53.
Bäck, J., Huttunen, S., Kristen, U., 1993. Carbohydrate distribution
and cellular injuries in acid rain and cold-treated spruce needles.
Trees 8, 75e84.
Baig, M.N., Tranquillini, W., 1976. Studies on upper timberline:
morphology and anatomy of Norway spruce (Picea abies) and
stone pine (Pinus cembra) needles from various habitat conditions.
Canadian Journal of Botany 54, 1622e1632.
Ballare, C.L., Scopel, A.L., Mazza, C.A., 1999. Effects of solar UV-B
radiation on terrestrial ecosystems: case studies from southern
South America. In: Rozema, J. (Ed.), Stratospheric Ozone
Depletion. The Effects of Enhanced UV-B Radiation on Terrestrial
Ecosystems. Backhuys Publishers, Leiden, pp. 293e311.
Ballare, C.L., Rousseaux, M.C., Searles, P.S., Zaller, J.G.,
Giordano, C.V., Robson, T.M., Caldwell, M.M., Sala, O.E.,
Scopel, A.L., 2001. Impacts of solar ultraviolet-B radiation on
terrestrial ecosystems of Tierra del Fuego (southern Argentina). An
overview of recent progress. Journal of Photochemistry and
Photobiology 62, 67e77.
Baumbusch, L.O., Eiblmeier, M., Schnitzler, J.-P., Heller, W.,
Sandermann Jr., H., Polle, A., 1998. Interactive effects of ozone
and low UV-B radiation on antioxidants in spruce (Picea abies)
and pine (Pinus sylvestris) needles. Physiologia Plantarum 104,
248e254.
Bielawski, W., Joy, K.W., 1986. Reduced and oxidized glutathione and
glutathione-reductase activity in tissues of Pisum sativum. Planta
169, 267e272.
Bilger, W., Johnsen, T., Schreiber, U., 2001. UV-excited chlorophyll
fluorescence as a tool for the assessment of UV-protection by the
epidermis of plants. Journal of Experimental Botany 52, 2007e2014.
Björn, L.O., 2002. Effects of ultraviolet-B radiation on terrestrial
organisms and ecosystems with special reference to the arctic. In:
Hessen, D.O. (Ed.), UV Radiation and Arctic Ecosystems.
Springer-Verlag, Berlin Heidelberg, pp. 93e121.
Björn, L.O., Callaghan, T.V., Gehrke, C., Johanson, U.,
Sonesson, M., Gwynn-Jones, D., 1998. The problem of ozone
depletion in northern Europe. Ambio 27, 275e279.
ARTICLE IN PRESS
DTD 5
M. Turunen, K. Latola / Environmental Pollution
Blumthaler, M., Ambach, W., Ellinger, R., 1997. Increase in solar UV
radiation with altitude. Journal of Photochemistry and Photobiology 39, 130e134.
Bornman, J.F., 1999. Localisation and functional significance of
flavonoids and related compounds. In: Rozema, J. (Ed.), Stratospheric Ozone Depletion. The Effects of Enhanced UV-B
Radiation on Terrestrial Ecosystems. Backhuys Publishers, Leiden,
pp. 59e69.
Bornman, J.F., Vogelmann, T.C., 1988. Penetration of blue and UV
radiation measured by fibre optics in spruce and fir needles.
Physiologia Plantarum 72, 699e705.
Boyce, R.L., Vostral, C.B., Friedland, A.J., 2002. Winter water
relations of New England conifers and factors influencing their upper
elevational limits. II. Modeling. Tree Physiology 22, 801e806.
Caldwell, M.M., 1968. Solar ultraviolet radiation as an ecological
factor for alpine plants. Ecological Monographs 38, 243e268.
Campbell, B.D., Hofmann, R.W., Hunt, C.L., 1999. UV-B effects on
New Zealand pasture ecosystems. In: Rozema, J. (Ed.), Stratospheric Ozone Depletion. The Effects of Enhanced UV-B
Radiation on Terrestrial Ecosystems. Backhuys Publishers, Leiden,
pp. 227e249.
Cen, Y.B., Bornman, J.F., 1990. The response of bean plants to UV-B
radiation under different irradiances of background visible light.
Journal of Experimental Botany 41, 1489e1495.
Chabot, J.F., Chabot, B.F., 1975. Developmental and seasonal
patterns of mesophyll ultrastructure in Abies balsamea. Canadian
Journal of Botany 53, 295e304.
Chalker-Scott, L., 1999. Environmental significance of anthocyanins in
plant stress responses. Photochemistry and Photobiology 70, 1e9.
Clark, J.B., Lister, G.R., 1975. Photosynthetic action spectra of trees.
II. The relationship of cuticle structure to the visible and ultraviolet
spectral properties of needles from four coniferous species. Plant
Physiology 55, 407e413.
Cockell, C.S., Knowland, J., 1999. Ultraviolet radiation screening
compounds. Biological Reviews 74, 311e345.
Dai, Q., Yan, B., Huang, S., Liu, X., Peng, S., Lourdes, M.,
Miranda, L., Chavez, A.Q., Vergara, B.S., Olszyk, D.M., 1997.
Response of oxidative stress defence systems in rice (Oryza sativa)
leaves with supplemental UV-B radiation. Physiologia Plantarum
101, 301e308.
Day, T.A., 2001. Ultraviolet radiation and plant ecosystems. In:
Cockell, C.S., Blaustein, A.R. (Eds.), Ecosystems, Evolution, and
Ultraviolet Radiation. Springer-Verlag, New York, pp. 81e117.
Day, T.A., Neale, P.J., 2002. Effects of UV-B radiation on terrestrial
and aquatic primary producers. Annual Review of Ecology and
Systematics 33, 371e396.
Day, T.A., Vogelmann, T.C., DeLucia, E.H., 1992. Are some life
forms more effective than others in screening out ultraviolet-B
radiation? Oecologia 92, 513e519.
Day, T.A., Howells, B.W., Rice, W.J., 1994. Ultraviolet absorption
and epidermal-transmittance spectra in foliage. Physiologia Plantarum 92, 207e218.
DeLucia, E.H., Berlyn, G.P., 1983. The effect of elevation on leaf
cuticle thickness and cuticular transpiration in balsam fir.
Canadian Journal of Botany 62, 2423e2431.
DeLucia, E.H., Day, T.A., Vogelmann, T.C., 1991. Ultraviolet-B
radiation and the Rocky mountain environment: measurement of
incident light and penetration into foliage. Current Topics in Plant
Biochemistry and Physiology 10, 32e48.
DeLucia, E.H., Day, T.A., Vogelmann, T.C., 1992. Ultraviolet-B and
visible light penetration into needles of two species of subalpine
conifers during foliar development. Plant, Cell and Environment
15, 921e929.
Dormann, C.F., Woodin, S.J., 2002. Climate change in the Arctic:
using plant functional types in a meta-analysis of field experiments.
Functional Ecology 16, 4e17.
--
(2005)
---e---
11
Dunning, C.A., Chalker-Scott, L., Scott, J.D., 1994. Exposure to
ultraviolet-B radiation increases cold hardiness in Rhododendron.
Physiologia Plantarum 92, 516e520.
Dvorák, J., Stokrová, J., 1993. Structure of the needles in the early
phases of development in Pinus ponderosa P. et C. Lawson with
special reference to plastids. Annals of Botany 72, 423e432.
Esterbauer, H., Grill, D., 1978. Seasonal variation of glutathione and
glutathione reductase in needles of Picea abies. Plant Physiology
61, 119e121.
Fernbach, E., Mohr, H., 1992. Photoreactivation of the UV light
effects on growth of Scots pine (Pinus sylvestris L.) seedlings. Trees
6, 232e235.
Flint, S.D., Jordan, P.W., Caldwell, M.M., 1985. Plant protective
response to enhanced UV-B radiation under field conditions: leaf
optical properties and photosynthesis. Photochemistry and Photobiology 41, 95e99.
Foyer, C.H., Lelandais, M., Kunert, K.J., 1994. Photo-oxidative stress
in plants. Physiologia Plantarum 92, 696e717.
Gervais, B.R., MacDonald, G.M., Snyder, J.A., Kremenetski, C.V.,
2002. Pinus sylvestris treeline development on the Kola Peninsula
of Russia: pollen and stomate evidence. Journal of Ecology 90,
627e638.
Grace, J., 1990. Cuticular water loss unlikely to explain tree-line in
Scotland. Oecologia 84, 64e68.
Grill, D., Pfeifhofer, H., Tschulik, A., Hellig, K., Holzer, K., 1988.
Thiol content of spruce needles at forest limits. Oecologia 76,
294e297.
Gröbner, J., Albold, A., Blumthaler, M., Cabot, T., De la
Casiniere, A., Lenoble, J., Martin, T., Masserot, D., Muller, M.,
Philipona, R., Pichler, T., Pougatch, E., Rengarajan, G.,
Schmucki, D., Seckmeyer, G., Sergent, C., Toure, M.L.,
Weihs, P., 2000. Variability of spectral solar ultraviolet irradiance
in an alpine environment. Journal of Geophysical Research 105,
26991e27003.
Gunthardt, M.S., Wanner, H., 1982. Die Menge des cuticulären
Wachses auf Nadeln von Pinus cembra L. und Picea abies (L.)
Karsten in Abhängigkeit von nadelalter und Stanort. Flora (Jena)
172, 125e137.
Gwynn-Jones, D., Lee, J., Johanson, U., Phoenix, G., Callaghan, T.,
Sonesson, M., 1999. The responses of plant functional types
to enhanced UV-B radiation. In: Rozema, J. (Ed.),
Stratospheric Ozone Depletion. The Effects of Enhanced UV-B
Radiation on Terrestrial Ecosystems. Backhuys Publishers, Leiden,
pp. 173e185.
Hadley, J.L., Smith, W.K., 1990. Influence of leaf surface wax and leaf
area to water content ratio on cuticular transpiration in western
conifers, U.S.A. Canadian Journal of Forest Research 20,
1306e1311.
Herrick, G.T., Friedland, A.D., 1991. Winter desiccation and injury of
subalpinc red spruce. Tree Physiology 8, 23e36.
Hideg, É., Vass, I., 1996. UV-B induced free radical production in
plant leaves and isolated thylakoid membranes. Plant Science 115,
251e260.
Hideg, É., Mano, J., Ohno, C., Asada, K., 1997. Increased levels of
monodehydroascorbate radical in UV-B-irradiated broad bean
leaves. Plant Cell Physiology 38, 684e690.
Hoch, W.A., Zeldin, E.L., McCown, B.H., 2001. Physiological
significance of antocyanins during autumnal leaf senescence. Tree
Physiology 21, 1e8.
Holmes, M.G., Keiller, D.R., 2002. Effects of pubescence and waxes
on the reflectance of leaves in the ultraviolet and photosynthetic
wavebands: a comparison of a range of species. Plant, Cell and
Environment 25, 85e93.
Hoque, E., Remus, G., 1999. Natural UV-screening mechanisms of
Norway spruce (Picea abies L. Karst) needles. Photochemistry and
Photobiology 69, 177e192.
ARTICLE IN PRESS
DTD 5
12
M. Turunen, K. Latola / Environmental Pollution
Huiskes, A., Lud, D., Moerdijk-Poortvliet, T., Rozema, J., 1999.
Impact of UV-B radiation on antarctic terrestrial vegetation. In:
Rozema, J. (Ed.), Stratospheric Ozone Depletion. The Effects of
Enhanced UV-B Radiation on Terrestrial Ecosystems. Backhuys
Publishers, Leiden, pp. 313e337.
Jansen, M.A.K., Babu, T.S., Heller, D., Gaba, V., Mattoo, A.K.,
Edelman, M., 1996. Ultraviolet-B effects on Spirodela oligorrhiza:
induction of different protection mechanisms. Plant Science 115,
217e223.
Jansen, M.A.K., Gaba, V., Greenberg, B.M., 1998. Higher plants and
UV-B radiation: balancing damage, repair and acclimation. Trends
in Plant Science 3, 131e135.
Jokela, K., Leszcynski, K., Visuri, R., 1993. Effects of arctic ozone
depletion and snow on UV exposure in Finland. Photochemistry
and Photobiology 58, 559e566.
Jones, C.G., Hartley, S.E., 1998. Global change and plant phenolic
concentrations: species level predictions using protein competition
model. In: De Kok, L.J., Stulen, I. (Eds.), Responses of Plant
Metabolism to Air Pollution and Global Change. Backhuys
Publishers, Leiden, pp. 23e50.
Jordan, B.R., 2002. Molecular response of plant cells to UV-B stress.
Functional Plant Biology 29, 909e916.
Jordan, B.R., He, J., Chow, W.S., Anderson, J.M., 1992. Changes in
mRNA levels and polypeptide subunits of ribulose 1,5-bisphosphate carboxylase in response to supplementary ultraviolet-B
radiation. Plant, Cell and Environment 15, 91e98.
Kalbin, G., Ohlsson, A.B., Berglund, T., Rydström, J., Strid, Å., 1997.
Ultraviolet-B radiation-induced changes in nicotinamide and
glutathione metabolism and gene expression in plants. European
Journal of Biochemistry 249, 465e472.
Karlsson, P.S., Weih, M., 2001. Soil temperatures near distribution
limit of the Mountain birch (Betula pubescens ssp. Czerepanovii):
Implications for seedling nitohgen economy and survival. Arctic,
Antarctic and Alpine Research 33, 88e92.
Kaundun, S.S., Lebreton, P., Fady, B., 1998. Geographical variability
of Pinus halepensis Mill. as revealed by foliar flavonoids. Biochemical Systematics and Ecology 26, 83e96.
Kinnunen, H., Huttunen, S., Laakso, K., 2001. UV-absorbing
compounds and waxes of Scots pine needles during a third growing
season of supplemental UV-B. Environmental Pollution 112,
215e220.
Körner, Ch., 1998. A re-assessment of high-elevation treeline positions
and their explanation. Oecologia 115, 445e459.
Körner, Ch., 1999. Alpine Plant Life. Functional Plant Ecology of
High Mountain Ecosystems. Springer, Berlin, Heidelberg.
Kossuth, S.V., Biggs, R.H., 1980. Ultraviolet-B radiation effects on
early seedling growth of Pinaceae species. Canadian Journal of
Forest Research 11, 243e248.
Laakso, K., Huttunen, S., 1998. Effects of the UV-B radiation (UV-B)
on conifers: a review. Environmental Pollution 99, 319e328.
Laakso, K., Kinnunen, H., Huttunen, S., 2001. The glutathione status
of mature Scots pines during the third season of UV-B radiation
exposure. Environmental Pollution 111, 349e354.
Laakso, K., Sullivan, J.H., Huttunen, S., 2000. The effects of UV-B
radiation on epidermal anatomy in loblolly pine (Pinus taeda L.)
and Scots pine (Pinus sylvestris L.). Plant, Cell and Environment
23, 461e472.
Laracine-Pittet, C., Lebreton, P., 1988. Flavonoid variability within
Pinus sylvestris. Phytochemistry 27, 2663e2666.
Larson, R.A., Garrison, W.J., Carlson, R.W., 1990. Differential
response of alpine and non-alpine Aquilegia species to
increased ultraviolet-B radiation. Plant, Cell and Environment
13, 983e987.
Latola, K., Kinnunen, H., Huttunen, S., 2001. Needle ontogeny of
mature Scots pines under enhanced UV-B radiation. Trees 15,
346e352.
--
(2005)
---e---
Lavola, A., 1998. Accumulation of flavonoids and related compounds
in birch induced by UV-B irradiance. Tree Physiology 18, 53e58.
Lavola, A., Aphalo, P.J., Lahti, M., Julkunen-Tiitto, R., 2003.
Nutrient availability and the effect of increasing UV-B radiation
on secondary plant compounds in Scots pine. Environmental and
Experimental Botany 49, 49e60.
Lipscomb, M.V., Nilsen, E.T., 1990. Environmental and physiological
factors influencing the natural distribution of evergreen and
deciduous Ericaceous shrubs on northeast and southwest slopes
of the southern Appalachian mountains. I Irradiance Tolerance.
American Journal of Botany 77, 108e115.
Mackerness, S.A.-H., Butt, P.J., Jordan, B.R., Thomas, B., 1996.
Amelioration of ultraviolet-B-induced down-regulation on
mRNA levels for chloroplast proteins, by high irradiance, is
mediated by photosynthesis. Journal of Plant Physiology 148,
100e106.
Malanga, G., Puntarulo, S., 1995. Oxidative stress and antioxidant
content in Chlorella vulgaris after exposure to ultraviolet-B
radiation. Physiologia Plantarum 94, 672e679.
Manetas, Y., 1999. Is enhanced UV-B radiation really damaging for
plants. Some case studies with European Mediterranean species. In:
Rozema, J. (Ed.), Stratospheric Ozone Depletion. The Effects of
Enhanced UV-B Radiation on Terrestrial Ecosystems. Backhuys
Publishers, Leiden, pp. 251e263.
Meijkamp, B., Aerts, R., van de Staaij, J., Tosserams, M.,
Ernst, W.H.O., Rozema, J., 1999. Effects of UV-B on secondary
metabolites in plants. In: Rozema, J. (Ed.), Stratospheric Ozone
Depletion. The Effects of Enhanced UV-B Radiation on Terrestrial
Ecosystems. Backhuys Publishers, Leiden, pp. 71e99.
Mendez, M., Gwynn-Jones, D., Manetas, Y., 1999. Enhanced UV-B
radiation under field conditions increases antocyanin and reduces
risk of photoinhibition but does not affect growth in the carnivorous
plant Pinguicula vulgaris. New Phytologist 144, 275e282.
Mirecki, R.M., Teramura, A.H., 1984. Effects of ultraviolet-B
irradiance on soybean. Plant Physiology 74, 475e480.
Musil, C., Wand, S., 1999. Impact of UV-B radiation on South African
Mediterranean ecosystems. In: Rozema, J. (Ed.), Stratospheric
Ozone Depletion. The Effects of Enhanced UV-B Radiation on
Terrestrial Ecosystems. Backhuys Publishers, Leiden, pp. 265e291.
Neitzke, M., 2002. The crude methanolic extraction of UV absorbing
pigments in leaves of three forest floor species along an elevation
gradient. Archives of Nature Conservation and Landscape Research 41, 97e110.
Neitzke, M., Therburg, A., 2000. Veränderung der Konzentration von
UV-B -Strahlung absorbierenden Substanzen in den Blättern der
Buche (Fagus sylvatica L.) entlang eines Höhengradienten. Flora
195, 236e244.
Noctor, G., Arisi, A.-C.M., Jouanin, L., Valadier, M.-H., Roux, Y.,
Foyer, C.H., 1997. Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in poplar
overexpressing g-glutamylcysteine synthetase. Planta 202, 357e369.
Ottander, C., Öquist, G., 1991. Recovery of photosynthesis in winterstressed Scots pine. Plant, Cell and Environment 14, 345e349.
Polle, A., 1997. Defense against photoxidative damage in plants. In:
Scandalios, J.G. (Ed.), Oxidative Stress and Molecular Biology of
Antioxidant Defences. Cold Spring Harbor Laboratory Press, New
York, pp. 623e666.
Polle, A., Rennenberg, H., 1992. Field studies on Norway spruce trees
at high altitudes: II. Defence systems against oxidative stress in
needles. New Phytologist 121, 635e642.
Polle, A., Rennenberg, H., 1994. Photooxidative stress in trees. In:
Foyer, C.H., Mullineaux, P.M. (Eds.), Causes of Photooxidative
Stress and Amelioration of Defense Systems in Plant. CRC Press
Inc, Boca Raton, pp. 199e218.
Poulson, M.E., Donahue, R.A., Konvalinka, J., Boeger, T., 2002.
Enhanced tolerance of photosynthesis to high-light ad drought
ARTICLE IN PRESS
DTD 5
M. Turunen, K. Latola / Environmental Pollution
stress in Pseudotsuga menziesii seedlings grown in ultraviolet-B
radiation. Tree Physiology 22, 829e838.
Predieri, S., Norman, H.A., Krizek, D.T., Pillai, P., Mirecki, R.M.,
Zimmerman, R.H., 1995. Influence of UV-B radiation on
membrane lipid composition and ethylene evolution in ‘Doyenne
d’Hiver’ pear shoots grown in vitro under different photosynthetic
photon fluxes. Environmental and Experimental Botany 35,
151e160.
Rao, M.V., Paliyath, G., Ormrod, D.P., 1996. Ultraviolet-B- and
ozone-induced biochemical changes in antioxidant enzymes of
Arabidopsis thaliana. Plant Physiology 110, 125e136.
Rau, W., Hofmann, H., 1996. Sensitivity to UV-B of plants growing in
different altitudes in the Alps. Journal of Plant Physiology 148,
21e25.
Robberecht, R., Caldwell, M.M., Billings, W.D., 1980. Leaf ultraviolet
optical properties along a gradient in the arctic-alpine life zone.
Ecology 61, 612e619.
Robinson, S.A., Wasley, J., Tobin, A.K., 2003. Living on the edge e
plants and global change in continental and maritime Antarctica.
Global Change Biology 9, 1681e1717.
Rozema, J., Oudejans, A., Houter, N., Schoonheim, H., Walraven, I.,
van’t Klooster, C., van Staaij, J., Tosserams, M., de Bakker, N.,
van Beem, A., Stroetenga, M., Broekman, R., van Heerwaarden,
L., Nelissen, H., Aerts, R., 1999. Responses of plants from dune
grassland ecosystem in the Netherlands to solar UV-B: UV-B
filtration and supplementation experiments. In: Rozema, J. (Ed.),
Stratospheric Ozone Depletion. The Effects of Enhanced UV-B
Radiation on Terrestrial Ecosystems. Backhuys Publishers, Leiden,
pp. 203e225.
Sase, H., Takamatsu, T., Yoshida, T., 1998. Variation in amount and
elemental composition of eppicuticular wax in Japanese cedar
(Cryptomeria japonica) leaves associated with natural environmental factors. Canadian Journal of Forest Research 28, 87e97.
Schnitzler, J.-P., Jungblut, T.P., Heller, W., Kofferlein, M.,
Hutzler, P., Heinzmann, U., Schmelzer, E., Ernst, D.,
Langebartels, C., Sandermann Jr., H., 1996. Tissue localization
of u.v.-B-screening pigments and of chalcone synthase mRNA in
needles of Scots pine seedlings. New Phytologist 32, 247e258.
Schupp, R., Rennenberg, H., 1988. Diurnal changes in the glutathione
content of spruce needles (Picea abies L.). Plant Science 57,
113e117.
Searles, P.S., Flint, S.D., Caldwell, M.M., 2001. A meta-analysis of
plant field studies simulating stratospheric ozone depletion.
Oecologia 127, 1e10.
Shi, S.-B., Zhu, W.-Y., Li, H.-M., Zhou, D.-W., Han, F., Zhao, X.-Q.,
Tang, Y.-H., 2004. Photosynthesis of Saussurea superba and
Gentiana straminea is not reduced after long-term enhancement
of UV-B radiation. Environmental and Experimental Botany 51,
75e83.
Stevens, G.C., Fox, J.F., 1991. The causes of treeline. Annual Review
of Ecological Systematics 22, 177e191.
Strand, M., Öquist, G., 1985. Inhibition of photosynthesis by freezing
temperatures and high light levels in cold-acclimated seedlings of
Scots pine (Pinus sylvestris) e I. Effects on the light-limited and
light-saturated rates of CO2 assimilation. Physiologia Plantarum
64, 425e430.
Streb, P., Shang, W., Feierabend, J., Blighny, R., 1998. Divergent
strategies of photoprotection in high-mountain plants. Planta 207,
313e324.
Sullivan, J.H., Teramura, A.H., 1988. Effects of ultraviolet-B
irradiation on seedling growth in the Pinaceae. American Journal
of Botany 75 (2), 225e230.
Sullivan, J.H., Teramura, A.H., Ziska, L.H., 1992. Variation in UV-B
sensitivity in plants from a 3000 m elevational gradient in Hawaii.
American Journal of Botany 79, 737e743.
Sullivan, J.H., Howells, B.W., Ruhland, C.T., Day, T., 1996. Changes
in leaf expansion and epidermal screening effectiveness in
--
(2005)
---e---
13
Liquidambar styraciflua and Pinus taeda in response to UV-B
radiation. Physiologia Plantarum 98, 349e357.
Takeuchi, Y., Kubo, H., Kasahara, H., Sakaki, T., 1996. Adaptive
alterations in the activities of scavengers of active oxygen in
cucumber cotyledons irradiated with UV-B. Journal of Plant
Physiology 147, 589e592.
Taulavuori, E., Bäckman, M., Taulavuori, K., Gwynn-Jones, D.,
Johanson, U., Laine, K., Callaghan, T., Sonesson, M., Björn, L.O.,
1998. Long-term exposure to enhanced ultraviolet-B radiation in
the sub-arctic does not cause oxidative stress in Vaccinium
myrtillus. New Phytologist 140, 691e697.
Tausz, M., Wonisch, A., Grill, D., Morales, D., Jimenez, M.S., 2003.
Measuring antioxidants in tree species in the natural environment:
from sampling to data evaluation. Journal of Experimental Botany
54, 1505e1510.
Tegischer, K., Tausz, M., Wieser, G., Grill, D., 2002. Tree- and needleage-dependent variations in antioxidants and photoprotective
pigments in Norway spruce needles at the alpine timberline. Tree
Physiology 22, 591e596.
Tranquillini, W., 1979. Physiological Ecology of the Alpine Timberline. Tree Existence at High Altitudes with Special Reference to the
European Alps. Ecological Studies 31. Springer-Verlag, Berlin
Heidelberg, New York.
Tuhkanen, S., 1999. The northern timberline in relation to climate. In:
Kankaanpää, S., Tasanen, T., Sutinen, M.-L. (Eds.), Sustainable
Development in Northern Timberline Forests. Proceedings of the
Timberline Workshop, the Finnish Forest Research Institute,
Research Papers 734. Whitehorse, Canada, pp. 29e61.
Turunen, M., Huttunen, S., 1990. Review of the response of epicuticular wax to air pollution. Journal of Environmental Quality 19,
35e45.
Turunen, M., Huttunen, S., 1991. Effect of simulated acid rain on the
epicuticular wax of Scots pine needles under northerly conditions.
Canadian Journal of Botany 69, 412e419.
Turunen, M., Huttunen, S., 1996. Scots pine needle surfaces on the
radial transects across the north boreal area of Finnish Lapland
and the Kola Peninsula of Russia. Environmental Pollution 93,
175e194.
Turunen, M., Vogelmann, T.C., Smith, W.K., 1999a. UV screening in
lodgepole pine (Pinus contorta ssp. latifolia) cotyledons and
needles. International Journal of Plant Science 160, 315e320.
Turunen, M., Heller, W., Stich, S., Sandermann, H., Sutinen, M.-L.,
1999b. Effects of UV exclusion on phenolic compounds of young
Scots pine seedlings in the subarctic. Environmental Pollution 106,
225e234.
Van de Staaij, J.W.M., Huijsmans, R., Ernst, W.H.O., Rozema, J.,
1995. The effect of elevated UV-B (280e320 nm) radiation levels on
Silene vulgaris: a comparison between a highland and lowland
population. Environmental Pollution 90, 357e362.
Van de Staaij, J.W.M., Bolink, E., Rozema, J., Ernst, W.H.O., 1997.
The impact of elevated UV-B (280e320 nm) radiation levels on the
reproduction biology of a highland and a lowland population of
Silene vulgaris. Plant Ecology 128, 172e179.
Veijola, P., 1998. The Northern Timberline and Timberline Forests in
Fennoscandia. The Finnish Forest Research Institute. Research
Papers 672. Gummerus Kirjapaino Oy. Saarijärvi.
Vogelmann, T.C., 1993. Plant tissue optics. Annual Review of Plant
Physiology and Plant Molecular Biology 44, 231e251.
Vostral, C.B., Boyc, R.L., Friedland, A.J., 2002. Winter water relations
of New England conifers and factors influencing their upper
elevational limits. I. Measurements. Tree Physiology 22, 793e800.
Wand, S.J.E., 1995. Concentration of ultraviolet-B radiation absorbing compounds in leaves of a range of fynbos species. Vegetatio
116, 51e60.
Wardle, P., 1998. Comparison of alpine timberlines in New Zealand
and the southern Andes. Royal Society of New Zealand Miscellaneous Publications 48, 69e90.
ARTICLE IN PRESS
DTD 5
14
M. Turunen, K. Latola / Environmental Pollution
Webb, A.R., 1997. Monitoring changes in UV-B radiation. In:
Lumsden, P. (Ed.), Plants and UV-B. Responses to Environmental
Change. Society for Experimental Biology, Seminar Series 64.
Cambridge University Press, Cambridge, pp. 13e30.
Wildi, B., Lutz, C., 1996. Antioxidant composition of selected high
alpine plant species from different altitudes. Plant Cell and
Environment 19, 138e146.
--
(2005)
---e---
Yang, X., Heisler, G.M., Montgomery, M.E., Sullivan, J.H.,
Whereat, E.B., Miller, D.R., 1995. Radiative properties of
hardwood leaves to ultraviolet irradiation. International Journal
of Biometeorology 38, 60e66.
Ziska, L.H., Teramura, A.H., Sullivan, J.H., 1992. Physiological
sensitivity of plants along an elevational gradient to UV-B
radiation. American Journal of Botany 79, 863e871.