Limnetica 25(1-2)01 12/6/06 13:54 Página 81

Limnetica, 25(1-2): 81-94 (2006)

The ecology of the Iberian inland waters: Homage to Ramon Margalef
© Asociación Española de Limnología, Madrid. Spain. ISSN: 0213-8409

Effects of ultraviolet radiation on aquatic bryophytes

Javier Martínez-Abaigar*, Encarnación Núñez-Olivera, María Arróniz-Crespo,
Rafael Tomás, Nathalie Beaucourt, Saúl Otero

Universidad de La Rioja. Complejo Científico-Tecnológico, Madre de Dios 51, 26006 Logroño (La Rioja), Spain
*Corresponding author: [email protected]

ABSTRACT

The depletion of the stratospheric ozone layer as a result of anthropogenic activities increases the ultraviolet-B (UV-B) irra-
diance at ground level. This may lead to harmful biological consequences affecting photosynthetic organisms. Mountain stre-
ams are especially exposed to a UV-B increase, and bryophytes play a key ecological role in them. In this paper, the effects of
enhanced UV-B radiation on photosynthetic organisms in general and on bryophytes in particular are described. Hereafter,
some results obtained by our group on the effects of UV-B on bryophytes from mountain streams are presented. Laboratory
and field experiments show that these effects depend on the species, the environmental factors (such as temperature), and the
origin of the samples (sun or shade conditions, low or high altitude). Among the variables measured, the maximum quantum
yield of photosystem II (Fv/Fm) and the level of UV-absorbing compounds seem to be the most responsive to enhanced UV-B,
but no variable responded in the same manner in every species. The potential use of aquatic bryophytes as bio-indicators of
changes in ambient UV-B radiation would require an adequate selection of both variables and species. Promising variables are
Fv/Fm, the concentration of UV-absorbing compounds (especially if they are analyzed individually) and DNA damage, where-
as the liverwort Jungermannia exsertifolia subsp. cordifolia has been revealed to be a good bio-indicator species. Globally, the
responses of aquatic bryophytes to UV-B radiation and their protecting systems are still poorly characterized, and thus further
study is required under both controlled and field conditions.

Keywords: aquatic bryophytes, mosses, liverworts, ultraviolet-B (UV-B) radiation, mountain streams, bio-indicators.

RESUMEN

La degradación antropogénica de la capa de ozono estratosférico provoca un aumento de la radiación ultravioleta-B (UV-B)
en la superficie de La Tierra. Esto puede causar consecuencias biológicas nocivas en los organismos fotosintéticos. Los arro-
yos de montaña están especialmente expuestos al aumento de UV-B, y los briófitos desempeñan un papel ecológico crucial en
estos ecosistemas. En el presente artículo, se describen los efectos de un aumento de radiación UV-B sobre los organismos
fotosintéticos en general y sobre los briófitos en particular. A continuación, se presentan algunos resultados obtenidos por
nuestro grupo de investigación sobre los efectos de la radiación UV-B en briófitos de arroyos de montaña. Los experimentos
realizados tanto en campo como en laboratorio muestran que dichos efectos dependen de la especie considerada, de los facto-
res ambientales (como la temperatura) y de la procedencia de las muestras (aclimatadas a condiciones de sol o sombra, pro-
venientes de baja o elevada altitud). Entre las variables analizadas, el rendimiento cuántico máximo del fotosistema II (Fv /Fm)
y el nivel de compuestos absorbentes de radiación UV parecen ser las que mejor responden a un aumento de UV-B, pero nin-
guna variable responde de la misma manera en todas las especies. El uso potencial de los briófitos acuáticos como bioindica-
dores de cambios en los niveles naturales de radiación UV-B requiere una selección adecuada tanto de las variables analiza-
das como de las especies empleadas. Fv /Fm y la concentración de compuestos absorbentes de radiación UV (en especial si
éstos son analizados individualmente), junto con los daños en el ADN, parecen ser las variables más prometedoras en este
campo, mientras que la hepática Jungermannia exsertifolia subsp. cordifolia podría resultar una buena especie bioindicadora.
Desde un punto de vista global, las respuestas de los briófitos acuáticos a la radiación UV-B, y los mecanismos protectores
que utilizan para hacerle frente, están todavía poco caracterizados, y en consecuencia se necesita una mayor investigación en
condiciones controladas y en campo.

Palabras clave: briófitos acuáticos, musgos, hepáticas, radiación ultravioleta-B (UV-B), arroyos de montaña, bioindicadores.
Limnetica 25(1-2)01 12/6/06 13:54 Página 82

82 Martínez-Abaigar et al.

ULTRAVIOLET RADIATION AND damage, and changes in mineral absorption

ITS EFECTS ON PHOTOSYNTHETIC can occur. This may lead to alterations in
ORGANISMS growth and development. However, some
controversy about the ecological relevance of
Ultraviolet (UV) radiation induces many harm- these effects still persists (Fiscus & Booker,
ful effects in all living organisms, including 1995; Allen et al., 1998; Searles et al.,
humans. UV-C radiation (<280 nm) is ecologi- 2001a). At the ecosystem level, UV-B can
cally not relevant since it is absorbed by atmos- affect decomposition, nutrient cycling, and
pheric oxygen and ozone. However, both UV-B trophic interactions (Caldwell et al., 1998).
(280-315 nm) and UV-A (315-400 nm) penetra- Photosynthetic organisms may develop a
te to the biosphere and have significant biologi- number of protection and repair mechanisms
cal effects, although only UV-B is absorbed by against the adverse effects of UV-B (Jansen
the stratospheric ozone layer. Biological res- et al., 1998): production of UV-absorbing
ponses to UV radiation are highly dependent on compounds (flavonoids, phenyl-propanoids,
wavelength, and thus the biologically effective mycosporine-like aminoacids, etc.), antioxi-
UV (UVBE) can be calculated. UVBE encom- dant and photo-protective mechanisms, and
pass UV-A and UV-B, but, given the logarith- DNA-repairing processes.
mic increase of its effects with the decrease in Much of the research regarding the effects
wavelength, it is often dominated by UV-B, of UV-B on photosynthetic organisms has
especially at its shorter wavelengths. Thus, focused on terrestrial environments, especially
most studies on the effects of UV radiation using crop plants, whereas aquatic ecosystems
have dealt with UV-B. have received less attention. The vast majority
UV-B irradiance at ground level depends of the studies concerning aquatic ecosystems
on a number of factors, such as latitude, sea- have dealt with marine phytoplankton and
son, hour of the day, altitude, presence of macroalgae (Figueroa & Gómez, 2001; Day &
clouds or aerosols, and surface reflectivity Neale, 2002; Häder et al., 2003; Helbling &
(Björn, 1999). In addition, ozone depletion as Zagarese, 2003), while the photosynthetic
a result of anthropogenic emissions of halo- organisms from freshwater ecosystems have
genated carbon compounds leads to an incre- been less studied in line with their minor con-
ase in UV-B. In mid-latitudes, the ozone loss tribution to the global biomass and primary
has led to a 6 to 12 % increase in UV-B radia- production of aquatic systems. However,
tion above 1980 levels, and predicted changes rivers and lakes have an outstanding ecologi-
show the ozone layer will remain vulnerable cal importance as local systems and, because
to further depletion in the near future of their lower depth compared to marine
(McKenzie et al., 2003). Consequently, stu- systems, they are highly exposed to the harm-
dies on the effects of ambient and elevated ful effects of UV-B radiation. In lakes, the
UV-B irradiances are increasingly important. penetration of UV radiation and its effects on
In humans, an excessive exposure to UV-B phytoplankton have been the most studied
causes acute and chronic damage to eyes and topics (see for instance Villafañe et al., 1999;
skin, including sunburn and cancer, and com- Huovinen & Goldman, 2000; Laurion et al.,
promises the immune system (Vanicek et al., 2000), but macrophytes have also been occa-
1999). In photosynthetic organisms, increa- sionally considered (Rae et al., 2001). In
sed UV-B may cause diverse damage in the rivers, scarce work has been done (Rader &
photosynthetic apparatus: pigment degrada- Belish, 1997a, 1997b; Kelly et al., 2003), pro-
tion, photoinhibition, and decreases in quan- bably due to intrinsic methodological pro-
tum yield, photosynthetic rate, and the acti- blems derived from their strongly dynamic
vity of the Calvin cycle enzymes (Jansen et environmental conditions (depth, discharge,
al., 1998). Also, DNA alterations, oxidative water velocity, chemistry, etc.).
Limnetica 25(1-2)01 12/6/06 13:54 Página 83

Ultraviolet radiation and aquatic bryophytes 83

ULTRAVIOLET RADIATION The results obtained are conflicting, since UV-

AND BRYOPHYTES B radiation has been found to either stimulate,
to depress, or to have no effect on bryophyte
To our knowledge, around 65 papers have been performance. Several studies have found a
published on the effects of UV-B radiation on growth reduction in bryophytes when exposed
bryophytes, among which only 49 contain ori- to UV-B (Sonesson et al., 1996; Gehrke et al.,
ginal data (Table 1). Half of these are strictly 1996; Markham et al., 1998; Gehrke, 1998,
bryological, whereas the remaining ones study 1999; Ballaré et al., 2001), but this effect seems
bryophytes together with other photosynthetic to depend on the species considered, the experi-
organisms, such as vascular plants or lichens. mental design and other additional factors such
The research on this topic has focused mainly as water availability and CO2 concentration.
on terrestrial and semi-aquatic bryophytes Other harmful effects (chlorophyll degradation,
from Antarctic habitats and circumpolar heath- reduction in photosynthesis rates and Fv/Fm)
lands and peatlands. The most used species are even less clear, since contradictory results
belong to mosses: several Sphagnum species, have been found. In addition, the increase in
Hylocomium splendens (typical from fo- UV-absorbing compounds, which represents the
rest soils), and Polytrichum commune (typical most usual response of vascular plants to
from a wide range of acid habitats in damp to enhanced UV-B (Searles et al., 2001a), has only
wet situations). Liverworts have been notably been manifested occasionally in bryophytes
less studied than mosses, whereas no hornwort (Markham et al., 1990; Ihle & Laasch, 1996;
has been investigated. Newsham et al., 2002; Martínez-Abaigar et al.,
Diverse methodological approaches have 2003a). Beneficial effects of UV-B radiation on
been applied. Studies have been conducted bryophyte growth have also been reported
under both field and controlled conditions, and (Johanson et al., 1995; Searles et al., 1999;
in the latter case both in the laboratory and in Phoenix et al., 2001), which further complica-
the greenhouse. The manipulation of UV-B has tes the global interpretation of the results. This
included the two main experimental options in controversy contrasts with intuitive thoughts
the context of UV-B research (Rousseaux et that bryophytes would be strongly sensitive to
al., 2004): exclusion experiments using filters, UV-B radiation, because of their structural sim-
and supplementation using lamps to simulate plicity and the consequent lack of defenses
ozone depletion. The duration of the experi- commonly found in higher plants: thick cuti-
ments has been diverse, from a few hours of cles, epicuticular waxes, epidermis (sometimes
UV-B exposure (usually under controlled con- with several cell layers), hairs on leaf surfaces,
ditions) to several years (under field condi- etc. It must be taken into account that bryophy-
tions). The bryophyte responses have been te “leaves” are mostly mono-stratified and lack
assessed using morphological and, especially, air spaces, which dramatically reduces the
physiological variables: colour, symptoms of radiation pathway and thus its attenuation.
cell degradation, ultrastructural damage, scle- Thus, bryophytes (with the exception of thal-
rophylly, reproductive effort, growth (both in loid forms, which have been understudied in
length and dry mass), photosynthesis and res- relation to UV radiation), could only acquire
piration rates, chlorophyll fluorescence varia- chemical and metabolic defenses through, for
bles, photosynthetic pigment composition instance, UV-absorbing compounds, antioxi-
(chlorophylls, carotenoids), DNA damage (pre- dant mechanisms, and repairing systems of
sence of thymine dimers and other photopro- DNA and photosynthetic machinery. However,
ducts), protein and glucid concentrations, the present knowledge on UV-absorbing com-
mineral elements content, and the appearance pounds in bryophytes suggests that this mecha-
of UV-absorbing compounds which could nism does not occur in most bryophytes
serve as a protective mechanism. (Arróniz-Crespo et al., 2004), and the rest of
Limnetica 25(1-2)01 12/6/06 13:54 Página 84

84 Martínez-Abaigar et al.

the mechanisms have hardly been tested regard- ing systems are still poorly characterized, and
ing UV-B radiation. Globally, the responses of thus further study is required both under con-
bryophytes to UV-B radiation and their protect- trolled and field conditions.

Table 1. Original papers on the effects of UV radiation on bryophytes. Key for “Used Species”: L, liverwort; M, moss. Key for “Ambient”:
T, terrestrial; P, peatlands; A, aquatic; R, rivers or streams; L, lakes. Key for “Type of Experiment”: F, Field; G, greenhouse; L, laboratory;
E, exclusion of UV-B radiation; S, supplement of UV-B radiation; N, samples exposed to natural levels of solar radiation; VSh, very short
duration (less than 1 day); Sh, short duration (1-30 days); M, medium duration (longer than one month and shorter than 6 months); Lo, long
duration (6 months - 1 year); VLo, very long duration (longer than 1 year); ?, undetermined duration; H, historical study (comparison of
samples over a prolonged period). Key for “Variables used”: A, alterations in DNA; Fl, chlorophyll fluorescence; FlS, fluorescence spectra;
G, growth; H, hydric relations; M, morphology; Mt1, primary metabolites (glucids, proteins, lipids); Mt2, secondary metabolites, including
UV-absorbing compounds; N, mineral nutrients; Ox, variables of oxidative stress (peroxide content, lipid peroxidation, ascorbate, superoxi-
de dismutase, peroxidase, catalase); P, photosynthesis; Ph, phenology; PP, photosynthetic pigments; PS1 and PS2, activity of photosystems I
and II, respectively; R, respiration; Rf, reflectance indices; Sc, sclerophylly; U, ultrastructure. Artículos originales relacionados con los
efectos de la radiación UV sobre los briófitos. Clave para “Especies utilizadas”: L, hepática; M, musgo. Clave para “Ambiente”: T, terres-
tre; P, turberas; A, acuático; R, ríos o arroyos; L, lagos. Clave para “Tipo de experimento”: F, campo; G, invernadero; L, laboratorio; E,
exclusión de radiación UV-B; S, suplemento de radiación UV-B; N, muestras expuestas a niveles naturales de radiación solar; VSh, dura-
ción muy corta (menos de 1 día); Sh, duración corta (1-30 días); M, duración media (mayor de 1 mes y menor de 6 meses); Lo, duración
larga (6 meses - 1 año); VLo, duración muy larga (mayor de 1 año); ?, duración indeterminada; H, estudio histórico (comparación de
muestras a lo largo de un periodo prolongado). Clave para “Variables utilizadas”: A, alteraciones en el ADN; Fl, fluorescencia de clorofi-
la; FlS, espectros de fluorescencia; G, crecimiento; H, relaciones hídricas; M, morfología; Mt1, metabolitos primarios (glúcidos, proteínas,
lípidos); Mt2, metabolitos secundarios, incluyendo compuestos absorbentes de UV; N, nutrientes minerales; Ox, variables de estrés oxidati-
vo (contenido de peróxido, peroxidación de lípidos, ascorbato, superóxido dismutasa, peroxidasa, catalasa); P, fotosíntesis; Ph, fenología;
PP, pigmentos fotosintéticos; PS1 y PS2, actividad de los fotosistemas I y II, respectivamente; R, respiración; Rf, índices de reflectancia;
Sc, esclerofilia; U, ultrastructura.

Reference Used species Ambient Type of Variables used

experiment

Arróniz-Crespo et al. Chiloscyphus polyanthos (L), Jungermannia exsertifolia A (R) F, N Mt2, Sc

(2004) subsp. cordifolia (L), Marsupella sphacelata (L),
Scapania undulata (L), Brachythecium rivulare (M),
Bryum alpinum (M), Bryum pseudotriquetrum (M),
Fontinalis antipyretica (M), Palustriella commutata (M),
Philonotis seriata (M), Polytrichum commune (M),
Racomitrium aciculare (M), Rhynchostegium riparioides (M),
Sphagnum flexuosum (M)
Ballaré et al. (2001) Sphagnum magellanicum (M) P F, E, VLo G, Mt2
Barsig et al. (1998) Polytrichum commune (M) P G, S, M Mt1, Mt2, PP, U
Björn et al. (1998) Aulacomnium turgidum (M), Dicranum elongatum (M), T, P F, S, M-VLo G, H
Hylocomium splendens (M), Polytrichum commune (M),
P. hyperboreum (M), Sphagnum fuscum (M)
Conde-Álvarez et al. Riella helicophylla (L) A (L) L, E, VSh Fl, Mt2, P, PP, R
(2002)
Csintalan et al. (2001) Dicranum scoparium (M), Leucobryum glaucum (M), T L, S, Sh-M Fl, FlS, Mt2
Mnium hornum (M), Pellia epiphylla (L),
Plagiomnium undulatum (M), Plagiothecium undulatum (M),
Polytrichum formosum (M),
Sphagnum capillifolium (M), Tortula ruralis (M)
Gehrke (1998) Sphagnum fuscum (M) P F, S, VLo G, M, Mt2, P, PP, R
Gehrke (1999) Hylocomium splendens (M), Polytrichum commune (M) T, P F, S, VLo G, M, Mt2, PP
Gehrke et al. (1996) Hylocomium splendens (M), Sphagnum fuscum (M) T, P F, S, VLo G, H, Mt2, PP
Huiskes et al. (1999) Sanionia uncinata (M) T - -
Huiskes et al. (2001) Sanionia uncinata (M) T F, E, Sh Fl
Huttunen et al. (1998) Dicranum sp. (M), Hylocomium splendens (M), T, P G, S, ? M
Polytrichum commune (M)
Limnetica 25(1-2)01 12/6/06 13:54 Página 85

Ultraviolet radiation and aquatic bryophytes 85

Table 1. Continued. Continuación.

Reference Used species Ambient Type of Variables used

experiment

Huttunen et al. (2005a) Dicranum scoparium (M), Funaria hygrometrica (M), T, P N, H M, Mt2
Hylocomium splendens (M), Pleurozium schreberi (M),
Polytrichum commune (M), Polytrichastrum alpinum (M),
Sphagnum angustifolium (M), S. capillifolium (M),
S. fuscum (M), S. warnstorfi (M)
Huttunen et al. (2005b) Hylocomium splendens (M), Pleurozium schreberi (M) T N, H M, Mt2
Ihle (1997) Conocephalum conicum (L) T L, S, VSh Mt1
Ihle & Laasch (1996) Conocephalum conicum (L) T L, S, VSh-Sh Fl, Mt1, Mt2, P
Johanson et al. (1995) Hylocomium splendens (M) T G, S, ? G, Ph
Lewis Smith (1999) Bryum argenteum (M), Bryum pseudotriquetrum (M), T F, E, M G
Ceratodon purpureus (M)
Lovelock & Robinson Bryum pseudotriquetrum (M), Ceratodon purpureus (M), T F, N, ? Mt2, PP, Rf
(2002) Grimmia antarctici (M)
Lud et al. (2002) Sanionia uncinata (M) T F, L, E, S, VSh-VLo A, G, Fl, M,
P, Mt2, PP
Lud et al. (2003) Sanionia uncinata (M) T F, E, S, VSh-Sh A, Fl, Mt2, P, PP, R
Markham et al. (1990) Bryum argenteum (M) T N, H Mt2
Markham et al. (1998) Marchantia polymorpha (L) T G, S, M G, M, Mt2, Ph
Martínez-Abaigar et al.Jungermannia exsertifolia subsp. cordifolia (L), A (R) L, S, M Fl, Mt2, P, PP, R, Sc
(2003a) Fontinalis antipyretica (M)
Martínez-Abaigar et al.Jungermannia exsertifolia subsp. cordifolia (L), A (R) L, S, M G, M
(2003b) Fontinalis antipyretica (M)
Montiel et al. (1999) Sanionia uncinata (M) T F, S, ? Fl
Newsham (2003) Andreaea regularis (M) T F, N, M Mt2, PP
Newsham et al. (2002) Sanionia uncinata (M), Cephaloziella varians (L) T F, N, Sh-M Fl, Mt2, PP
Newsham et al. (2005) Cephaloziella varians (L) T F, N, E, M Mt2, PP
Niemi et al. (2002a) Sphagnum angustifolium (M), S. papillosum (M), P F, S, M G, Mt2, PP
S. magellanicum (M)
Niemi et al. (2002b) Sphagnum balticum (M), Sphagnum papillosum (M) P F, S, M G, Mt2, PP
Núñez-Olivera et al. Jungermannia exsertifolia subsp. cordifolia (L), A (R) L, S, M Fl, G, Mt1, Mt2,
(2004) Fontinalis antipyretica (M) P, PP, R, Sc
Núñez-Olivera et al. Jungermannia exsertifolia subsp. cordifolia (L), A (R) L, S, Sh Fl, Mt1, Mt2, P,
(2005) Fontinalis antipyretica (M) PP, R, Sc
Phoenix et al. (2001) Hylocomium splendens (M) T F, S, VLo G, H
Post & Vesk (1992) Cephaloziella exiliflora (L) T F, N, Sh M, Mt2, P, PP, U
Prasad et al. (2004) Riccia sp. (L) T L, S, VSh Ox, PP, PS1, PS2
Rader & Belish (1997a) Fontinalis neomexicana (M) A (R) F, E-S, M G
Robinson et al. (2005) Grimmia antarctici (M) T F, E, VLo Fl, H, M, Mt2,
P, PP, Rf
Robson et al. (2003) Sphagnum magellanicum (M) P F, E, VLo G, M
Robson et al. (2004) Sphagnum magellanicum (M) P F, E, VLo G, M
Rozema et al. (2002) Tortula ruralis (M) T F, E, ? G, Mt2
Schipperges & Gehrke Hylocomium splendens (M), Sphagnum fuscum (M) T, P F-L, S, M- VLo G, H, P
(1996)
Searles et al. (1999) Sphagnum magellanicum (M) P F, E, Lo G, Mt2, PP
Searles et al. (2001b) Sphagnum magellanicum (M) P F, E, VLo G, M, Mt2
Searles et al. (2002) Sphagnum magellanicum (M) P F, E, VLo G, M, Mt2, PP
Sonesson et al. (1996) Hylocomium splendens (M) T L, S, M G, P
Sonesson et al. (2002) Dicranum elongatum (M), Sphagnum fuscum (M) P F, S, VLo G, H
Taipale & Huttunen Hylocomium splendens (M), Pleurozium schreberi (M) T F, S, M Mt2
(2002)
Takács et al. (1999) Dicranum scoparium (M), Leucobryum glaucum (M), T G, S, Sh-M Fl
Mnium hornum (M), Pellia epiphylla (L),
Plagiothecium undulatum (M), Polytrichum formosum (M),
Tortula ruralis (M)
Limnetica 25(1-2)01 12/6/06 13:54 Página 86

86 Martínez-Abaigar et al.

ULTRAVIOLET RADIATION AND any treatment condition, and there was a loss of
AQUATIC BRYOPHYTES FROM material in all samples from the beginning to the
MOUNTAIN STREAMS conclusion of the experiment, which casts doubt
on the significance of the results.
Before our studies, only two other ones had been For several reasons, we circumscribe our rese-
conducted on the effects of UV radiation on arch interest to the effects of UV-B radiation on
truly aquatic bryophytes (see Table 1), despite aquatic bryophytes from mountain streams.
the interest of how diverse organisms from diffe- Firstly, these ecosystems might be particularly
rent habitats respond to this environmental fac- exposed to the effects of UV-B radiation, since
tor. In Conde-Álvarez et al. (2002), samples of 1) the biologically active UV-B radiation increa-
the thalloid liverwort Riella helicophylla from a ses between 5 % and 20 % per 1000 m altitudi-
saline lake were cultivated throughout a natural nal increase (Björn et al., 1998); 2) UV-B radia-
daily light cycle under two radiation treatments: tion can easily reach the organisms because they
solar radiation (UV + photosynthetically active live at relatively low depths or even emersed, and
radiation or PAR) and solar radiation deprived of UV-B radiation can penetrate into the oligotro-
UV (PAR treatment). There were significant dif- phic waters typically occurring in mountain stre-
ferences between the two treatments in the ams; and 3) the low temperatures which prevail
maximum quantum yield of photo-system II during most of the year may limit the develop-
(Fv/Fm), the effective quantum yield of photo- ment of protection and repairing mechanisms
synthetic energy conversion of PSII (ΦPSII), the against UV-B radiation. Secondly, bryophytes
electron transport rate (ETR) and the initial are the most abundant primary producers in
slope of ETR vs. irradiance curve (all higher in mountain streams and are also important in
PAR plants than in UV+PAR plants throughout nutrient cycles and food webs (Bowden et al.,
the day), photosynthetic capacity (higher in PAR 1999; Núñez-Olivera et al., 2001). This domina-
plants only at noon), chlorophyll a (lower in tion suggests that they can withstand present
UV+PAR only at 11.00), and phenolic com- levels of UV-B radiation, but the underlying
pounds (higher in UV+PAR only at 13.30). No physiological mechanisms are unknown and the
differences between treatments were found in structural protections against UV-B are lacking
dark respiration, photochemical quenching, and (as it was mentioned above for bryophytes as a
carotenoid concentration, and only slight ones in group). Thirdly, bryophytes have an outstanding
non-photochemical quenching (higher in bio-indication ability in a number of pollution
UV+PAR only in the morning). Thus, UV radia- processes and environmental changes (see a
tion (particularly UV-B) caused some damage to recent review in Ah-Peng & Rausch de
the photosynthetic apparatus. Recovery of inhi- Traubenberg, 2004), which could suggest their
bited photosynthesis took place in the afternoon, potential use as bio-indicators of changes in UV-
therefore solar UV radiation did not cause irre- B levels. And finally, the scarcity of studies
versible damage in the short term. Rader & existing on this particular topic recommends
Belish (1997a) carried out a ten-week field increasing our knowledge on it, especially consi-
experiment in which samples of the moss dering the present social interest on the causes
Fontinalis neomexicana were transplanted from and consequences of global climate change.
a reference site to both a shaded and an open In our work, we have conducted both labora-
section of a mountain stream and were irradiated tory and field studies. In the laboratory, we have
with enhanced levels of UV-B radiation. The cultivated bryophytes under enhanced UV-B
transplants from the open site showed an impor- simulating a 20 % ozone depletion, with the aim
tant, although non-significant, reduction in dry to characterize bryophyte responses to higher
biomass with respect to those growing under than present UV-B levels. The applied biologi-
ambient conditions. However, the moss in this cally effective UV-B (UV-BBE) was 0.67 W m-2,
experiment failed to grow in any site and under equivalent to an exposure of 9.6 kJ m-2 d-1,
Limnetica 25(1-2)01 12/6/06 13:54 Página 87

Ultraviolet radiation and aquatic bryophytes 87

which was calculated using the generalized plant moss against UV-B radiation, at least under the
damage action spectrum of Caldwell (1971). We specific experimental conditions used. Also,
established three general radiation regimes the increment of UV-absorbing compounds
(PAR, PAR + UV-A, and PAR + UV-A + UV-B) in the liverwort might be a useful ecophysiologi-
to distinguish the effects of UV-A and UV-B cal tool in the bioindication of UV-B.
radiations separately. Bryophyte responses were The different response of the two studied spe-
analyzed in terms of sclerophylly, the photo- cies to UV-B radiation was also evident in their
synthetic pigment composition, the rates of net morphological features (Martínez-Abaigar et
photosynthesis and dark respiration, some varia- al., 2003b). When exposed to enhanced UV-B,
bles of chlorophyll fluorescence, and the UV- the moss showed brown colour, depressed
absorbing compounds. In addition, we occasio- growth, development of the central fibrilar body
nally measured DNA damage (through the in the cells, chloroplast disappearance and pre-
appearance of thymine dimers), protein concen- sence of protoplasts progressively vesiculose,
tration, length growth and morphological vacuolized and finally hyaline. These symptoms
symptoms (both macro- and microscopic). The are little specific and have been described in
duration of the experiments was diverse, from several pleurocarpous mosses as a response to
3 days to 4 months. We have concentrated our diverse processes of senescence and stress (both
studies on two species, the moss Fontinalis natural and anthropogenic). The uniquely speci-
antipyretica and the foliose liverwort Junger- fic response of the moss to enhanced UV-B was
mannia exsertifolia subsp. cordifolia (hereafter a colour change in the cell walls, from yellow to
J. cordifolia), which were always collected from orange-brown. In contrast, the exposed samples
streams between 1300 and 2000 m altitude. of the liverwort looked healthy and their macro-
The two bryophytes mentioned above res- and microscopic appearances were quite similar
ponded differently to the enhancement in UV-B to those of control samples.
radiation under controlled conditions, while UV- In the laboratory, we also examined the
A radiation had a scarce biological effect influence of temperature (2 ºC vs. 10 ºC) on
(Martínez-Abaigar et al., 2003a), as it occurred the physiological and morphological responses
in other experiments using bryophytes (Niemi et of Fontinalis antipyretica and Jungermannia cor-
al., 2002a, 2002b). The samples of the moss difolia to enhanced UV-B (Martínez-Abaigar et
which were irradiated with UV-B showed, with al., 2003b; Núñez-Olivera et al., 2004). The
respect to the control, decreases in the chlo- influence of temperature on the effects of UV-B
rophyll and carotenoid concentration, the chlo- radiation depended on the species: the higher the
rophyll a/b quotient, the chlorophylls/phaeopig- UV-B tolerance, the lower the influence of tem-
ments ratios, the net photosynthesis rates, the perature. Also, different morphological and
light saturation point, Fv/Fm and ETR. They also physiological variables showed varied responses
showed increases in the sclerophylly index to this influence. Particularly, the lower tempera-
(“leaf ” mass per area) and the dark respiration ture used in our study enhanced the adverse
rates. The majority of these changes were indica- effects of UV-B radiation on several important
tive of plant stress and some of them had been physiological variables (Fv/Fm, growth and chlo-
previously found in bryophytes exposed to rophylls/phaeopigments ratios) in the UV-B-sen-
enhanced UV-B radiation. However, the UV-B- sitive F. antipyretica, but not in the more UV-B-
irradiated samples of the liverwort only showed a tolerant J. cordifolia. Thus, the adverse effects of
decrease in Fv/Fm, which might be the most sen- cold and UV-B radiation were apparently additi-
sitive physiological variable to UV-B, together ve in the moss (probably because the develop-
with a 20 % increase in the concentration of UV- ment of protection mechanisms was limited by
absorbing compounds. This defense mechanism, cold), whereas this additiveness was lacking in
rarely described in bryophytes, would enable the the liverwort. We conducted a Principal Com-
liverwort to have a higher tolerance than the ponents Analysis (PCA) for both species using
Limnetica 25(1-2)01 12/6/06 13:54 Página 88

88 Martínez-Abaigar et al.

the physiological data obtained in the experi- (MEUVAC) and also different forms in their
ments and confirmed their different response to absorbance spectra in the UV band. The high
the concomitant action of UV-B and cold. levels of MEUVAC and the clearly hump-sha-
Another environmental factor that can in- ped spectra in the UV-B and UV-A wavelengths
fluence the response of different species to UV-B (280-400 nm), which were found in the liver-
radiation is their previous field acclimation to worts, contrasted with the low levels and non
sun or shade conditions (Núñez-Olivera et al., hump-shaped spectra generally found in the
2005). Shade samples of Fontinalis antipyretica mosses (except for Polytrichum commune).
were more sensitive to the UV-B treatment than Thus, the accumulation of MEUVAC might
sun samples, and Fv/Fm was the physiological represent a frequent and constitutive a protect-
variable which better discriminated both types of ing mechanism against UV-B radiation in liver-
samples, since it decreased 42 % in the shade worts, but not in mosses.
samples and only 27 % in the sun samples at the In another field experiment, we tested the
end of the culture period. In Jungermannia cor- effects of a natural altitudinal gradient of ultra-
difolia, controls and UV-B-treated samples were violet-B (UV-B) radiation, from 1140 to 1816 m
not significantly different in either the sun or the altitude, on the physiology of 11 populations of
shade samples. PCAs for each species, ranking Jungermannia cordifolia (Arróniz-Crespo,
the physiological results along the culture 2005). Several physiological variables showed
period, strongly supported these points. In con- significant linear relationships with altitude:
clusion, the shade samples were more sensitive global MEUVAC levels, the concentrations of
to UV-B than the sun samples, but only in the two phenolic derivatives, ETRmax and NPQmax
more UV-B-sensitive species. increased with altitude, whereas photoinhibition
We also determined that the sensitivity of percentage and respiration rates decreased. This
bryophyte species to artificially enhanced UV-B was also confirmed by a PCA, since most of
could be tested without having to cultivate the these variables represented significant loading
samples for a long period. A continuous UV-B factors ordinating populations by altitude. The
exposure of 78 h reproduced the differences in characteristics shown by high-altitude popula-
the responses of Fontinalis antipyretica and tions may confer tolerance to high UV-B levels,
Jungermannia cordifolia, which had been pre- and the specific response to UV-B of the two
viously found in longer experiments lasting 36- phenolic derivatives suggests that they could be
82 days (Núñez-Olivera et al., 2005). For this used as indicators of the spatial changes in UV-
short-term test, several culture conditions, B radiation. In addition, the concentrations of
which were known to accelerate the appearance these two phenolic derivatives increased specifi-
of damage, were imposed: high ratio UV- cally under artificially enhanced UV-B radiation
B/PAR, continuous UV-B exposure, and cold (unpublished results). An interesting question
temperature. This type of fast test may therefore remains to be solved: could these compounds be
be used instead of long-duration tests to evalua- used as indicators of temporal changes in UV-B,
te the UV-B tolerance of bryophytes. which could be related to ozone depletion?
The different nature of the protection mecha-
nisms between mosses and liverworts, which
had been previously pointed out for Fontinalis CONCLUSIONS AND PERSPECTIVES
antipyretica and Jungermannia cordifolia under
laboratory conditions, was tested in a field sur- 1. Our results demonstrate that the effects of
vey conducted for 14 aquatic bryophytes from UV-B radiation on aquatic bryophytes depend
mountain streams, 10 mosses and 4 liverworts primarily on the species, and thus they do not
(Arróniz-Crespo et al., 2004). The diverse spe- constitute a single functional group in this
cies showed significantly different levels of respect. The different responses to UV-B are
methanol-extractable UV-absorbing compounds revealed not only by changes in colour or in
Limnetica 25(1-2)01 12/6/06 13:54 Página 89

Ultraviolet radiation and aquatic bryophytes 89

key physiological variables, such as growth, 6. The use of aquatic bryophytes as bio-indica-
chlorophyll concentration, photosynthesis tors of changes in UV-B radiation requires an
rates or chlorophyll fluorescence parameters, adequate selection of both variables and spe-
but also by variables responsible for protect- cies. Promising variables regarding this point
ing mechanisms, such as the concentration of are Fv/Fm, because of its sensitivity to UV-B,
UV-absorbing compounds. In particular, the and the concentration of UV-absorbing com-
constitutive presence and/or inducible enhan- pounds, due to its remarkable specificity of
cement of UV-absorbing compounds depend response. The analysis of individual UV-
strongly on the species and, outstandingly, on absorbing compounds may have a stronger
the type of bryophyte (moss or liverwort) ecological and physiological relevance than
considered. the usual global analysis of these compounds,
2. It is recommendable to evaluate UV-B sensi- since each one may respond in a different
tivity in sufficiently prolonged experiments, manner to UV-B. Thus, a previous identifica-
however short-term (72 h) tests may render tion of the compounds occurring in the diffe-
comparable results. rent species is clearly needed. A third variable
3. The responses of aquatic bryophytes to UV-B potentially useful for bio-indication purposes
radiation depend not only on specific genetic could be the evaluation of DNA damage cau-
factors, but also on environmental factors (such sed specifically by UV-B radiation. Regard-
as temperature) and the origin of the samples ing the species selection, our results point at
(sun or shade conditions, low or high altitude). Jungermannia cordifolia because of its good
The effects of these factors depend on the spe- responsiveness to UV-B, availability of
cies: in the UV-B sensitive ones, both cold and healthy biomass throughout the year (if popu-
previous shade acclimation may exacerbate the lations are selected properly), and wide distri-
harmful effects of enhanced UV-B. bution range over mountain streams of the
4. Among the variables measured under labora- northern hemisphere.
tory conditions, the maximum quantum yield 7. Two phenolic derivatives from Jungermannia
of photo-system II (Fv/Fm) and the level of cordifolia which absorb UV radiation have
UV-absorbing compounds seem to be the shown their ability to increase in response to
most responsive ones to enhanced UV-B. a field spatial gradient of UV-B. The future
However, no variable responds in the same combination of laboratory and field works
manner in every species, which still limits studying the behaviour of these compounds
our global comprehension on the effects of under different UV treatments, and particu-
UV-B on bryophytes. The positive thing here larly the field assessment of their seasonal
is that a “UV-B syndrome” may be identified and inter-annual variations in response to
by the treatment of physiological data of con- temporal changes in ambient UV-B, could
trol and UV-B-exposed samples through mul- allow for the development of a protocol of
tivariant analyses (such as PCA), since both bio-indication of the potential increase in UV-
types of samples usually appear clearly sepa- B radiation due to ozone depletion.
rated in the generated plots.
5. The noteworthy variability of the results
reported in the literature on the effects of UV ACKNOWLEDGEMENTS
radiation on bryophytes may be due to the
above-mentioned diversity of species, envi- We are grateful to the Ministerio de Educación
ronmental factors, variables and experimental y Ciencia of Spain and the Fondo Europeo de
conditions used in the different studies. Thus, Desarrollo Regional (FEDER), and to the
it is necessary to take into account the metho- Government of La Rioja (Consejería de
dological approaches to appropriately inter- Educación, Cultura, Juventud y Deportes), for
pret the results obtained. their financial support through the Projects
Limnetica 25(1-2)01 12/6/06 13:54 Página 90

90 Martínez-Abaigar et al.

REN2002-03438/CLI, CGL2005-02663/BOS R. M. LEBLANC, A. STEINMAN & A. SUREN.

and ACPI 2003/06. Saúl Otero and María 1999. Roles of bryophytes in stream ecosystems.
Arróniz-Crespo benefited from grants of the J. N. Am. Benthol. Soc., 18: 151-184.
CALDWELL, M. M. 1971. Solar UV irradiation and
Spanish Ministerio de Educación y Ciencia.
the growth and development of higher plants. In:
Photophysiology: current topics in photobiology
and photochemistry, Vol. 6. A.C. Giese (ed.): 131-
REFERENCES 177. Academic Press, New York.
AH-PENG, C. & C. RAUSCH DE TRAUBEN- CALDWELL, M. M., L. O. BJÖRN, J. F. BORN-
BERG. 2004. Bryophytes aquatiques bioaccumu- MAN, S. D. FLINT, G. KULANDAIVELU, A. H.
lateurs de polluants et indicateurs écophysiologi- TERAMURA & M. TEVINI. 1998. Effects of
ques de stress: synthèse bibliographique. Cryptog. increased solar ultraviolet radiation on terrestrial
Bryol., 25: 205-248. ecosystems. J. Photochem. Photobiol. B: Biol.,
ALLEN, D. J., S. NOGUÉS & N. R. BAKER. 1998. 46: 40-52.
Ozone depletion and increased UV-B radiation: is CONDE-ÁLVAREZ, R. M., E. PÉREZ-RODRÍ-
there a real threat to photosynthesis? J. Exp. Bot., GUEZ, M. ALTAMIRANO, J. M. NIETO, R.
49: 1775-1788. ABDALA, F. L. FIGUEROA & A. FLORES-
ARRÓNIZ-CRESPO, M., E. NÚÑEZ-OLIVERA, J. MOYA. 2002. Photosynthetic performance and pig-
MARTÍNEZ-ABAIGAR & R. TOMÁS. 2004. A ment content in the aquatic liverwort Riella heli-
survey of the distribution of UV-absorbing com- cophylla under natural solar irradiance and solar
pounds in aquatic bryophytes from a mountain irradiance without ultraviolet light. Aquat. Bot., 73:
stream. Bryologist, 107: 202-208. 47-61.
ARRÓNIZ-CRESPO, M. 2005. Efectos de la radia- CSINTALAN, Z., Z. TUBA, Z. TAKÁCS & E. LAI-
ción ultravioleta-B sobre briófitos acuáticos de TAT. 2001. Responses of nine bryophyte and one
ríos de montaña. Tesis Doctoral, Universidad de lichen species from different microhabitats to eleva-
La Rioja. 226 pp. ted UV-B radiation. Photosynthetica, 39: 317-320.
BALLARÉ, C. L., M. C. ROUSSEAUX, P. S. SEAR- DAY, T. A. & P. J. NEALE. 2002. Effects of UV-B
LES, J. G. ZALLER, C. V. GIORDANO, T. M. radiation on terrestrial and aquatic primary produ-
ROBSON, M. M. CALDWELL, O. E. SALA & A. cers. Ann. Rev. Ecol. Syst., 33: 371-396.
L. SCOPEL. 2001. Impacts of solar ultraviolet-B FIGUEROA, F. L. & I. GÓMEZ. 2001.
radiation on terrestrial ecosystems of Tierra del Photosynthetic acclimation to solar UV radiation
Fuego (Southern Argentina). An overview of of marine red algae from the warm-temperate
recent progress. J. Photochem. Photobiol. B: coast of south Spain: a review. J. Appl. Phycol.,
Biol., 62: 67-77. 13: 235-248.
BARSIG, M., K. SCHNEIDER & C. GEHRKE. FISCUS, E. L. & F. L. BOOKER. 1995. Is increased
1998. Effects of UV-B radiation on fine structure, UV-B a threat to crop photosynthesis and produc-
carbohydrates, and pigments in Polytrichum com- tivity? Photosynth. Res., 43: 81-92.
mune. Bryologist, 101: 357-365. GEHRKE, C., U. JOHANSON, D. GWYNN-
BJÖRN, L. O., T. V. CALLAGHAN, C. GEHRKE, U. JONES, L. O. BJÖRN, T. V. CALLAGHAN & J.
JOHANSON, M. SONESSON & D. GWYNN- A. LEE. 1996. Effects of enhanced ultraviolet-B
JONES. 1998. The problem of ozone depletion in radiation on terrestrial subarctic ecosystems and
northern Europe. Ambio, 27: 275-279. implications for interactions with increased
BJÖRN, L. O. 1999. Ultraviolet-B radiation, the atmospheric CO2. Ecol. Bull., 45: 192-203.
ozone layer and ozone depletion. In: Stratospheric GEHRKE, C. 1998. Effects of enhanced UV-B radia-
ozone depletion: the effects of enhanced UV-B tion on production related properties of a
radiation on terrestrial ecosystems. J. Rozema Sphagnum fuscum dominated subarctic bog.
(ed.): 21-37. Backhuys Publishers, Leiden. Funct. Ecol., 12: 940-947.
BOWDEN, W. B., D. ARSCOTT, D. PAPPATHANA- GEHRKE, C. 1999. Impacts of enhanced ultraviolet-
SI, J. FINLAY, J. M. GLIME, J. LACROIX, C. L. B radiation on mosses in a subarctic heath ecosys-
LIAO, A. HERSHEY, T. LAMPELLA, B. PETER- tem. Ecology, 80: 1844-1851.
SON, W. WOLLHEIM, K. SLAVIK, B. SHE- HÄDER, D. P., H. D. KUMAR, R. C. SMITH & R.
LLEY, M. B. CHESTERTON, J. A. LACHANCE, C. WORREST. 2003. Aquatic ecosystems: effects
Limnetica 25(1-2)01 12/6/06 13:54 Página 91

Ultraviolet radiation and aquatic bryophytes 91

of solar ultraviolet radiation and interactions with effects of enhanced UV-B radiation on a subarctic
other climatic change factors. Photochem. heath ecosystem. Ambio, 24: 106-111.
Photobiol. Sci., 2: 39-50. KELLY, D. J., M. L. BOTHWELL & D. W. SCHIN-
HELBLING, E. W. & H. E. ZAGARESE (eds.). DLER. 2003. Effects of solar ultraviolet radiation
2003. UV effects in aquatic organisms and ecosys- on stream benthic communities: an intersite com-
tems. Oxford: Royal Society of Chemistry. 575 parison. Ecology, 84: 2724-2740.
pp. LAURION, I., M. VENTURA, J. CATALÁN, R.
HUISKES, A. H. L., D. LUD, T. C. W. MOERDIJK- PSENNER & R. SOMMARUGA. 2000. Atte-
POORTVLIET & J. ROZEMA. 1999. Impact of nuation of ultraviolet radiation in mountain lakes:
UV-B radiation on Antarctic terrestrial vegetation. Factors controlling the among- and within-lake
In: Stratospheric ozone depletion: the effects of variability. Limnol. Oceanogr., 45: 1274-1288.
enhanced UV-B radiation on terrestrial ecosys- LEWIS SMITH, R. I. 1999. Biological and environ-
tems. J. Rozema (ed.): 313-337. Backhuys mental characteristics of three cosmopolitan mos-
Publishers, Leiden. ses dominant in continental Antarctica. J. Veg.
HUISKES, A. H. L., D. LUD & T. C. W. MOER- Sci., 10: 231-242.
DIJK-POORTVLIET. 2001. Field research on the LOVELOCK, C. E. & S. A. ROBINSON. 2002.
effects of UV-B filters on terrestrial Antarctic Surface reflectance properties of Antarctic moss
vegetation. Plant Ecol., 154: 77-86. and their relationship to plant species, pigment
HUOVINEN, P. S. & C. R. GOLDMAN. 2000. composition and photosynthetic function. Plant
Inhibition of phytoplankton production by UV-B Cell Environ., 25: 1239-1250.
radiation in clear subalpine Lake Tahoe, LUD, D., T. C. W. MOERDIJK, W. H. VAN DE
California-Nevada. Verh. Internat. Verein. POLL, A. G. J. BUMA & A. H. L. HUISKES.
Limnol., 27: 157-160. 2002. DNA damage and photosynthesis in
HUTTUNEN, S., H. KINNUNEN & K. LAAKSO. Antarctic and Arctic Sanionia uncinata (Hedw.)
1998. Impact of increased UV-B on plant ecosys- Loeske under ambient and enhanced levels of UV-
tems. Chemosphere, 36: 829-833. B radiation. Plant Cell Environ., 25: 1579-1589.
HUTTUNEN, S., N. M. LAPPALAINEN & J. LUD, D., M. SCHLENSOG, B. SCHROETER & A.
TURUNEN. 2005a. UV-absorbing compounds in H. L. HUISKES. 2003. The influence of UV-B
subarctic herbarium bryophytes. Environ. Pollut., radiation on light-dependent photosynthetic per-
133: 303-314. formance in Sanionia uncinata (Hedw.) Loeske in
HUTTUNEN, S., T. TAIPALE, N. M. LAPPALAI- Antarctica. Polar Biol., 26: 225-232.
NEN, E. KUBIN, K. LAKKALA & J. KAURO- MARKHAM, K. R., A. FRANKE, D. R. GIVEN &
LA. 2005b. Environmental specimen bank sam- P. BROWNSEY. 1990. Historical Antarctic ozone
ples of Pleurozium schreberi and Hylocomium level trends from herbarium specimen flavonoids.
splendens as indicators of the radiation environ- Bull. Liaison Groupe Polyphenols, 15: 230-235.
ment at the surface. Environ. Pollut., 133: 315- MARKHAM, K. R., K. G. RYAN, S. J. BLOOR & K.
326. A. MITCHELL. 1998. An increase in the luteo-
IHLE, C. & H. LAASCH. 1996. Inhibition of pho- lin:apigenin ratio in Marchantia polymorpha on
tosystem II by UV-B radiation and the conditions UV-B enhancement. Phytochemistry, 48: 791-794.
for recovery in the liverwort Conocephalum coni- MARTÍNEZ-ABAIGAR, J., E. NÚÑEZ-OLIVERA,
cum Dum. Bot. Acta, 109: 199-205. N. BEAUCOURT, M. A. GARCÍA-ÁLVARO, R.
IHLE, C. 1997. Degradation and release from the TOMÁS & M. ARRÓNIZ. 2003a. Different
thylakoid membrane of Photosystem II subunits physiological responses of two aquatic bryophytes
after UV-B irradiation of the liverwort to enhanced ultraviolet-B radiation. J. Bryol., 25:
Conocephalum conicum. Photosynth. Res., 54: 17-30.
73-78. MARTÍNEZ-ABAIGAR, J., E. NÚÑEZ-OLIVERA,
JANSEN, M. A. K., V. GABA & B. M. GREEN- R. TOMÁS, N. BEAUCOURT, M. A. GARCÍA-
BERG. 1998. Higher plants and UV-B radiation: ÁLVARO & M. ARRÓNIZ. 2003b. Daños
balancing damage, repair and acclimation. Trends macroscópicos y microscópicos causados por un
Plant Sci., 3: 131-135. aumento de la radiación ultravioleta-B en dos
JOHANSON, U., C. GEHRKE, L. O. BJÖRN, T. V. briófitos acuáticos del Parque Natural de Sierra
CALLAGHAN & M. SONESSON. 1995. The Cebollera (La Rioja). Zubía, 21: 29-49.
Limnetica 25(1-2)01 12/6/06 13:54 Página 92

92 Martínez-Abaigar et al.

MCKENZIE, R. L., L. O. BJÖRN, A. BAIS & M. Effects of global change on a sub-Arctic heath:
ILYASD. 2003. Changes in biologically active effects of enhanced UV-B radiation and increased
ultraviolet radiation reaching the Earth’s surface. summer precipitation. J. Ecol., 89: 256-267.
Photochem. Photobiol. Sci., 2: 5-15. POST, A. & M. VESK. 1992. Photosynthesis, pig-
MONTIEL, P., A. SMITH & D. KEILLER. 1999. ments, and chloroplast ultrastructure of an
Photosynthetic responses of selected Antarctic Antarctic liverwort from sun-exposed and shaded
plants to solar radiation in the southern maritime sites. Can. J. Bot., 70: 2259-2264.
Antarctic. Polar Res., 18: 229-235. PRASAD, S. M., R. DWIVEDI, M. ZEESHAN & R.
NEWSHAM, K. K., D. A. HODGSON, A. W. A. SINGH. 2004. UV-B and cadmium induced chan-
MURRAY, H. J. PEAT & R. I. LEWIS SMITH. ges in pigments, photosynthetic electron transport
2002. Response of two Antarctic bryophytes to activity, antioxidant levels and antioxidative enzy-
stratospheric ozone depletion. Global Change me activities of Riccia sp. Acta Physiol. Plant.,
Biol., 8: 972-983. 26: 423-430.
NEWSHAM, K. K. 2003. UV-B radiation arising RADER, R. B. & T. A. BELISH. 1997a. Short-term
from stratospheric ozone depletion influences the effects of ambient and enhanced UV-B on moss
pigmentation of the Antarctic moss Andreaea (Fontinalis neomexicana) in a mountain stream. J.
regularis. Oecologia, 135: 327-331. Freshw. Ecol., 12: 395-403.
NEWSHAM, K. K., P. GEISSLER, M. NICOLSON, RADER, R. B. & T. A. BELISH. 1997b. Effects of
H. J. PEAT & R. I. LEWIS-SMITH. 2005. ambient and enhanced UV-B radiation on periphy-
Sequential reduction of UV-B radiation in the ton in a mountain stream. J. Freshw. Ecol., 12:
field alters the pigmentation of an Antarctic leafy 615-628.
liverwort. Environ. Exp. Bot., 54: 22-32. RAE, R., D. HANELT & I. HAWES. 2001.
NIEMI, R., P. J. MARTIKAINEN, J. SILVOLA, A. Sensitivity of freshwater macrophytes to UV
WULFF, S. TURTOLA & T. HOLOPAINEN. radiation: relationship to depth zonation in an oli-
2002a. Elevated UV-B radiation alters fluxes of gotrophic New Zealand lake. Mar. Freshw. Res.,
methane and carbon dioxide in peatland micro- 52: 1023-1032.
cosms. Global Change Biol., 8: 361-371. ROBINSON, S. A., J. D. TURNBULL & C. E.
NIEMI, R., P. J. MARTIKAINEN, J. SILVOLA, E. LOVELOCK. 2005. Impact of changes in natural
SONNINEN, A. WULFF & T. HOLOPAINEN. ultraviolet radiation on pigment composition,
2002b. Responses of two Sphagnum moss species physiological and morphological characteristics
and Eriophorum vaginatum to enhanced UV-B in of the Antarctic moss, Grimmia antarctici. Global
a summer of low UV intensity. New Phytol., 156: Change Biol., 11: 476-489.
509-515. ROBSON, T. M., V. A. PANCOTTO, S. D. FLINT, C.
NÚÑEZ-OLIVERA, E., A. GARCÍA-ÁLVARO, N. L. BALLARÉ, O. E. SALA, A. L. SCOPEL & M.
BEAUCOURT & J. MARTÍNEZ-ABAIGAR. M. CALDWELL. 2003. Six years of solar UV-B
2001. Changes in element concentrations in aqua- manipulations affect growth of Sphagnum and
tic bryophytes over an annual cycle. Arch. vascular plants in a Tierra del Fuego peatland.
Hydrobiol., 152: 253-277. New Phytol., 160: 379-389.
NÚÑEZ-OLIVERA, E., J. MARTÍNEZ-ABAIGAR, ROBSON, T. M., V. A. PANCOTTO, C. L.
R. TOMÁS, N. BEAUCOURT & M. ARRÓNIZ- BALLARÉ, O. E. SALA, A. L. SCOPEL & M. M.
CRESPO. 2004. Influence of temperature on the CALDWELL. 2004. Reduction of solar UV-B
effects of artificially enhanced UV-B radiation on mediates changes in the Sphagnum capitulum
aquatic bryophytes under laboratory conditions. microenvironment and the peatland microfungal
Photosynthetica, 42: 201-212. community. Oecologia, 140: 480-490.
NÚÑEZ-OLIVERA, E., M. ARRÓNIZ-CRESPO, J. ROUSSEAUX, M. C., S. D. FLINT, P. S. SEARLES
MARTÍNEZ-ABAIGAR, R. TOMÁS & N. & M. M. CALDWELL. 2004. Plant responses to
BEAUCOURT. 2005. Assessing the UV-B toleran- current solar ultraviolet-B radiation and to supple-
ce of sun and shade samples of two aquatic mented solar ultraviolet-B radiation simulating
bryophytes using short-term tests. Bryologist, ozone depletion: An experimental comparison.
108: 435-448. Photochem. Photobiol., 80: 224-230.
PHOENIX, G. K., D. GWYNN-JONES, T. V. ROZEMA, J., L. O. BJÖRN, J. F. BORNMAN, A.
CALLAGHAN, D. SLEEP & J. A. LEE. 2001. GABERSCIK, D. P. HÄDER, T. TROST, M.
Limnetica 25(1-2)01 12/6/06 13:54 Página 93

Ultraviolet radiation and aquatic bryophytes 93

GERM, M. KLISCH, A. GRÖNIGER, R. P. SONESSON, M., T. V. CALLAGHAN & B. A.

SINHA, M. LEBERT, Y. Y. HE, R. BUFFONI- CARLSSON. 1996. Effects of enhanced ultravio-
HALL, N. V. J. DE BAKKER, J. VAN DE STAAIJ let radiation and carbon dioxide concentration on
& B. B. MEIJKAMP. 2002. The role of UV-B the moss Hylocomium splendens. Global Change
radiation in aquatic and terrestrial ecosystems - an Biol., 2: 67-73.
experimental and functional analysis of the evolu- SONESSON, M., B. A. CARLSSON, T. V.
tion of UV-absorbing compounds. J. Photochem. CALLAGHAN, S. HALLING, L. O. BJÖRN, M.
Photobiol. B: Biol., 66: 2-12. BERTGREN & U. JOHANSON. 2002. Growth of
SCHIPPERGES, B. & C. GEHRKE. 1996. two peat-forming mosses in subarctic mires: spe-
Photosynthetic characteristics of subarctic mosses cies interactions and effects of simulated climate
and lichens. Ecol. Bull., 45: 121-126. change. Oikos, 99: 151-160.
SEARLES, P. S., S. D. FLINT, S. B. DÍAZ, M. C. TAIPALE, T. & S. HUTTUNEN. 2002. Moss flavonoids
ROUSSEAUX, C. L. BALLARÉ & M. M. and their ultrastructural localization under enhanced
CALDWELL. 1999. Solar ultraviolet-B radiation UV-B radiation. Polar Record, 38: 211-218.
influence on Sphagnum bog and Carex fen eco- TAKÁCS, Z., Z. CSINTALAN, L. SASS, E. LAI-
systems: first field season findings in Tierra del TAT, I. VASS & Z. TUBA. 1999. UV-B tolerance
Fuego, Argentina. Global Change Biol., 5: 225- of bryophyte species with different degrees of
234. desiccation tolerance. J. Photochem. Photobiol. B:
SEARLES, P. S., S. D. FLINT & M. M. CALD- Biol., 48: 210-215.
WELL. 2001a. A meta-analysis of plant field stu- VANICEK, K., T. FREI, Z. LITYNSKA & A.
dies simulating stratospheric ozone depletion. SCHMALWIESER. 1999. UV-Index for the
Oecologia, 127: 1-10. public. A guide for publication and interpretation
SEARLES, P. S., B. R. KROPP, S. D. FLINT & M. of solar UV Index forecasts for the public prepa-
M. CALDWELL. 2001b. Influence of solar UV-B red by the Working Group 4 of the COST-713
radiation on peatland microbial communities of Action “UV-B Forecasting”. Brussels: European
southern Argentina. New Phytol., 152: 213-221. Union. 40 pp.
SEARLES, P. S., S. D. FLINT, S. B. DÍAZ, M. C. VILLAFAÑE, V.E., M. ANDRADE, V. LAIRANA, F.
ROUSSEAUX, C. L. BALLARÉ & M. M. ZARATTI & E.W. HELBLING. 1999. Inhibition
CALDWELL. 2002. Plant response to solar ultra- of phytoplankton photosynthesis by solar ultravio-
violet-B radiation in a southern South American let radiation: studies in Lake Titicaca, Bolivia.
Sphagnum peatland. J. Ecol., 90: 704-713. Freshwat. Biol., 42: 215-224.