Plant Ecology 128: 139147, 1997.

c 1997 Kluwer Academic Publishers. Printed in Belgium.

139

The effect of enhanced ultraviolet-B radiation on germination and seedling

development of plant species occurring in a dune grassland ecosystem
Marcel Tosserams, Esther Bolink & Jelte Rozema
Department of Ecology and Ecotoxicology, Faculty of Biology, Vrije Universiteit, De Boelelaan 1087, 1081 HV
Amsterdam, The Netherlands

Key words: Development, Dune grassland ecosystem, Germination, Ozone depletion, Plant growth, Seedlings,
UV-absorbing pigments, UV-B

Abstract
The germination of seeds of seven plant species occurring in a dune grassland vegetation of the Netherlands, was
studied at four levels of UV-B radiation simulating unto 45% stratospheric ozone reduction during April. With the
exception of seeds of Senecio jacobaea, germination of the dune grassland species was not affected by enhanced
UV-B irradiance. Although a clear UV-B fluence-response relationship was not observed, the germination rate of
S. jacobaea seeds and maximal germination percentage were reduced at enhanced UV-B. Germination rate in the
dark was higher than germination in the light for Oenothera biennis, Plantago lanceolata, Rumex obtusifolius and
S. jacobaea. Total dry biomass accumulation of seedlings was not affected by increased UV-B radiation in any of
the species tested. Clear-cut differences in UV-absorbance of methanolic extracts were observed between species.
Enhanced UV-B irradiance stimulated UV-absorbance of seedling extracts of Holcus lanatus and Verbascum thapsus.
A clear UV-B fluence-response relationship was observed for both species. The results indicate that germination of
the studied plant species probably will not be adversely affected by the expected stratospheric ozone reduction in
The Netherlands.
Introduction
Since a decrease of the earths stratospheric ozone
column thickness was observed and reports on the
causes of this phenomenon were published, a considerable amount of research has focused on the implications of increased solar UV-B radiation for life on earth
(Caldwell & Flint 1994; Teramura & Sullivan 1994).
Growth chamber studies as well as greenhouse and
field experimentation have led to a better understanding
of how enhanced solar UV-B radiation may affect plant
life. There are considerable differences in the UV-B
response of different plant species (Krupa & Kickert
1989, Tosserams et al. 1997) and between cultivars
of the same species (Biggs et al. 1981; Teramura &
Murali 1986; Barnes et al. 1993; Dai et al. 1994).
UV-B radiation may reduce plant growth and yield
(Tevini & Teramura 1989; Teramura & Sullivan 1994).
To avoid damage by UV-B radiation, plants evolved

*122992*

protective mechanisms. Photorepair is reported to be an

efficient mechanism for plants to ameliorate UV inflicted damage (Pang & Hays 1991; Chen et al. 1994). In
addition, the synthesis of UV absorbing compounds in
the epidermal layer of leaves and flowers, reduces the
UV-B fluence rate before it can cause damage to underlying tissues (Flint & Caldwell 1983; Tevini et al. 1991;
Stapleton & Walbot 1994; Lois & Buchanan 1994).
These absorbing compounds, mainly flavonoids, also
act as scavengers counteracting radical formation by
UV-B radiation (Larson 1988; Lonchampt et al. 1989).
It has been suggested that enhanced solar UVB radiation might directly or indirectly affect natural vegetation resulting in alterations of species composition (Tevini & Teramura 1989). However, experimental data concerning effects of enhanced UV-B radiation on plants in their natural environment is scanty
(Rozema et al. 1991; Caldwell & Flint 1994). Most of
the reports describe the effects of UV-B on seedlings

Article: VEGE 025ROZ, PIPS Nr. 122992 BIO2KAP

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140
and individual plants grown in pots. Other developmental stages like germination, flowering and seedset are less well documented. These stages in plant
development however, might prove to be susceptible to
UV-B. In a recent study by Musil (1995), dicotyledonous Asteraceae exhibited delayed flowering, decreased
flower production and reduced numbers of seeds set in
response to elevated UV-B. In addition, the latter study
as well as several earlier studies (Flint & Caldwell
1984; Feder & Shrier 1990), demonstrated the UVB sensitivity of pollen germination and pollen tube
growth. It is reasonable to assume that developmental
stages may have differential UV-B sensitivity, regarding that the maximal UV-B exposure of different developmental stages may vary considerably (Teramura &
Sullivan 1994).
In order to obtain a better understanding of the
consequences of increased solar UV-B radiation on
natural ecosystems it is important to evaluate effects of
UV-B radiation on all developmental stages during the
life history of a specific plant species. The aim of the
present study was to determine to what extent enhanced
UV-B radiation influences seed germination and initial
seedling development of different plant species of a
dune grassland ecosystem in The Netherlands.

Material and methods

Experimental design. Caryopses of the grass species
Bromus hordeaceus L. and Holcus lanatus L., seeds
and fruits of the herbaceous species Oenothera biennis L., Plantago lanceolata L., Senecio jacobaea L.,
Rumex obtusifolius L. and Verbascum thapsus L., were
collected in a dune grassland (Heemskerk, NoordHolland, The Netherlands, 52 N, 4 E). Experiments
were conducted in a greenhouse from January till April
1993. For each species 32 petri-dishes each containing
two paper filters (Schleicher and Schuell, 90 mm) and
fifty seeds (6 rows of 7 seeds and one row of 8 seeds),
were used. During the course of the experiment, the filtration papers were humidified regularly with demineralized water. The distance between adjacent seeds was
sufficient ( 5 times seed diameter) to avoid mutual
influences (Justice 1972). The top of all petri-dishes
was removed after which the dishes were divided into
4 groups of 8 dishes. Per group 4 petri-dishes were
covered with UV-B transparent acrylic glass (Type 006;
50  12  0.3 cm) and cellulose acetate foil (50 
12  0.01 cm). This combination transmits radiation
290 nm (Figure 1). The remaining 4 petri-dishes

Figure 1. Spectral irradiance as received by the seeds of the UV-B

treatment and the respective control. (
) Acrylic glass covered
with cellulose acetate (absorbance 290 nm); (
) Acrylic glass
covered with polyester foil (absorbance 313 nm). Measurements
were conducted using an Optronics OL 752 Spectroradiometer.

were also covered with acrylic glass but the cellulose

acetate was replaced by polyester foil (Mylar, Type
S; 12  50  0.013 cm) this combination transmits
radiation 313 nm (Figure 1) and served as the UVA control treatment. Each group was placed underneath a lamp system consisting of two Philips 40W/12
UV-B fluorescent tubes covered with cellulose acetate
(0.1 mm, transmittance
290 nm; Tamboer & Co.
Chemie B.V., Haarlem, The Netherlands), suspended
on both sides of a Philips 400W HPI/T lamp. Because
of photodegradation, the cellulose acetate wrapped
around the UV-B tubes was replaced twice a week.
All treatments were screened from adjacent treatment
by a sheet of polyester foil. The UV-B lamps operated
from 1000 till 1600 h daily. The spectral irradiance
underneath the filters was measured with a doublemonochromator spectroradiometer (Optronic Model
OL 752, Orlando, FL, USA). The spectroradiometer
was calibrated for absolute responsivity against a 200
W tungsten-halogen standard lamp (Optronic Model
OL 752-10, Orlando, FL, USA). Before the measurements, wavelength accuracy was checked with a dual
calibration and gain check source module (Optronic
Model OL 752150, Orlando, FL, USA), by scanning
a low-pressure mercury vapour lamp with a known
peak emission at 312.9 nm.
Using the generalised plant action spectrum (Caldwell 1971) normalised at 300 nm, the daily biologically
effective UV-B radiation (UV-BBE ) levels received by
the seeds of the different groups were 2.46, 4.35, 5.75
and 9.18 kJ m,2 day,1 . According to an empirical

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model designed by Green et al. (1980), the lowest UVBBE level is comparable to the ambient UV-BBE (2.98
kJ m,2 day,1 ) on a clear day during April in The
Netherlands. The other UV-BBE levels simulate a situation of 17, 28 and 45% stratospheric ozone reduction
respectively in the same month. The UV-BBE received
by the seeds in the UV-A control groups was 0.033,
0.052, 0.070 and 0.105 kJ m,2 day,1 respectively.
In addition, four petri-dishes each with fifty seeds of
the same species, were wrapped in aluminium foil.
One of these dishes was placed underneath each lamp
system to test whether microclimate at the different
sites in the greenhouse influenced germination. The
400W HPI/T lamps provided 250 mol m2 s,1 additional photosyntheticallyactive radiation (PAR) during
16 hours a day. The maximal value of PAR measured
on a clear day was 800 mol m2 s,1 . Temperature
during the experiment varied between 13.9 C (night)
and 34.5 C (day).
Measurements. To determine the weight and the
water content of the seeds, fresh and dry weight (48 hr,
70 C) of 50 seeds per plant species were determined.
The number of germinated seeds was counted twice
a day. A seed was defined germinated at the moment
the radicula appeared. When all seeds had germinated or no further germination was observed, counting was stopped. After the germination experiment,
the UV absorbance of the seedlings was determined.
UV absorbing compounds were extracted with 5 ml of
an acidified methanolic solution (CH2 OH:HCl:H2 O,
79:1:20 v/v) from approximately 15 mg of fresh plant
material per petri-dish. Because seedlings of V. thapsus
were very small, all plant material was used for the
determination of UV absorbance. The extracts were
stored for one night (8 C) after which they were boiled
for 10 minutes at 90 C in a waterbath. The absorbance of the solution was measured with a Perkin-Elmer
Lambda 15 UV/VIS Spectrophotometer at either 300
or 310 nm. Total dry weight (48 hr, 70 C) per petridish was determined for all species except V. thapsus.
Statistics. All data were subjected to analysis of variance (ANOVA; Sokal & Rohlf, 1981). Dry weight data
were transformed to their natural logarithms. Analysis
of variance for repeated measurements was used for
the analysis of germination data.

Table 1. Biomass and water content of 50 seeds of the plant species

used. Values presented are means of 2 replicate measurements
SEM

Plant species

Fresh weight Dry weight Water content

(mg)
(mg)
(%)

Monocotyledons
Bromus hordeaceus 204
Holcus lanatus
11.2

 4.0
 0.3

182
10.1

 3.4
 0.6

10.8
10.1

 0.1
 3.0

Dicotyledons
Oenothera biennis
Plantago lanceolata
Rumex obtusifolius
Senecio jacobaea
Verbascum thapsus

 0.7
 3.0
 0.9
 0.2
 0.0

24.4
76.2
55.5
11.3
7.5

 0.7
 2.7
 0.8
 0.2
 0.2

6.9
10.5
11.2
6.7
9.5

 0.1
 0.1
 0.1
 0.2
 2.3

26.2
85.1
62.5
12.1
8.3

Results and discussion

Large differences of seed biomass were observed
between the different species (Table 1). Fresh weight
of reproductive units varied between 166 (V. thapsus)
and 4,080 g (B. hordeaceus). According to Harrington (1972), the water content of seeds should ideally
be 5-14%. The water content of all seeds used in this
experiment lies well within this range.
Receiving 7.1 kJ m,2 day,1 UV-BBE , seed germination of radish was reduced by 26%, while germination
of cucumber and bean was reduced by 23% when compared with control plants receiving 0.2 kJ m,2 day,1
UV-BBE (Tevini et al. 1983). In contrast, Krizek (1975)
observed no adverse effects on the percentage of germination for a range of crop species after 72 h of continuous exposure to UV-B irradiance. Germination of
Silene vulgaris seeds originating from a highland and
a lowland population was also unaffected by enhanced
UV-B irradiance (van de Staaij 1994). Musil (1995)
reported enhanced germination for several dicotyledonous and monocotyledonous arid-environment ephemerals. In the present experiment maximal seed germination (Figures 2 and 3) of control treatments varied
between 74% (P. lanceolata) and 97% (B. hordeaceus,
R. obtusifolius and V. thapsus). Enhanced UV-B only
affects the maximal germination percentage of S. jacobaea (Figure 3). For this species, both germination rate
and the maximal germination percentage were negatively affected by enhanced UV-B radiation. A clear
UV-B fluence-response relationship however, was not
observed. A significant UV-B effect (p=0.008) was
only present at 4.35 kJ m,2 day,1 UV-BBE . Possibly,

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Figure 2. The effect of UV-B irradiance on germination of dune grassland plant species . In each treatment seeds either received 9.18 kJ m,2
day,1 UV-BBE ( ) or did not receive UV-B ( ). The other UV-BBE treatments are not presented because they did not significantly differ from
the presented data. Germination data of dark controls ( ) was only included when it was significantly different from the other treatments. All
presented data are means of 4 replicates SEM.

the seed coat of most species provides sufficient protection against deleterious UV-B effects (Krizek 1975).
Dark controls of O. biennis, P. lanceolata, R.
obtusifolius and S. jacobaea had a higher germination
rate as compared to germination in the light (Figures 2
and 3). Dark and light germination of the other plant
species tested was comparable (data not shown).
Total seedling dry weight of all species tested was
not affected by enhanced UV-B irradiance (Figure 4).
In accordance, Krizek (1975) reported no adverse
effects on dry weight accumulation of a variety of crop
species after 72 h of continuous UV-B irradiance. A
marked decrease of dry weight was reported by Tevini
et al. (1983) for bean and cucumber seedlings.
The accumulation of UV absorbing compounds
(e.g. flavonoids) in epidermal tissue appears to be
an important protective mechanism, which effectively reduces the detrimental action of UV-B irradiance on plants (Middleton & Teramura 1993; Kootstra
1994; Lois & Buchanan 1994; Stapleton & Walbot
1994). The absorbance of UV-B radiation by flavonoids and related phenolic compounds varies between
cultivars and species (Teramura et al. 1991; Day et

al. 1994; Wand 1995). In agreement, clear-cut differences in UV-B absorbance between seedling extracts
of the control treatments were observed in the present
experiment (Figure 5). Controls of O. biennis had the
highest absorbance ( 0.65) while the lowest absorbance (between 0.1 and 0.15) was observed in R. obtusifolius and V. thapsus seedlings.
In many plant species UV-B irradiation enhances
the accumulation of absorbing compounds (Tevini &
Teramura 1989). This UV-B-enhanced accumulation
is due to a higher activity and/or higher rate of biosynthesis of L-phenylalanine ammonia-lyase (PAL). This
enzyme regulates the diversion of L-phenylalanine into
precursors for secondary phenolics. In barley primary
leaves UV-B irradiance prolonged the activity of PAL
resulting in an enhanced accumulation of UV absorbing compounds (Liu & McClure 1995). The influence
of UV-B on the stimulation of UV-B absorbance varied between species. Absorbance of B. hordeaceus,
O. biennis, P. lanceolata, R. obtusifolius and S. jacobaea remained unaffected by increasing UV-B levels,
whereas the UV-B absorbance of H. lanatus and
V. thapsus was increased by UV-B enhancement. The

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Figure 3. The effect of UV-B irradiance on germination of S. jacobaea seeds. Four UV-BBE levels were applied: (A) 2.46 kJ m,2 day,1 ; (B)
4.35 kJ m,2 day,1 ; (C) 5.75 kJ m,2 day,1 ; (D) 9.18 kJ m,2 day,1 . In each treatment seeds were either irradiated with UV-B ( ) or did not
receive UV-B ( ). Germination of dark controls ( ) is only included in D. All presented data are means of 4 replicates SEM.

UV-B absorbance of H. lanatus seedlings was stimulated by 37, 61, 74, and 99% when the different UVB treatments were compared to their respective controls. This is in agreement with results of Wellmann
(1985) who demonstrated the linear dependency of
flavonol accumulation with UV-B fluence. Seedlings
of V. thapsus also exhibited a clear UV-B fluenceresponse relationship. For this species the maximal
stimulation of absorbance was 28% at the highest UVB treatment.
Although large differences between species were
observed, the presence and/or accumulation of absorbing compounds may already protect the seedlings
against detrimental effects of UV-B radiation directly
after emergence from the soil. Enhanced UV-B fluence rates might however stimulate the accumulation
of phenolic compounds in some species, which may
affect herbivory (Coley et al. 1985), litter quality and
decomposition processes (Gehrke et al. 1995, Rozema

et al. 1997) in natural environments. However, other

environmental factors like drought and mineral deficiency have also been shown to stimulate the accumulation of phenolic compounds in plants (Balakumar et
al. 1993; Murali & Teramura 1985). Therefore, further studies on the interaction of these factors with
enhanced UV-B radiation are necessary to elucidate
the contribution of UV-B in the accumulation of these
compounds in natural ecosystems.
Our results indicate that germination and early
seedling development are not adversely affected by
enhanced UV-B irradiance. Even at the relatively high
UV-BBE levels used in this experiment, no reduction of
germination rate and capacity was observed for most
species tested. In natural environments several factors
may influence the maximal UV-B exposure of germinating seeds. First of all timing of germination is
important. In the field, germination may occur largely
in the dark, avoiding solar irradiance. Secondly, the

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Figure 4. The influence of enhanced UV-B irradiance on dry matter accumulation of seedlings. Seedlings received no UV-B ( ) or additional
UV-B ( ). Values presented are means of 4 replicates SEM. Bars marked with the same letter are not significantly different (p 0.05). Data
for V. thapsus was not available because all seedlings were used for the determination of UV-absorbance.

position of the seed in the soil profile is important.

Thirdly, vegetation density may markedly influence
the UV-B climate at soil level. Even in the relatively
sun exposed dune grassland ecosystem, germination
is expected to occur at a relatively low UV-BBE level.

Therefore, we conclude that the expected ozone reductions for The Netherlands (WMO 1994) will probably
not negatively influence germination of plant species
of the dune grassland ecosystem.

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Figure 5. The influence of enhanced UV-B irradiance on UV-B absorbance of methanolic seedling extracts. Seedlings received no UV-B ( ),
additional UV-B ( ) or were kept in the dark ( ). Absorbance was measured at 300 (B. hordeaceus, O. biennis, S. jacobaea and V. thapsus) or
310 nm (H. lanatus, P. lanceolata and R. obtusifolius) and was recalculated to a concentration of 1 mg fresh material per ml extraction solution.
Values presented are means of 4 replicates SEM. Bars marked with the same letter are not significantly different (p 0.05).

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Acknowledgements
We would like to thank dr Joe Sullivan and Professor
dr W.H.O. Ernst for their critical comments on the
manuscript. This work was supported by the Dutch
National Research Programme on Global Air Pollution
and Climate Change (NRP project number: 850022).

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