Plant Ecology (2006) 182:137 –152
Springer 2005

DOI 10.1007/s11258-005-9023-1

Outdoor studies on the effects of solar UV-B on bryophytes: overview and

methodology

Peter Boelen1,*, M. Karin de Boer2, Nancy V. J. de Bakker1 and Jelte Rozema1

1
Institute of Ecological Science, Department of Systems Ecology, Faculty of Earth and Life Sciences, Vrije
Universiteit, De Boelelaan 1087, 1081 HV, Amsterdam, The Netherlands; 2Department of Marine Biology,
University of Groningen, 14, 9750 AA, Haren, The Netherlands; *Author for correspondence (e-mail:
peter.boelen@ecology.falw.vu.nl; phone: +31 20 5987048; fax: +31 20 5987123)

Received 1 September 2004; accepted in revised form 15 December 2004

Key words: Antarctic, Arctic, Bryophytes, Chorisodontium aciplyllum, Cyclobutane Pyrimidine dimers,
DNA damage, mosses, Ozone depletion, Polytrichum strictum, Sanionia uncinata, Terrestrial polar eco-
systems, Ultraviolet-B radiation, UV-B exposure systems, UVBR, Warnstorfia sarmentosa

Abstract

In this review all recent field studies on the effects of UV-B radiation on bryophytes are discussed. In
most of the studies fluorescent UV-B tubes are used to expose the vegetation to enhanced levels of UV-
B radiation to simulate stratospheric ozone depletion. Other studies use screens to filter the UV-B part
of the solar spectrum, thereby comparing ambient levels of UV-B with reduced UV-B levels, or analyse
effects of natural variations in UV-B arising from stratospheric ozone depletion. Nearly all studies show
that mosses are well adapted to ambient levels of UV-B radiation since UV-B hardly affects growth
parameters. In contrast with outdoor studies on higher plants, soluble UV-B absorbing compounds in
bryophytes are typically not induced by enhanced levels of UV-B radiation. A few studies have
demonstrated that UV-B radiation can influence plant morphology, photosynthetic capacity, photo-
synthetic pigments or levels of DNA damage. However, there is only a limited number of outdoor
studies presented in the literature. More additional, especially long-term, experiments are needed to
provide better data for statistical meta-analyses. A mini UV-B supplementation system is described,
especially designed to study effects of UV-B radiation at remote field locations under harsh conditions,
and which is therefore suited to perform long-term studies in the Arctic or Antarctic. The first results
are presented from a long-term UV-B supplementation experiment at Signy Island in the Maritime
Antarctic.

Introduction 280 –315 nm) at ground level. Since the 1970s

Stratospheric ozone depletion occurs mainly over
polar regions during spring. A relatively small
decrease in stratospheric ozone concentration,
owing to anthropogenic emissions of chloroflu-
orocarbons (CFCs), will strongly affect the inten-
sity of ultraviolet-B radiation (UV-B radiation:
springtime stratospheric ozone over the Antarctic
has decreased up to 50%, leading to increases in
biologically effective UV-B radiation of more than
130% (Madronich et al. 1998; WMO 2003).
Many studies on the effects of enhanced UV-B
radiation have focused on higher plants. However,
Antarctic terrestrial ecosystems are dominated by
138
cryptogams, with mosses predominating in the
moister, more sheltered habitats and lichens in the
more arid and windswept situations (Fenton
1982). There are approximately 75 moss species
but relatively few achieve dominance (Fowbert
1996) and higher plants are poorly represented in
the Antarctic.
Until several years ago relatively little was known
about the effects of UV-B radiation on mosses. This
is remarkable because beforehand it was assumed
that the majority of bryophytes were particularly
susceptible to UV-B radiation and that they were
more sensitive to UV-B radiation than higher
plants (Gehrke 1999). Firstly, most bryophytes
have (undifferentiated) leaves of only one cell layer
thickness and no protective cuticle and epidermis to
attenuate UV-B. Secondly, since leaf water content
in bryophytes depends on air humidity, high levels
of solar radiation can lead to physiological
inactivity, which may hinder processes such as
DNA photorepair. Finally, since most bryo-
phytes are rootless, mosses are not able to
compensate for aboveground stresses, such as
UV-B radiation, through the belowground stor-
age of assimilates.
Studies on the effects of UV-B radiation on
mosses are not only important to predict the
effects of future ozone depletion scenarios but are
also essential for studies that attempt to recon-
struct historical ozone levels. Rozema et al.
(2001b) suggested that polyphenolic compounds
in pollen and spores that have been incorporated
into moss banks may be applied as a new proxy
for the reconstruction of historic variation in
solar UV-B levels. In the Antarctic, e.g. at Signy
Island, two species of moss, Chorisodontium aci-
phyllum and Polytrichum strictum, form charac-
teristic peat banks which may be over 2 m deep,
may cover more than 2500 m2 in area and are as
much as 5000 years old (Fenton 1980). The moss
peat banks consist mainly of the relatively
uncompacted remains of the two moss species.
The mosses become incorporated into the per-
mafrost at a depth of 20 to 30 cm. Since most
parts of Antarctic moss peat banks are perma-
nently frozen, these banks may represent a unique
archive of historical UV-B levels (Rozema et al.
2001c; 2002). Besides the analysis of UV-B in-
duced polyphenolic compounds pollen and spores
that are incorporated into these moss banks, the
preservation of frozen moss material may allow
DNA extraction and quantification of cyclobu-
tane pyrimidine dimers (CPDs) caused by expo-
sure to solar UV-B radiation (Caldwell et al.
1998).
In this paper we give an overview of recent field
studies on the effects of altered levels of UV-B
radiation on bryophytes. The experimental meth-
ods that have been used to manipulate levels of
UV-B radiation in the field are discussed. Fur-
thermore, a mini UV-B supplementation system,
especially designed to study the effects of enhanced
UV-B radiation on terrestrial vegetation at remote
field locations, is described. This UV-B supple-
mentation system has already been used for two
consecutive years at Signy Island in the Maritime
Antarctic where natural vegetation (four moss
species and the higher plant Deschampsia
antarctica) is exposed to enhanced UV-B radiation
in a long-term experiment.
Outdoor studies on the effects of solar UV-B on
bryophytes: an overview
UV-B radiation can have many direct and indirect
effects on organisms. UV-B radiation induces
damage to essential molecules like proteins, pig-
ments and DNA. This damage can influence
important cellular processes such as nutrient up-
take, DNA transcription and replication or pho-
tosynthesis, which eventually can lead to decreased
growth rate or impaired reproduction (see Rozema
et al. 1997a; Caldwell et al. 1998; Searles et al.
2001; Robinson et al. 2003). There are several
strategies to minimise the deleterious effects of UV-
B radiation. In higher plants UV-B damage to
essential molecules is avoided by producing UV-B
absorbing compounds (see Meijkamp et al. 1999;
Searles et al. 2001) or by increasing leaf thickness
(Bornman and Vogelmann 1991). Another strategy
is to utilise repair mechanisms to ameliorate UV-B
induced damage.
Studies on the ecophysiological responses of
higher plants to UV-B are mainly based on
greenhouse or climate room experiments. In a
meta-analysis of field based studies on higher
plants, Searles et al. (2001) concluded that the
accumulation of UV-B absorbing compounds in
leaves was the most apparent effect of enhanced
UV-B radiation while most morphological and
photosynthetic parameters were not affected. In

contrast to higher plants, most studies on bryo-
phyte responses to UV-B are conducted under
field conditions. These outdoor studies investigat-
ing the impact (on growth, morphology, photo-
synthetic parameters, UV-B screening pigments
and DNA damage) of UV-B radiation on bryo-
phytes are summarised in Table 1. All field
experiments considered here were carried out in
polar or sub-polar regions. There is a substantial
variation in the duration of the studies, with some
performed for 10 h and others for up to 6 years.
Long-term studies are more difficult to maintain
but have the advantage that slow processes, such
as growth, can be monitored. The majority of the
studies have employed UV-B lamps to simulate a
decrease in stratospheric ozone concentration. In
other studies screens were used to reduce solar
UV-B below ambient levels. These studies can be
particularly valuable at Antarctic sites with se-
verely depleted stratospheric ozone concentra-
tions, but comparisons between UV-B
supplementation studies and exclusion experi-
ments should be done with care. Covering plants
with screens can have artefactual effects on tem-
perature and water availability.
Growth, morphology and reproduction
In higher plants many effects of UV-B radiation
involve morphogenetic changes. Plant morphoge-
netic parameters that may change are plant height,
leaf area, branching and plant phenology (Rozema
et al. 1997a).
Only a few field studies relating growth and
morphology to UV-B exposure and, to our
knowledge, no studies relating reproduction have
been reported for bryophytes. Long-term field
studies of Sphagnum sp. showed that UV-B radi-
ation can influence shoot biomass and length but
that biomass production per area is not affected
(Gehrke 1998; Searles et al. 2002; Robson et al.
2003). Lud et al. (2002) showed that, while shoot
biomass and length were unaffected, branching of
the Antarctic moss Sanionia uncinata was reduced
by reduction of ambient UV-B levels. In a green-
house experiment where the moss Hylocomium
splendens was grown under enhanced UV-B levels
the phenological development of the moss was
accelerated by up to 2 weeks (Johanson et al.
1995).
139
Photosynthetic activity
UV-B radiation can directly or indirectly affect
many photosynthetic processes in higher plants
such as performance of Photosystem II, the
integrity of the thylakoid membrane and enzy-
matic processes in the Calvin Cycle (Bornman
1989; Teramura and Sullivan 1994; Jansen et al.
1998). However, most of these studies have been
carried out under unrealistic irradiance conditions
with low levels of UV-A radiation and/or PAR
(Photosynthetic Active Radiation; 400 –700 nm).
Field studies, with plants exposed to more realistic
enhanced levels of UV-B radiation, reveal that in
most cases photosynthetic performance is not
affected (Allen et al. 1998; Searles et al. 2001;
Dormann and Woodin 2002).
Although Montiel et al. (1999) observed a
decreased photochemical yield in the moss
Sanionia uncinata, in most field studies on terres-
trial bryophytes (i.e. Sanionia uncinata, Bryum ar-
genteum, Sphagnum fuscum) photosynthetic
activity is not affected by reduced or enhanced UV-
B radiation (Gehrke 1998; Green et al. 2000; Hu-
iskes et al. 2001; Lud et al. 2002, 2003; Newsham
et al. 2002). Also in the majority of the bryophytes
(including three Sphagnum sp.) that have been
investigated, concentrations of chlorophylls are not
influenced by UV-B exposure (Gehrke 1999;
Searles et al. 1999, 2002; Niemi et al. 2002a, b,
Newsham et al. 2002; Lud et al. 2003; Newsham
2003). However in Sphagnum fuscum, chlorophyll a
concentrations decreased, while chlorophyll levels
in Sphagnum balticum increased after exposure to
supplemental UV-B radiation (Gehrke 1998; Niemi
et al. 2002a).
Oxidative damage
Although ultraviolet-A radiation (UV-A: 315 –
400 nm) is considered to be the major generator of
intracellular oxidative stress (Pourzand and Tyrrel
1999), several studies have shown that UV-B
radiation exposure can lead to increases in reactive
oxygen species (ROS) in plants. ROS can react
with lipids, pigments, proteins and nucleic acids,
leading to inactivation of enzymes, membrane
damage or oxidative DNA damage (see Day 2001).
Plants cells usually contain enzymatic and non-
enzymatic defences against oxygen toxicity. These
Table 1. Summary of outdoor studies on the effects of UV-B radiation on terrestrial bryophytes.
140
Species Location Duration and Growth morphology Photosynthetic Photosynthetic Membranes UV-B absorbing DNA References
(Latitude type of study and reproduction activity and photopro- compounds damage
/Longitude) tective pigments (UACs)

Andreaea regularis Antarctic 1 month in situ Increased carot- Increased UACs Newsham
Adelaide Island enoids under naturally (2003)
(6734¢ S, under naturally elevated UV-BR
6807¢ W) elevated
UV-BR
Cephaloziella varians Antarctic 1 month in situ No effect of Increased Increased UACs Newsham
Adelaide Island naturally ele- carotenoids under naturally et al. (2002)
(6734¢ S, vated UV-BR under naturally elevated UV-BR
6807¢ W) on Fv/Fm elevated
(maximum UV-BR
quantum yield
of PSII)
Chorisodontium aciphyl- Maritime Ant- 3 –5 weeks of No effect of en- No effect of This paper
lum arctic Signy enhanced hanced enhanced
Island (6042¢ S, UV-BR simu- UV-BR on UV-BR on
4535¢ W) lating 15 and UACs CPD accu-
30% ozone mulation
depletion
Dicranum elongatum Northern Swe- 2 years en- No effect of UV-BR No effect of No effect of Sonesson
den Abisko hanced UV-BR on growth UV-BR on UV-BR on et al. (2002)
(6821¢ N, simulating 20% chlorophyll flavonoids
1849¢ E) ozone reduction
Hylocomium splendens Northern Swe- 3 –6 years Growth reduced No effect on No effect on Gehrke (1999);
den Abisko enhanced UV- after 3 years but chlorophyll and UACs after Phoenix et al.
(6835¢ N, BR simulating enhanced after carotenoid con- 3 years (2001)
1882¢ E) 15% ozone 6 years, shoot mor- centrations after
depletion phology altered after 3 years of en-
3 years hanced
UV-BR
Polytrichum commune Northern Swe- 3 years Annual length incre- Concentration Less UACs after Gehrke (1999)
den Abisko enhanced ment reduced, no ef- of chlorophyll a 3 years of en-
(6835¢ N, UV-BR simu- fect on and carotenoids hanced
1882¢ E) lating 15% biomass, shoot mor- decreased, no UV-BR
ozone depletion phology altered effect on chlo-
rophyll b
concentration
Polytrichum strictum Maritime Ant- 3 –5 weeks of No effect of en- No effect of This paper
arctic Signy Is- enhanced UV- hanced enhanced
land (6042¢ S, BR simulating UV-BR on UV-BR on
4535¢ W) 15 and 30% UACs CPD accu-
ozone depletion mulation
Sanionia uncinata Maritime Ant- 3 –5 weeks of No effect of en- No effect of This paper
arctic Signy Is- enhanced UV- hanced enhanced
land (6042¢ S, BR simulating UV-BR on UV-BR on
4535¢ W) 15 and 30% UACs CPD accu-
ozone depletion mulation
Antarctic Léo- 3 –4 weeks No effect on Huiskes et al.
nie Island screening study PSII quantum (2001)
(6735¢ S, yield
6820¢ W)
Antarctic Léo- 2 years screen- No effect on biomass Lud et al. (2002)
nie Island ing study or length growth, less
(6735¢ S, branching under re-
6820¢ W) duced UV-BR
Antarctic Léo- 2 days of en- No effect on ac- No effect of DNA dam- Lud et al. (2002)
nie Island hanced UV-BR tual and maxi- UV-BR on age in-
(6735¢ S, (8.4 kJ mum quantum chlorophyll creased un-
6820¢ W) m)2 day)1, yield of PSII, no der en-
weighted with effect on photo- hanced UV-
Setlow, norma- synthetic gas BR
lised at 300 nm) exchange
Arctic Ny-Ales- 2 days of en- No effect on ac- No effect of DNA dam- Lud et al. (2002)
und, Svalbard hanced UV-BR tual and maxi- UV-BR on age in-
(7855¢ N, (8.4 kJ mum quantum chlorophyll creased un-
1156¢ E) m)2 day)1, yield of PSII der en-
weighted with hanced UV-
Setlow, norma- BR
lised at 300 nm)
Antarctic Léo- 3 short-term No effect on ac- No effect on Lud et al. (2003)
nie Island screening stud- tual and maxi- chlorophyll
(6735¢ S, ies mum quantum concentrations
6820¢ W) yield of PSII, no
effect on photo-
synthetic gas
exchange
Antarctic Léo- 10 h of en- No effect on No effect of en- DNA dam- Lud et al. (2003)
nie Island hanced UV-BR chlorophyll and hanced UV-BR age in-
(6735¢ S, (in total 8.7 kJ carotenoid con- on UACs creased un-
6820¢ W) m)2, weighted centrations der en-
with Setlow, hanced UV-
normalised at BR
300 nm)
Antarctic A- 7 days of en- PSII quantum Montiel et al.
delaide Island hanced UV-BR yield reduced (1999)
(6734¢ S, (30% of back- under enhanced
6807¢ W) ground solar UV-BR com-
levels, no UV-A pared to ambi-
control) and ent and reduced
screening study UV-BR
141
Table 1. Continued.
142
Species Location Duration and Growth morphology Photosynthetic Photosynthetic Membranes UV-B absorbing DNA References
(Latitude type of study and reproduction activity and photopro- compounds damage
/Longitude) tective pigments (UACs)

Antarctic 1 month in situ No effect of Increased carot- Increased UACs Newsham et al.
Adelaide Island naturally enoids under under naturally (2002)
(6734¢ S, elevated naturally ele- elevated UV-BR
6807¢ W) UV-BR on Fv/ vated UV-BR
Fm (maximum
quantum yield
of PSII)
Sphagnum angustifolium Central Finland 14 weeks of No effect of UV-BR No effect on Membrane No effect of en- Niemi et al.
Kuopio enhanced on capitulum chlorophyll and leakage of hanced (2002b)
(6213¢ N, UV-BR simu- or stem dry mass carotenoid con- Mg and Ca UV-BR on
2735¢ E) lating 30% centrations after after UACs
ozone depletion 14 weeks of en- 6 weeks
hanced UV-BR exposure to
enhanced
UV-BR, No
effect of
UV-BR on
membrane
permeabil-
ity after
12 weeks
exposure
Sphagnum balticum Central Finland 14 weeks of No effect of UV-BR Increase of Increase of No effect of en- Niemi et al.
Kuopio enhanced on capitulum chlorophyll a, membrane hanced (2002a)
(6213¢ N, UV-BR simu- or stem dry mass chlorophyll b conductivity UV-BR on
2735¢ E) lating 30% and carotenoids UACs
ozone depletion, after exposure
no UV-A con- to enhanced
trol UV-BR
Sphagnum fuscum Northern Swe- 2 years of en- Decrease in annual Maximum net Chlorophyll a No effect of en- Gehrke (1998)
den Abisko hanced UV-BR length increment, dry photosynthesis and carotenoids hanced UV-BR
(6835¢ N, simulating 15% mass per unit length (NPmax) in- decreased under on UACs
1882¢ E) ozone depletion increased, no effect on creased under enhanced UV-
production of biomass UV-BR when BR, no effect on
per area calculated per chlorophyll b
unit chloro-
phyll, no effect
on NPmax on a
dry-mass basis,
dark respiration
decreased
Sphagnum fuscum Northern Swe- 2 years No effect of UV-B R No effect of No effect of Sonesson et al.
den Abisko enhanced on growth UV-BR on UV-BR on (2002)
(6821¢ N, UV-BR chlorophyll flavonoids
1849¢ E)
Sphagnum magellanicum Central Finland 14 weeks of en- No effect on Membrane Niemi et al.
Kuopio hanced UV-BR chlorophyll and leakage of Mg (2002b)
(6213¢ N, simulating 30% carotenoid con- after 12 weeks
2735¢ E) ozone depletion centrations after exposure to en-
14 weeks of en- hanced UV-BR
hanced UV-BR
Southern 3 –6 years Height growth de- No effect on No effect on Searles et al.
Argentina Tier- screening study creased but capitu- chlorophyll and UACs (1999, 2002);
ra del Fuego (near ambient lum density increased carotenoids Robson et al.
(5451¢ S, and reduced under near-ambient (2003)
6836¢ W) UV-BR) conditions, no effect
on production of
biomass per area
Sphagnum papillosum Central Finland 14 weeks of No effect on Increase of No effect of en- Niemi et al.
Kuopio enhanced chlorophyll and membrane con- hanced (2002a)
(6213¢ N, UV-BR simu- carotenoid con- ductivity, leak- UV-BR on
2735¢ E) lating 30% centrations after age of Mg and UACs
ozone depletion, 14 weeks of en- Ca
no UV-A con- hanced UV-BR
trol
Central Finland 14 weeks of No effect on No effect of No effect of en- Niemi et al.
Kuopio enhanced chlorophyll and UV-BR on hanced (2002b)
(6213¢ N, UV-BR simu- carotenoid con- membrane per- UV-BR on
2735¢ E) lating 30% centrations after meability after UACs
ozone depletion 14 weeks of en- 12 weeks expo-
hanced UV-BR sure
Warnstorfia sarmentosa Maritime Ant- 3 –5 weeks of No effect of en- No effect of This paper
arctic Signy Is- enhanced hanced enhanced
land (6042¢ S, UV-BR simu- UV-BR on UV-BR on
4535¢ W) lating 15 and UACs CPD accu-
30% ozone mulation
depletion
143
144
so-called antioxidants can remove, neutralise or
scavenge ROS in cells, thereby protecting cellular
components from oxidative damage. Enzymatic
antioxidants are superoxide dismutase (SOD),
catalase (CAT), ascorbate peroxidase (AP) dehy-
droascorbate reductase and glutathione reductase.
Non-enzymatic defences are carotenoids, flavo-
noids, ascorbate and glutathione (Dai et al. 1997;
Jansen et al. 1998).
Very little is known about UV-induced
oxidative stress in bryophytes. Niemi et al.
(2002a, b) showed that enhanced UV-B levels
could lead to increased membrane permeability in
Sphagnum spp. Although the authors did not
mention this, an increase in membrane perme-
ability could be the result of oxidative stress (Dai
et al. 1997).
In a growth chamber experiment, Markham
et al. (1998) studied the effects of varying UV-B
levels on the liverwort Marchantia polymorpha.
They found a strong correlation between increasing
UV-B levels and the ratio of two individual flavo-
noids. Since the total UV-B screening effectiveness
of the flavonoids was not altered, they suggested
that an increase of one particular flavonoid
(a luteolin glycoside) improved the level of
antioxidant defence.
UV-B-absorbing compounds
Many plants can adapt to high UV-B fluxes by the
production of secondary metabolites which absorb
UV-B radiation. In a meta-analysis of 62 outdoor
irradiation studies (no studies of moss species
included), Searles et al. (2001) concluded that the
accumulation of UV-B absorbing compounds in
leaves was the most apparent effect of enhanced
UV-B radiation. UV-B radiation stimulates the
production of phenylalanine ammonium lysase
(PAL) and other key enzymes of the phenylpropa-
noid pathway (Rozema et al. 1997a; Meijkamp
et al. 1999). PAL catalyses the formation of phen-
ylalanine to trans-cinnamic acid, which leads to the
formation of complex phenolic compounds such as
flavonoids, tannins and lignin. Although flavo-
noids can be found in many (but not all) moss
species (Markham 1990), most studies show that
UV-B absorbing compounds in bryophytes were
not enhanced by supplemental levels of UV-B
radiation applied from fluorescent UV lamps
(Barsig et al. 1998; Gehrke 1998; Markham et al.
1998; Gehrke 1999; Niemi et al. 2002b; Searles
et al. 2002; Lud et al. 2003). In an outdoor UV-B
supplementation experiment (see below) at Signy
Island (Maritime Antarctic) soluble UV-B absorb-
ing compounds in four moss species (Sanionia
uncinata, Chorisodontium aciphyllum, Warnstorfia
sarmentosa and Polytrichum strictum) were not
induced by enhanced levels of UV-B radiation
(Figure 1). However, studies by Newsham et al.
(2002) and Newsham (2003) suggested that in
Antarctic bryophytes UV-B absorbing pigments
may be induced within 24 h under natural ele-
vated irradiances of UV-B arising from ozone
depletion. In addition, Markham et al. (1990)
found that flavonoid concentrations in herbar-
ium specimens of Bryum argenteum were corre-
lated with historical ozone levels for the period
1960 –1990.
UV-B induced DNA damage and repair
UV-B radiation can cause dimerization of DNA
bases, leading to the formation of photoproducts
like cyclobutane pyrimidine dimers (CPDs) and
pyrimidine (6 –4) pyrimidone photoproducts. Cells
need to repair this damage before they can proceed
with DNA transcription or replication. There are
two main pathways to repair dimerised pyrimi-
dines: excision (dark) repair and photodependent
repair (Sancar and Sancar 1988).
Lud et al. (2002, 2003) studied the effects of
ambient and enhanced levels of UV-B radiation on
the bipolar bryophyte Sanionia uncinata. They
concluded that ambient summer levels of UV-B
radiation did not induce significant levels of DNA
damage. However, DNA damage, measured as
CPDs, clearly increased as a result of artificially
enhanced UV-B radiation. DNA damaged during
the day was repaired during the (non dark) night.
In 2003 an outdoor UV-B supplementation
experiment (see below) was started at Signy Island
in the Maritime Antarctic. The effects of UV-B
radiation on four moss species (Sanionia uncinata,
Chorisodontium aciphyllum, Warnstorfia sarmen-
tosa and Polytrichum strictum) was investigated
(Figure 2). Levels of DNA damage were low
but comparable with concentrations found by
Lud et al. (2002, 2003). A significant difference
between mosses exposed to enhanced levels of
 145

35 35
Sanionia uncinata Warnstorfia sarmentosa
30 30

Absorbance (280 - 320 nm) . mg-1

Absorbance (280 - 320 nm) . mg-1

25 25

20 20

15 15

10 10

5 5

0 0
C UVA UVB1 UVB2 C UVA UVB1 UVB2

35 35
Chorisodontium aciphyllum Polytrichum strictum
30 30
-1
Absorbance (280 - 320 nm) . mg

-1
Absorbance (280 - 320 nm) . mg
25 25

20 20

15 15

10 10

5 5

0 0
C UVA UVB1 UVB2 C UVA UVB1 UVB2

Figure 1. Soluble UV-B absorbing compounds (acidified methanol extracts, see Rozema et al. 2001b) in four moss species from
outdoor experiments at Signy Island (6042¢ S, 4535¢ W) after 5 weeks (2 February until 6 March 2003) of exposure to UV-B radiation
simulating 15 or 30% ozone depletion (C=ambient control, UVA=UV-A control, UVB1=15% ozone depletion, UVB2, 30% ozone
depletion, error bars represent standard deviation, n=4). Around noon five randomly selected shoots per species per plot (four plots
per treatment) were collected . The top sections (circa 0.5 cm) of air dried shoots were pooled and used for methanol extraction.

UV-B and the controls (ambient UV-B levels) solar radiation leaves the natural relations of
could not be demonstrated. This suggests that the solar spectrum intact and avoids the UV-A
these mosses are well adapted to ambient levels of radiation produced by fluorescent tubes which is
UV-B radiation. thought to perhaps influence plant growth
(Newsham et al. 1996). These studies do not sim-
ulate ozone depletion scenarios but are valuable
Outdoor studies on the effects of solar UV-B and have substantially increased our knowledge of
on bryophytes: methodology the mechanisms behind UV-B effects on plants.
However, screens alter several other abiotic fac-
Outdoor experiments are important tools for tors other than incident radiation, notably tem-
studying changes to vegetation that might occur as perature and water availability (Kennedy 1995).
a result of stratospheric ozone depletion. There Recently, Krizek and Mirecki (2004) showed that
are several methods to manipulate UV-B radiation cellulose diacetate films, used in some UV-exclu-
in the field. In many field studies screens are used sion studies (ambient control), release phytotoxic
to filter the UV-B portion of the solar spectrum compounds.
(Rozema et al. 1997a; Ballare et al. 2001; Lud Newsham et al. (2002) and Newsham (2003)
et al. 2003). In this way ambient solar UV-B levels performed non-manipulative studies at Antarctic
can be compared with reduced levels of solar sites experiencing natural substantial stratospheric
UV-B radiation. Filtration of the UV-B band of ozone depletion. Multiple regression analyses
146

2 2
Sanionia uncinata Warnstorfia sarmentosa
DNA damage (CPD · Mb )

DNA damage (CPD · Mb )

-1

-1
1 1

0 0
C UVA UVB1 UVB2 C UVA UVB1 UVB2

2 2
Chorisodontium aciphyllum Polytrichum strictum
DNA damage (CPD · Mb-1)

DNA damage (CPD · Mb )

-1

1 1

0 0
C UVA UVB1 UVB2 C UVA UVB1 UVB2

Figure 2. DNA damage, expressed as cyclobutane pyrimidine dimers (CPDs) per million nucleotides (Boelen et al. 2002) in four moss
species from outdoor experiments at Signy Island after 3 weeks (2 February until 22 February 2003) of exposure to UV-B radiation
simulating 15 or 30% ozone depletion (C=ambient control, UVA=UV-A control, UVB1=15% ozone depletion, UVB2, 30% ozone
depletion, error bars represent standard deviation, n=4). Around noon five randomly selected shoots per species per plot (four plots
per treatment) were collected and immediately frozen at )80 C. The top sections (circa 0.5 cm) of the shoots were pooled and used for
DNA extraction.

indicated that the ratio of UV-B radiation to PAR
irradiance was the best predictor for concentrations
of UV-B screening pigments and carotenoids in
foliage of Antarctic bryophytes. Although this kind
of study gives insight into the effects of enhanced
levels of UV-B radiation arising from ozone
depletion, levels of UV-B depend on local condi-
tions and cannot be modified to simulate future
ozone depletion scenarios.
In UV-B supplementation studies, the vegetation
is exposed to UV-B radiation emitted by fluorescent
lamps, thus simulating a decrease in stratospheric
ozone concentration. In modulated outdoor
supplementation systems ambient UV-B levels are
monitored and the output of the UV-B lamps is
varied to supply a UV-B dose proportional to
ambient levels (Caldwell et al. 1983, Sullivan et al.
1994, Niemi et al. 2002b). The advantage of this
method is that local changes in irradiance, e.g.
caused by cloud cover, are accommodated for by
the system. However, modulated experiments need
complex and expensive lamp dimming systems and
sensors to monitor ambient and treatment UV-B
levels. Most of the lamp field experiments that have
taken place have used simpler and more robust
systems in which lamps have been switched on for a
specific period of time centred around solar noon
(e.g. Johanson et al. 1995; Gehrke 1998). In these
so-called ‘‘square wave’’ systems, exposure times
are calculated with mathematical models (e.g.
Green 1983) and expressed in terms of a certain
level of ozone depletion. Switching times are
adjusted every day or week to follow seasonal
patterns of solar radiation. In some experiments the

diurnal pattern of exposure has been improved by
switching on alternate lamps in several stages (‘‘step
wave’’ systems; e.g. Gehrke 1999). Since both sys-
tems do not compensate for overcast days, ratios of
UV-B:UV-A:PAR can differ between days.
Outdoor UV-B supplementation systems need
an electricity supply, which is sometimes not
available in the field. Besides this, the frames
that are necessary to support the lamps are
usually large, which can create problems on
steep slopes or places exposed to strong winds.
Gehrke et al. (1996), Gehrke (1998) developed a
small UV-B supplementation system to study
effects of enhanced UV-B radiation on an om-
brotrophic peatland ecosystem close to the
Abisko Scientific Research Station in northern
Swedish Lapland.
A mini UV-B supplementation system
In 2002 the Vrije Universiteit Amsterdam started
several long-term experiments to study the
effects of enhanced UV-B radiation on natural
vegetation. A mini UV-B supplementation system
was developed to expose vegetation in the Ant-
arctic, the Arctic and the Netherlands. A similar
system has been used for short-term experiments
in the Antarctic (Rozema et al. 1997b; Huiskes
et al. 2001; Rozema et al. 2001a; Lud et al. 2002,
2003).
The mini UV-B supplementation system uses
mini-fluorescent UV-tubes (Vilber-Lourmat
T-15M, 12 V, 15 W) that can be powered by bat-
teries when a regular electricity supply is not
available. Each lamp frame contains one UV-tube
(44 cm in length , 30 mm diameter, preburned for
70 h). Since these lamps are small, and cheap and
easy to transport, many individual lamps can be
used to increase the number of statistically inde-
pendent replicates. Our experimental design
incorporates two UV-B treatments (UV-B1 and
UV-B2) where short-wave UV-C radiation
(<280 nm) is excluded by cellulose acetate (CA)
filters placed on UV-B transmitting plexiglass
underneath each tube, one UV-A control treatment
(UV-A treatment, Mylar foil, same exposure time
as UV-B2 treatment) and a further control where
the fluorescent tubes are replaced by wooden bars
(control C). Each treatment is replicated four
times. The tubes are controlled by timers (Grässlin,
147
Germany) which automatically adjust the exposure
time every week to follow seasonal changes in
natural UV-B radiation (see below).
Lamp spectra at sample height (48 cm) were
measured using an Optronics 752 spectroradiom-
eter, calibrated against a NIST-traceable OL752-
10E standard lamp (Figure 3). The spatial distri-
bution of UV-B radiation emitted by the UV-B
lamps was measured using a UVX radiometer
(UVP Inc, Upland, USA) with a UVX-31 sensor.
A 25 –30% reduction of radiation levels was
recorded at the edges of each 30
35 m plot
(Figure 4a). Since UV-B levels increase strongly as
the distance between the vegetation and the UV-B
lamp decreases (Figure 4b), the lamp distance or
exposure time have to be adjusted as plant height
increases.
Biologically effective irradiances (BEIs) were
calculated from lamp spectra using Caldwell’s
(1971) generalised plant action spectrum, the
DNA action spectrum from, Setlow (1974) and the
new biological spectral weighting function
(BSWF) for plant growth from Flint and Caldwell
(2003a), all normalised at 300 nm. Lamp output
and terminal voltage of the batteries, that are used
to power the lamps when a regular power supply is
not available, are temperature dependent. To
estimate the influence of temperature and lamp
voltage on lamp output, these parameters were
investigated in a temperature controlled climate
room. Lamp output was dependent on tempera-
ture and tube voltage (Figure 5). In general lamp
output was lower at lower temperatures and
voltages.
Since CA foils degrade in time (Steeneken et al.
1995) the BEI under the lamp was recorded over
40 h. From these data the average lamp output
(average irradiance at sample height during 20 h:
Caldwell weighted: 0.079 W m)2, Setlow weigh-
ted: 0.076 W m)2, weighted with new BSWF
from Flint & Caldwell: 0.071 W m)2) was calcu-
lated. In the field foils were replaced after 20 h
exposure time. The extra UV-B doses required to
simulate a 15 or 30% reduction in ozone were
calculated using the irradiance model of Green
(1983) and computer encoded by Björn and
Murphy (1985). The outcome of this simulation
depends on the biological weighting function that
is used (Flint and Caldwell 2003a, b). We have
used the generalised plant action spectrum from
Caldwell (1971) since this is the most common
148

0.014

0.012
Irradiance (W · m · nm )

0.010
-1

0.008
-2

0.006

0.004

0.002

0.000

280 300 320 340 360 380 400

wavelength (nm)
Figure 3. Lamp spectra from UV-B minilamps at sample height (48 cm) after 9 h of exposure; dashed line: UV-C radiation excluded
with cellulose acetate (CA) foil (UV-B treatment), solid line: UV-C and UV-B radiation excluded with Mylar foil (UV-A treatment).

relative UV-B irradiance

1 2 3 4 5 6 7 8
15
(a) 75
(b) 0.00
75 85
90
10
90 85
80 0.10
distance from centre (cm)

80
distance from lamp (m)

85 90 95 95
90 85
5

0.20

0
80
95 95
85 90 90 85 0.30
-5

95
80 80 0.40
-10
90 90 I = 0.366 * d -1.365
85
75
85 R2 = 0.991
-15 0.50
-15 -10 -5 0 5 10 15
distance from centre (cm)

Figure 4. Spatial distribution of UV-B radiation emitted by the mini UV-B lamp system. (a) Contour plot of relative UV-B irradiance
(centre=100%) at sample height (48 cm). (b) Relative irradiance in the centre plotted against lamp distance.

used BSWF and in this way is possible to culated doses were used to determine the duration
compare our experiments with other (previous) of exposure time. The daily irradiation was cen-
field experiments. Average lamp output and cal- tred around solar noon.

0.10
0.09
Biologically effective irradiance (W m )
-2
0.08
0.07
0.06
0.05
0.04
0.03
0.02
0.01
0.00
10
Figure 5. Lamp output (Caldwell weighted biologically effective irradiance at sample height, 48 cm) and terminal voltage of the
batteries, that are used to power the lamps when a regular power supply is not available, are temperature dependent. To estimate the
influence of temperature and lamp voltage on lamp output these parameters were investigated in a temperature controlled climate
room. Lamp output was slightly dependent on temperature and tube voltage. In general lamp output is lower at lower temperatures
and at lower voltages.
Concluding remarks
Bryophytes are a significant species group of
terrestrial plants, especially in polar and sub-
polar regions where the relative increase in UV-
B radiation due to stratospheric ozone depletion
is high. In this review an attempt has been made
to summarise all outdoor studies on the effect of
UV-B radiation on bryophytes. Since there are
only a limited number of field studies on bryo-
phytes presented in the literature, a statistical
meta-analysis of these data has not been made
so far. However, nearly all studies demonstrated
that mosses are well adapted to ambient levels
of UV-B radiation since UV-B hardly affects
growth parameters. In all screening studies,
where reduced UV-B levels were compared with
ambient levels, no effect of UV-B reduction or
exclusion on photosynthesis, accumulation of
DNA damage and levels of UV-absorbing
compounds was found. DNA damage can
accumulate under enhanced levels of UV-B
149
4 ˚C
8 ˚C
12 ˚ C
11 12 13 14
Lamp voltage (V)
radiation, but is quickly repaired when lamps
are switched off. A few studies have demon-
strated that supplemental UV-B radiation can
influence photosynthetic activity and photosyn-
thetic pigments.
In a meta-analysis of outdoor studies on higher
plants, Searles et al. (2001) concluded that the
accumulation of UV-B absorbing compounds in
leaves was the most apparent effect of enhanced
UV-B radiation. This is probably not true for
bryophytes. In all studies where UV-B was arti-
ficially enhanced no increase of UACs was
found. However, two in situ studies from New-
sham et al. (2002) and Newsham (2003) sug-
gested that UACs were induced within 24 h
under naturally elevated UV-B radiation. Fur-
thermore, in all studies described above, soluble
UACs have been measured. Meijkamp et al. (in
preparation) showed that non-soluble (cell-wall
bound) compounds contribute largely to the
constitutive UV-screen in Vicia faba leaves.
Therefore in future studies the responses of
150
insoluble flavonoids to UV-B in bryophyte tis-
sues should be investigated.
Long-term studies have shown that even though
biomass production per area is not altered, shoot
morphology can be influenced by UV-B radiation.
Changes in plant morphology might affect eco-
system structure and function. For example, more
branching or a decrease in annual length incre-
ment can lead to reduced plant size, which can
shift the competitive balance by altering inter-
specific competition for visible light. To study
these subtle interactions it is essential to continue
these long-term experiments.
The mini UV-B supplementation system that
we have described here is especially designed to
study effects of UV-B radiation at remote field
locations under harsh conditions and is therefore
highly suited to perform long-term studies in the
Arctic or Antarctic. Polar ecosystems are char-
acterised by extreme aridity and low temperatures
and within this context it would be interesting to
consider potential interactions between UV-B
stress and other environmental factors, such as
water availability and temperature.
Acknowledgements
This work was funded by the Dutch council for
Scientific Research (NWO-ALW grant UVANT-
ARCTIC, No. 851.20.010). We would like to
thank Rod Strachan, Judith Dickson and Pete
Convey from the British Antarctic Survey and Stef
Bokhorst from the Netherlands Institute of
Ecology for their support at the long-term field
experiment at Signy Island. Logistic support from
the British Antarctic Survey is also gratefully
acknowledged. We would like to thank Eveline
Schut, Mariska Wagenaar and Rob Broekman for
technical assistance. We also thank Martien van
Vilsteren, Daan van Marum and Flip de Kriek
(Electronics department and Mechanical depart-
ment from de Vrije Universiteit Amsterdam) for
their skilful support in designing and constructing
the mini UV-B supplementation system. Anita G.
J. Buma and Willem van de Poll, University of
Groningen, are thanked for their help with DNA
damage analysis. Further we wish to thank K.
Newsham and L.O. Björn for constructive sug-
gestions on an earlier version of this manuscript.
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