Ecosystems, Evolution, and Ultraviolet Radiation (PDFDrive)

Ecosystems, Evolution, and Ultraviolet Radiation
Springer Science+Business Media, LLC

Charles S. Cockell Andrew R. Blaustein
Editors
Ecosystems, Evolution, and

Ultraviolet Radiation
Springer
Charles S. Cockell Andrew R. Blaustein
British Antarctic Survey Department of Zoology
High Cross Oregon State University
Madingley Road Corvallis, OR 97331-2914
Cambridge CB3 OET USA
UK blaustea@bcc.orst.edu
csco@bas.ac.uk
Library of Congress Cataloging-in-Publication Data

Ecosystems, evolution, and ultraviolet radiation / edited by Charles S. Cockell, Andrew R. Blaustein.
p. cm.
Includes bibliographical references and index.
I. Photobiology. 2. Evolution (Biology). 3. Ultraviolet radiation. 4. Ecology.

I. Cockell, Charles S. II. Blaustein, Andrew R.
QH515 .E28 2001
571.4'56-dc21 00-045037
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© 2001 Springer Science+Business Media New York

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Preface
In 1928, Harry Marshall speculated on the role of ultraviolet radiation in ex-

tinction (Marshall, H.T. 1928. Ultra-violet and extinction. American Naturalist
62: 165-187). He speculated that volcanoes could throw dust into the atmosphere,
blocking out ultraviolet light and causing rickets in animals, which would then
perish. Perhaps a search for an increase in the incidence of rickets manifested in
fossil bones would reveal past episodes of alterations in the ultraviolet environ-
ment. At the time his hypothesis was undoubtedly regarded as bizarre. The pa-
per is rarely to be found referenced in any subsequent discussion on the role of
physical factors in shaping evolution or in any discourse on catastrophism.
The reasons for the disappearance of this quite prescient work into history are
probably twofold. First, at the time little was known about the biological effects
and importance of ultraviolet radiation as a stressor and selection pressure. Mod-
els of atmospheric factors that might influence the surface UV regime were crude.
There was no way to quantitatively constrain the ideas presented and so, it was
probably thought, the idea had little merit beyond speCUlation. Second, the lack
of knowledge on the biological effects of UV radiation meant that the next step--
considering the evolutionary consequences of altered UV radiation regimes-
could hardly be embarked upon with any confidence.
In this volume, we return to the idea of UV radiation, its effects on ecosys-
tems, and the likely evolutionary consequences of changed UV radiation envi-
ronments, past, present, and future. The first two chapters examine the history
of the UV radiation climate of earth and the factors that determine organismal
and ecosystem exposure. Their purpose is to give the reader a physical perspec-
tive on UV radiation and an understanding of the constantly changing UV envi-
ronment to which ecosystems are exposed. Variations in the UV radiation envi-
ronment occur at the local level (such as boundary layer and plant canopy effects)
through to global-scale changes (such as alterations in the column abundance of
UV-B-protecting ozone). UV radiation regimes also vary over temporal scales.
These alterations occur on time scales of seconds (the movement of clouds and
plant canopies) to literally billions of years (gross long-term changes in the com-
position of the Earth's atmosphere).
In the chapters that follow, five specific biological and ecological topics in
photobiology are considered-the effects of UV radiation on amphibians, plants,
v
vi Preface
corals, aquatic microbial ecosystems, and, finally, Antarctic ecosystems that are
exposed to the anthropogenic ally generated ozone "hole." These chapters con-
sider UV radiation effects at a diversity of levels from the biochemical to the
community. Their purpose is to provide the reader with our current understand-
ing of the ecological effects of UV radiation, and the areas in which questions
still remain, and to provide a perspective from which the reader can better un-
derstand questions in evolutionary photobiology. The final chapter investigates
the biological consequences of extraterrestrial ultraviolet fluxes, which are quite
different from those experienced on the Earth.
Our knowledge of the role of UV radiation in shaping ecology and evolu-
tionary change is still in its infancy. In this volume, we bring together a number
of authors with the aim of helping to consolidate a better understanding of this
interesting area of photobiology.
Cambridge, UK CHARLES S. COCKELL

Corvallis, Oregon, USA ANDREW R. BLAUSTEIN
Contents
Preface v
Contributors ix
1 A Photobiological History of Earth 1

CHARLES S. COCKELL
2 Physical Factors Determining Ultraviolet Radiation Flux

into Ecosystems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 36
MARGUERITE A. XENOPOULOS AND DAVID W. SCHINDLER
3 Ultraviolet Radiation and Amphibians . . . . . . . . . . . . . . . . . . . . .. 63

ANDREW R. BLAUSTEIN, LISA K. BELDEN, AUDREY C. HATCH,
LEE B. KATS, PETER D. HOFFMAN, JOHN B. HAYS, ADOLFO MARCO,
DOUGLAS P. CHIVERS, AND JOSEPH M. KrESECKER
4 Ultraviolet Radiation and Plant Ecosystems 80

THOMAS A. DAY
5 Ultraviolet Radiation and Coral Communities ................ 118

DANIEL F. GLEASON
6 Ultraviolet Radiation and Aquatic Microbial Ecosystems ........ 150

DONAT-P. HADER
7 Ultraviolet Radiation and the Antarctic Coastal

Marine Ecosystem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 170
MARIA VERNET AND WENDY KOZLOWSKI
8 Ultraviolet Radiation and Exobiology ...................... 195

CHARLES S. COCKELL
Index 219
vii
Contributors
ANDREW R. BLAUSTEIN THOMAS A. DAY

Department of Zoology Associate Professor
3029 Cordley Hall Department of Plant Biology and
Oregon State University The Photosynthesis Center
Corvallis, OR 97331-2914 Arizona State University
USA Life Sciences E-218
P.O. Box 871601
LISA BELDEN Tempe, AZ 85287-1601
Department of Zoology USA
3029 Cordley Hall
Oregon State University
Corvallis, OR 97331-2914 DANIEL F. GLEASON
USA Department of Biology
Georgia Southern University
DOUGLAS P. CHIVERS P.O. Box 8042
Department of Biology Statesboro, GA 30460-8042
University of Saskatchewan USA
112 Science Place
Saskatoon
Saskatchewan S7N 5E2 DONAT-P. HADER
Canada Institut flir Botanik und Phar-
mazeutische Biologie
CHARLES COCKELL Friedrich-Alexander-U ni versiHit
British Antarctic Survey Staudtstr. 5
High Cross D-91058 Erlangen
Madingley Road Germany
Cambridge CB3 OET
UK
AUDREY HATCH
and
Department of Zoology
MIS 245-3 3029 Cordley Hall
NASA Ames Research Center Oregon State University
Moffett Field, CA 94035-1000 Corvallis, OR 97331-2914
USA USA
ix
x Contributors
JOHN B. HAYS ADOLFO MARCO

Department of Environmental and Estacion Biologica de Dofiana
Molecular Toxicology CSIC
Oregon State University Apartado 1056
Corvallis, OR 97331 Sevilla 41080
USA Spain
PETER D. HOFFMAN DAVID W. SCHINDLER

Department of Environmental and Department Biological Sciences
Molecular Toxicology University of Alberta
Oregon State University Edmonton, Alberta T6G 2E9
Corvallis, OR 97331 Canada
USA
MARIA VERNET
LEE B. KATS Marine Research Division
Natural Science Division Scripps Institution of Oceanography
Pepperdine University La Jolla, CA 92093-0218
Malibu, CA 90263 USA
USA
MARGUERITE A. XENOPOULOS
JOSEPH M. KIESECKER Department Biological Sciences
Department of Biology University of Alberta
Pennsylvania State University Edmonton, Alberta T6G 2E9
208 Mueller Laboratory Canada
University Park, PA 16802
USA
WENDY KOZLOWSKI
Marine Research Division
Scripps Institution of Oceanography
La Jolla, CA 92093-0218
USA
1
A Photobiological History of Earth
CHARLES S. COCKELL
Ultraviolet radiation has been a ubiquitous physical stressor since the origin of
the first microbial ecosystems during the Archean era (3.9-2.5 Ga [billion years]
ago). Although the UV radiation that reaches the surface of the Earth spatially
and temporally depends on many factors (Xenopoulos and Schindler, Chapter 2,
this volume), during the history of life on Earth four distinct periods of photo-
biological history can be recognized (Cockell and Knowland 1999). First, the pe-
riod during which UV radiation influenced chemistry on prebiotic Earth during
the Hadean era (>3.9 Ga ago) dominated by the involvement of UV radiation in
organic complexification as well as the deleterious effects it may have had on
exposed prebiotic molecules. Because this does not involve ecosystems or bio-
logical organisms per se, it is not discussed in detail here, although discussions
on the role of UV radiation on prebiotic Earth can be found elsewhere (Sagan
1973; Kolb, Dworkin and Miller 1994; Cleaves and Miller 1998; Bernstein et al.
1999; Cockell and Knowland 1999).
The second stage involves the role of UV radiation during the Archean era
when it is supposed that the Earth lacked a significant 0 3 (ozone) column and
was therefore exposed to higher fluxes of UV-B (280-320 nm) and UV-C
(200-280 nm) radiation. The third stage is the transition phase. Atmospheric 02
(oxygen) partial pressures and thus 0 3 column abundances rose, and biologically
effective irradiances on the surface of the Earth were reduced. The fourth phase
is the period since this transition that covers the Proterozoic and Phanerozoic (2.5
Ga ago to the present). During this period, life has been protected by the 0 3 col-
umn but subjected to alterations in the UV -B radiation regime as a result of short-
term changes in 0 3 column abundances caused by either natural variations or
stochastic alterations in the astronomical environment.
This chapter discusses what is known about each of these phases.
UV Radiation from the Archean to the

Archean-Proterozoic Transition
The partial pressure of O2 in the present-day atmosphere (~210 millibars [mb])
is an imbalance caused principally by the activity of photosynthetic organisms,
the burial of organic carbon, and the lack of reductants from volcanic outgassing
2 Charles S. Cockell
and oceanic upwelling to mop up the O2 so produced. A diversity of direct ge-

ologic and isotopic evidence from Archean facies suggests that the Archean atmo-
sphere was essentially anoxic. These data include the lack of red beds before 2.0
Ga ago, the deposition of easily oxidizable uraninites in rocks older than 2.3 Ga,
and the concentrations of rare-earth metal ions in Archean sedimentary rocks
that are not enriched, unlike their Phanerozoic counterparts. The increased for-
mation of sulfate deposits at about 2.5 Ga ago and an increase in the niobium!
thorium ratio from about 3 Ga to 2 Ga ago, as well as the disappearance of banded
iron formations formed from reduced iron, further support this picture (e.g., Hol-
land 1984; Walker et al. 1983; Holland and Beukes 1990; Holland 1994; Lowe
1994; Walker and Brimblecombe 1985; Collerson and Kamber 1999).
The reasons for the lack of atmosphere O2 in the Archean are still a point of
discussion. Either a greater flux of reductants, particularly hydrogen, mopped up
O2 being produced by oxygenic photosynthesizers in the earliest period of the
Archean (Margulis, Walker and Rambler 1976; Schopf, Hayes and Walter 1983)
or oxygenic photosynthesis was a later innovation and thus there was limited O2
production in the Archean. Alternatively, oxygenic photosynthesizers did exist
in the Archean, but primary productivity was low (Knoll 1979), which plausibly
could be caused by a lower biomass of autotrophs during a period when anaer-
obic chemoheterotrophs may have dominated the Earth's microbial ecosystems
(Schopf, Hayes and Walter 1983).
Numerous arguments suggesting the presence of oxygenic photosynthesis in
the Archean have been previously presented (Schopf 1994, and discussions
therein). Microbial communities inhabited the Earth as early as 3.5-3.3 Ga ago
(Schopf and Packer 1987) and probably as early as 3.8 Ga ago (Mojzsis et al.
1996). Many of these microfossils, which possess coccoid and filamentous forms,
bear strong morphological similarities with extant cyanobacteria, suggesting that
this phylum may have existed as early as 3.5 Ga ago (Schopf 1994). Of course,
morphological similarities do not necessarily imply physiological similarities
(Schopf 1994). Nevertheless, these Archean organisms apparently existed as in-
tertidal stromatolites. The habitat similarities of these organisms, as well as their
morphological similarities to present-day cyanobacteria, thus suggest that they
may have been oxygenic photosynthesizers (Schopf 1994).
Regardless of the mechanisms underlying the low atmospheric partial pressure
of O2 in the Archean and the arguments on the extent of oxygenic photosynthe-
sis during this time, the photobiological consequences were identical: the early
Earth lacked a significant 0 3 column and as a result it might have been subjected
to much higher biologically effective irradiances than the present-day Earth. Re-
sults using a photochemical model and assumptions about the temperature of
early Earth suggest that, at 3.5 Ga ago, O2 levels were at most ~1 X 10- 4 PAL
(present atmospheric level) and possibly much lower (Kasting 1987). At these
partial pressures, the 0 3 column abundance would have been insufficient to re-
duce biologically effective irradiances by any significant fraction.
The effects of this photobiological environment can best be assessed using
radiative transfer models that allow for the calculation of surface UV fluxes.
1. Photobiological History of Earth 3
Weighting functions can be used to calculate the biological effect of these fluxes.
As we are fairly sure that the basic structure of DNA has not changed since the
Archean, action spectra for DNA damage (Green and Miller 1975) can be use-
ful for evaluating early Archean photobiology. Similar arguments also apply to
photosystem II. The action spectra for isolated spinach chloroplasts (Jones and
Kok 1966) may seem an unlikely analogue for early photosystems, but the ex-
periments specifically examined the effects of UV radiation on photosystem II.
Because PSII is similar in chloroplasts and their nonsymbiotic precursors, the
cyanobacteria, this action spectrum is useful for gathering first-order approxi-
mations.
Once these estimates of UV flux and weighted irradiance are made, then phys-
iological responses of organisms to early environments can be assessed. There
are two approaches to examine the consequences of these calculated fluxes on
early microbial ecosystems. First, modem analogue organisms such as cyanobac-
teria can be used. Because of the diversity of gross morphological similarities
between present-day and Archean-early Proterozoic fossils, (such as the stro-
matolitic matting habitat in which organisms lower in the stratified community
can get the advantage of UV protection from organisms in the upper layers),
these models for coping with UV radiation can be used to understand possible
responses of Archean communities (Pierson, Mitchell and Ruff-Roberts 1993).
The approach reaches a useful limit: This limit is when specific physiological re-
sponses are considered based on modem organisms, such as, for example, the
efficacy of DNA repair processes. Over the past 3.5 billion years, Archean mi-
croorganisms have evolved into mammoths, moths, and astronauts, and so al-
though morphological and habitat characteristics of Archean cyanobacteria may
well be similar to present-day organisms, as alluded to earlier, there is consid-
erable latitude for changes in internal physiological responses and biosynthetic
pathways.
With these uncertainties a second approach is useful-to find the upper limits
of UV tolerances on present-day Earth and to compare these to the radiation en-
vironments suggested for early Earth. If present-day organisms can be demon-
strated to possess adequate physiological responses to those theoretically required
on early Earth, then it is probably an acceptable interpolation to suggest that such
survivorship may have existed on early Earth.
Calculation of UV Radiation on Early Earth

The calculation of UV flux at the surface of the early Earth depends on two prin-
cipal components: the luminosity of the early sun and the composition of the pa-
leoatmosphere. At 3.5 Ga ago when there are unequivocal signs of life in the fos-
sil record, the sun was probably 25% less luminous than it is today (Newman
and Rood 1977; Gough 1981). This difference might correspond to an approxi-
mately 35% lower flux across the UV range of biological interest, based on the
data presented by Zahnle and Walker (1982) for solar fluxes at this time. These
spectra are based on direct observations of young stars. The exact reductions in
UV depend on the degree to which the reduction of solar luminosity was a func-
tion of lower temperature (thus changing the spectral distribution of the radia-
tion) or a smaller radius of the sun Gust changing total output) (Gough 1981).
These discussions have been presented elsewhere, but ultimately the assumptions
that are made tum out to be of little consequence, because the differences in
DNA-weighted irradiances between early Earth and present-day Earth are over-
whelmingly determined by the effect of the lack of 0 3 , not assumptions about
whether the solar luminosity was between 25% and 35% lower.
Early stars often emit considerably more UV radiation at wavelengths below
200 nm (Zahnle and Walker 1982; Canuto et al. 1982, 1983). These T-Tauri stars
have been observed directly, and it is possible that during the formation of the
Earth our own sun was emitting an intensity of UV radiation at these wavelengths
10,000 times greater than today and still 4 times greater 3.5 Ga ago (Canuto et
al. 1982). Because CO2 (carbon dioxide) absorbs wavelengths of UV radiation
below 200 nm, it is unlikely that T-Tauri emissions reached the surface of the
Earth. They may have had significant effects on the chemistry of the paleoat-
mosphere, although calculations suggest that 0 3 production by these emissions
would not be· sufficient to significantly alter surface UV flux, with 0 3 column
abundances being generally less than 1 X 10 16 cm- 2 (Canuto et al. 1982, 1983).
The composition of the Archean atmosphere is not well known, but at 3.5 Ga
ago, atmospheric composition may have been approximately 1 bar CO2 (Kast-
ing 1987), with N2 (nitrogen) partial pressures probably similar to those today
(-0.8 bar). An upper limit of 10 bar CO 2 has been suggested for the very early
Archean (Walker 1986), but this would lead to surface temperatures of about
85°C (Kasting 1987). Investigations of pC0 2 at the Archean-Proterozoic transi-
tion at about 2.7-2.2 Ga suggest values as low as 40 mb (Rye, Kuo and Holland
1995). These latter values are consistent with the lower boundary for CO2 sug-
gested at this time in earlier work (Kasting 1987).
These values can be used to derive the spectral irradiance of UV radiation
reaching the surface of the Earth. The direct UV flux reaching the ground is cal-
culated according to Beer's law, and the diffuse UV flux is calculated according
to a Delta-Eddington approximation. This 8-2 stream method has been described
previously and is a classical approach to calculating UV radiative transfer (Joseph,
Wiscombe and Weinman 1976; Haberle et al. 1993). In Figure 1.1, irradiances
are shown for a zenith angle of 0° (sun overhead) for two atmospheric compo-
sitions (early Archean at 3.5 Ga ago and late Archean at 2.7 Ga ago). Typical
values for a zenith angle of 0° on present-day Earth are shown. All cases assume
clear cloudless skies. Clouds can have an effect on UV flux (Xenopoulos and
Schindler, Chapter 2, this volume). Integrated over time, comparisons between
the photobiological environment of present-day Earth and early Earth could be
strongly influenced by cloudiness. It is unlikely, however, that the planet would
have been 100% cloudy all the time; therefore, the calculations presented here
still provide an upper boundary on instantaneous UV exposure.
10 0
____ Present-day flux
10-1
Extraterrestrial flux -3.5Ga ago
10-2 - - ... - - 1 bar CO 2 atmosphere -3.5 Ga ago
.'
.'
,,
10-3 - - .. - - 40 mb CO 2 atmosphere -3.5 Ga ago
J'
i:" , Sulfur haze
··
10-4
; _ Organic haze, ,=7 (1 bar C02)
10-5 ,
... · I
,-./
(
200 220 240 260 280 300 320 340 360 380 400
Wavelength (nm)
FIGURE 1.1. UV irradiance reaching the surface of the Archean Earth for various atmo-
spheric scenarios described in the text. Data are for a zenith angle of 0°. Two CO 2 par-
tial pressures are provided for 3.5 Ga.
The DNA-weighted irradiances received at the surface of the Earth may be

calculated for these atmospheres. In the high-pC0 2 case (l bar), the value is
54 W/m 2 using a DNA action spectrum normalized to 300 nm. For a pC0 2
of 40 mb, DNA-weighted irradiances increase to approximately 101 W/m 2 .
Table 1.1 shows some selected effective irradiances for various early Earth sce-
narios, and Figure 1.2 shows the action spectra used to calculate these values.
Archean Day Length

Instantaneous exposure was much higher than today, but day length was shorter.
At 3-2.5 Ga ago, day length may have been 14 h (Walker et al. 1983); this is
because the Earth has undergone a tidally induced slowing of its rotation rate
caused by the presence of a moon. If we assume that obliquity was about the
same-and it has been suggested that the Earth's obliquity is moon stabilized
TABLE 1.1. Weighted irradiances for various atmospheric scenarios discussed

in the text.
Atmosphere DNA-weighted irradiance Photosystem inhibition
Present-day value 0.071 17.5
1 bar CO2, 0.8 bar N2 54.1 16.3
(-3.5 Ga ago)
40 mb CO 2, 0.8 bar N2 101 26.3
(-3-2.7 Ga ago)
40 mb CO 2 atmosphere with 3.41 9.54
sulfur haze at 1.5 X 10 17 cm- 2
Organic haze in atmosphere, T = 7 0.034 0.013
DNA damage
- - - . - Photosystem damage
200 220 240 260 280 300 320 340 360 380 400
Wavelength (nm)
FIGURE 1.2. Action spectra for DNA damage and photosystem inhibition described in the
text and used to calculate the Archean biologically effective irradiances described in this
chapter.
(Laskar, 10utel and Robutel 1993)-then although the instantaneous DNA-

weighted irradiance would have been just over three orders of magnitude higher
than today, the daily weighted fluence would have been only 500 times greater
because of shorter day length (Cockell 1999a) at any comparable latitude. This
difference would have had implications for the daily damage that a microorgan-
ism would have had to repair and would have gone some way to offsetting
the lack of an 0 3 column. However, it is clear that the overwhelming influence
is the lack of an 0 3 column, not day length, when comparisons are made to
present-day Earth (see Table 1.1).
The values calculated here are for a worse case scenario. They assume cloud-
less skies without any UV absorbers in the Archean atmosphere other than CO2.
Could other factors have altered surface UV flux?
Atmospheric Absorbers and Effects on

Archean Photobiology
Although we can make quite robust investigations of the effects of changing CO 2
and N2 partial pressures on the UV climate of early Earth, trace quantities of
other compounds could well have had profound consequences for UV exposure.
Kasting et al. (1989) investigated the surface UV effects of a sulfur haze in the
early atmosphere caused by photolytic production of sulfur from S02 (sulfur
dioxide) and H2S (hydrogen sulfide) volcanic outgassing. At high enough tem-
peratures (~45°C), sulfur could have reduced the integrated UV flux by as much
as sevenfold. The photochemical arguments for this scenario are uncertain. It
would have required a CO2 partial pressure exceeding 2 bar, which is contentious.
Figure 1.1 and Table 1.1 show the photobiological consequences of a haze with
a column abundance of ~ 1.5 X 10 17 cm- 2 as they envisaged.
A plausible contaminant in the early Earth atmosphere was a CH4 -generated

hydrocarbon smog, the CH4 (methane) produced by either early methanogens or
nonbiological processes (Sagan and Chyba 1997). This idea is analogous to early
suggestions that an organic aldehyde haze may have provided screening on early
Earth (Sagan 1973). Organic molecules are effective UV absorbers. At an opti-
cal depth of 7 in the UV region, which has been suggested for early Earth (Sagan
and Chyba 1997), DNA-weighted irradiances would have been reduced to ap-
proximately 0.04 W/m2, similar to exposed present-day Earth (see Figure 1.1 and
Table 1.1). Even modest smogs could have provided shielding for early life.
Finally, it has also been argued that appreciable levels of O 2 (0.01-0.02 PAL)
could have existed on early Earth. Numerous geologic, physiological, and bio-
chemical arguments have been presented for this scenario (Towe 1996). These
O2 levels, which could result in 0 3 abundances -4 X 10 18 cm~2, would cause
reductions in biologically effective irradiances by two orders of magnitude, re-
sulting in DNA-weighted irradiances only two- to threefold higher than typical
present-day values. Although not disproven, the geologic and isotopic evidence
alluded to earlier is currently more consistent with an anoxic Archean atmo-
sphere.
Biological Effects of High UV Radiation Flux

Let us assume that such atmospheric absorbers did not exist and that UV expo-
sures were the maximum that radiative transfer calculations suggest. What would
be the effect of these irradiances, and would they really be influential in the bio-
geographic distribution of life, either on land or in the photic zone of aquatic en-
vironments?
The calculations shown here lead to DNA-weighted irradiances two and a half
to three orders of magnitude higher than on present-day Earth, similar to those
presented previously (Garcia-Pichel 1998; Rettberg et al. 1998; Cockell 1998).
Although a radiative transfer model was not used by Cockell (1998), similar or-
der of magnitude differences between early and present-day Earth were calcu-
lated. These differences in biologically effective irradiances have been directly
confirmed in orbital experiments. Rettberg et al. (1998) used the extraterrestrial
spectrum in Earth orbit to calculate loss of viability of Bacillus subtilis. By mea-
suring the change in Coomassie blue staining, which is inversely proportional to
the UV radiation received, they demonstrated that the biologically effective ir-
radiances in Earth orbit were three orders of magnitude higher than on the sur-
face of the Earth. Garcia-Pichel demonstrated DNA-weighted irradiances on early
Earth two orders of magnitude higher using an action spectrum for killing Es-
cherichia coli under anoxia (Garcia-Pichel 1998). The slightly lower value cal-
culated could be because UV fluxes were calculated from the expected reduc-
tions in blackbody flux from the sun, assuming that the reduction in solar
luminosity was caused by a temperature change. These values give slightly lower
UV fluxes than the assumption of 35% reduction in luminosity taken in this chap-
ter. However, the qualitative conclusions in all these works are essentially iden-
tical. They demonstrate that the Archean environment was one in which DNA
damage to exposed phototrophs could have been very substantially higher than
today.
Methods for Coping with UV Flux on Early Earth

Even under the highest UV radiation fluxes that are calculated, many mecha-
nisms could have existed on a microbially dominated Archean Earth to screen
UV radiation effectively. A number of these have been discussed previously, and
some are reviewed here with some new data.
The Oceans
The oceanic water column would have been an effective screen. UV-B radiation
can penetrate to significant depths into the present-day oceans, with 1% of inci-
dent radiation recorded at a depth of 50 meters (m) in some Antarctic waters
(Smith et al. 1992). The penetration of short UV wavelengths into water led orig-
inally to suggestions that impurities such as iron and nitrogenous salts might have
been important for life in the photic zone (Margulis et al. 1976). Although these
substances might have provided additional protection (see following), the water
attenuation coefficients in the UV -C are almost an order of magnitude higher
than those in the UV-B (Smith and Baker 1981). Biologically damaging UV-C
is quite quickly attenuated. Figure 1.3 shows the attenuation of wavelengths be-
tween 200 and 750 nm in the late Archean oceans and present-day oceans (Cock-
ell 2000b). Expressed as a DNA-weighted irradiance (Figure 1.4) at a depth of
approximately 30 m, irradiances could have been similar to the exposed surface
of present-day Earth.
In the early Archean, the presence of upwelled ferrous iron could have pro-
vided additional UV attenuation in the oceans. Holland suggested that ferrous
iron concentrations could have been about 3 ppm (Holland 1984). With ab-
sorbance coefficients almost an order of magnitude higher than ferric iron, fer-
rous iron has been suggested as a potentially important UV screen (Olson and
Pierson 1986; Pierson, Mitchell and Ruff-Roberts 1993; Garcia-Pichel 1998).
However, if oxygenic photosynthesis had existed in the early Archean then this
ferrous iron could have been stripped from the photic zone. Certainly by the late
Archean and early Proterozoic, when the prevalence of banded iron formations
decreases (Lowe 1994; Holland 1994), it is likely that ferrous iron was exhausted
as a screen and that this could have happened before significant rises in atmo-
sphere p02 occurred (Garcia-Pichel 1998).
Other UV absorbers encountered in the present-day oceans were probably not
available. The lack of colonization of land by plants, together with the putatively
smaller area of exposed continental cratons (Veizer 1983), would have meant
fewer humic substances and less allochthonous carbon in the oceanic photic zone,
a 10
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E
.6
Q.)
'-'
<= 0.1
.~
"0
0.01
200 250 300 350 400 450 500 550 600 650 700 750
Wavelength (nm)
b
10
~
E
~
N
E
u; Q.)
0
E
.6
Q.)
'-' 0.1
<=
:0 '"
FIGURE 1.3a,b. Spectral irradiance pen- ~
etrating into (a) the Archean oceans as-
suming a 40 mb COz, 0.8 bar N2 atmo- 0.01 +""'T"-f....."'"".,......,..~~,.....+-.,...~...,
200 250 300 350 400 450 500 550 600 650 700 750
sphere and (b) present-day oceans for a
zenith angle of 0°. Wavelength (nm)
making the waters quite clear except in localized areas of high productivity where
dissolved organic carbon could have come from autochthonous sources, such as
in coastal regions.
Although much of the photic zone of many aquatic environments may have
been clear during the early Archean and almost certainly by the late Archean,
as Figure 1.4 suggests, the photic zone could have been colonized by a low-
diversity, high-UV-resistant biota that could have been numerically abundant
(Cockell 2000a,b). The photic zone of many Archean water bodies could well
have been oligotrophic. However, it is true to say that the surface microlayer,
which today is inhabited by the neuston, would probably have been a particu-
larly extreme environment. Below a 30-m depth, UV radiation would have been
10
- - - Archean Oceans (8=0°)
_ _ _ Archean Oceans (8=60°)
Present·day Oceans (8=0°)

4
.••• ·4· . . . Present-day Oceans (8=60°)
30
40 +-~--'-~-~--r--r--r-~
lE-05 0.0001 0.001 0.01 0.1 10 100 1000
Biologically Effective Irradiance (DNA)Wm-2
FIGURE 104. DNA-weighted irradiance penetrating into the Archean oceans (same atmo-
spheric assumptions as in Figure 1.3 and at () = 0° and () = 60°). The vertical line from
the suiface is the value of present-day DNA-weighted irradiances at () = 0°. It gives an
indication of the depth at which DNA-weighted irradiances would the same as the ex-
posed surface of present-day Earth.
significantly reduced, but PAR would have been one to two orders of magnitude
higher than the light saturation points of many present-day phytoplankton (Kirk
1994). A deep chlorophyll maximum of high photosynthetic productivity could
have existed in the Archean as it does today (Garcia-PicheI1998; Cockell 2000b).
Thus, the stratified oceans that some envisage in the Precambrian (Chamberlain
and Marland 1977) are not prevented from being inhabited by photobiological
considerations.
Intertidal and Terrestrial Habitats

In examining a range of physical and biological screening methods, Cockell
(1998) concluded that there are a wide variety of substrates that can provide re-
duction of DNA-weighted irradiances of more than two orders of magnitude. Un-
der such substrates, Archean organisms could be exposed to DNA-weighted ir-
radiances similar to an exposed organism on present-day Earth. Because we know
a diversity of single-celled organisms exist in exposed habitats today, such as,
for example, the neuston that inhabit the microlayer of the oceans, then it is ap-
parent that survival and growth under even the worst UV estimates for the Archean
is likely to be possible with appropriate strategies. Admittedly, even exposed sin-
gle-celled neuston produce UV-screening compounds. Therefore, the compari-
son between biologically effective irradiances achieved by hiding under sub-
strates and the full exposed value on present-day Earth is not entirely accurate.
However, it suffices in that here we are considering order-of-magnitude reduc-
tions that many of these substrates do provide compared to the full sky exposure.
Terrestrial habitats that would protect against UV radiation include the lithic
habit (under or within rocks). In such substrates, light levels are reduced to ap-
proximately 0.005% of incidence at depths at which some organisms (Nienow,
McKay and Friedman 1998), such as the primitive cyanobacterium Chroococ-
cidiopsis, are still able to photosynthesize. These reductions are sufficient to re-
duce UV irradiances from values experienced on the Archean Earth down to val-
ues well below those in exposed regions today.
Reduced ferrous iron, which would have been upwelled from the deep anoxic
Archean oceans, may also have protected some organisms (Olson and Pierson
1986; Garcia-PicheI1998). As suggested earlier, it could have been stripped from
the water by an oxidized upper layer. Although it would therefore have precip-
itated from the surface layers in the oceans, providing limited UV protection, in
intertidal regions it could have precipitated directly onto intertidal communities
as ferric iron, providing some protection.
Sediments themselves can provide UV protection DNA-weighted irradiances
would be reduced to present-day exposed values within the first few millimeters.
Garcia-Pichel and Bebout found that UV-B was reduced to 1% between 1.25 and
0.23 mm from the surface (Garcia-Pichel and Bebout 1996). In some sediments
such as carbonate sands, UV-B radiation was found to be higher in the very near
surface environment because of light-trapping effects. Nevertheless, it is clear
that sedimentary layers would have been an effective strategy for a microbial
benthos.
Protection of organisms may be enhanced by the matting habit, whereby the
upper layer of dead organisms protects organisms underneath by virtue of their
UV-screening compounds. Margulis et al. (1976) showed that, after 3 days of
continuous exposure to 254-nm radiation, a protected Lyngbya sp. community
was still viable, although cells on the surface were killed after minutes. This mat-
ting habit is well preserved in the Archean fossil record in the form of stroma-
tolitic layering in microbial communities (Walter 1983). Indeed, it is probably
the only UV protection strategy that we can truly support with confidence based
on real fossil record evidence.
Other less commonly distributed strategies could have existed. For example,
even thin layers of elemental sulfur will absorb UV radiation in the UV -C and
UV-B regions (Cockell 1998). Some microbial mats near hot springs become
covered in thin layers of sulfur (Castenholz, Bauld and Jorgensen 1990). It is
plausible that organisms with sufficient sulfur coverings in solfatara fields could
acquire UV protection. Table 1.2 lists a diversity of potential protection mecha-
nisms with their possible locations on early Earth.
Ultraviolet Radiation-Screening Compounds

The disadvantage of many of these substrates is that they also absorb photosyn-
thetically active radiation (PAR). This absorbance is not a concern for organisms
that compete by slow persistent growth, such as some cyanobacteria. However,
for many organisms such as those that inhabit the oceanic photic zone, there may
N TABLE 1.2. A selection of ultraviolet (UV) -screening methods found on present-day earth that may have been relevant on early earth.
UV -screening method Example Comments Location
Physical methods
Iron compounds Many mat-forming organisms Provides specific UV absorption Intertidal habitats and possibly in the photic
(Pierson et al. 1993) zone of the early Archean oceans
Solid NaCI Evaporites/halophiles Specific UV absorption Intertidal evaporates and terrestrial salt pans
(Rothschild 1990)
Sulfur Thermophilic mats and organisms Specific UV absorption Near hydrothermal regions and in solfatara
near hydrothermal regions fields
(Cockell 1998)
Water column Oceanic and freshwater Impurities such as iron or dissolved organics Open oceans; inland lakes and water bodies
communities (Sagan 1973; may have improved attenuation, but
Margulis et al. 1976) significant screening of UVC radiation
even in clear waters
Rock/sand/soillsnow Endolithic communities, desert Many of these physical substrates are nonspecific Intertidal regions and terrestrial habitats as
(particularly with crusts, snow, algae, etc. and will attenuate visible wavelengths, well as inland lakes and water bodies.
impurities )/calcium (Nienow et al. 1988; Garcia- although they have the advantage of generating
carbonate/gypsum Pichel and Belnap 1996) a local microenvironment for the organisms,
(calcium sulfate) particularly in extreme environments
Sediments Benthic habitats (Garcia-Pichel and Attenuation of UV radiation under a Intertidal regions and inland lakes and water
Bebout 1996) millimeter or more of sediment bodies
Organics Any 7T-electron-containing May have been important on prebiotic Earth; Water bodies
chromophore (Sagan 1973; small compounds provide nonspecific UV-C
Cockell 1998) absorption
Biological methods
Matting Many cyanobacterial mats/ Dead or living upper layers protect lower layers; Mainly intertidal and terrestrial cyanobacterial
stromatolitic formations can be specific to UV if upper layers contain communities and associated biota
(Margulis et al. 1976) UV -screening compounds
UV -screening Scytonemin in cyanobacteria, Specific biological screening of UV radiation Specific to organism, not to habitat
compounds mycosporine-like amino acids,
etc. (Garcia-Pichel et al. 1992;
Vincent and Quesada 1994)
Fortuitous production Mycosporine-like amino acids May occur when other physiological processes Same as above
of organics that in response to osmotic effects produce compounds that happen to screen in
screen UV (Oren 1997) the UV
Adapted from Cockell (1998).

1. Photobiological History of Earth l3
have been considerable advantages to be gained by exploiting higher PAR lev-

els, which would have necessarily exposed them to higher UV flux. Selection
pressures must have existed for the evolution of UV -specific screening com-
pounds that allowed transmission of visible light but attenuated UV wavelengths.
This selection pressure would have been intensified, compared to today, by the
higher weighted irradiances. Under these circumstances it is un surprising that the
evolution of UV -screening compounds occurred.
The evolution of UV-screening compounds such as mycosporine-like amino
acids (MAAs), which can screen in the UV-B and UV-A (Karentz et al. 1991;
Garcia-Pichel and Castenholz 1993), as well as scytonemin, a UV-A-screening
compound associated with terrestrial cyanobacteria (Garcia-Pichel, Sherry and
Castenholz 1992), would have led to important versatilities in the colonization
of exposed habitats (Garcia-PicheI1998). Garcia-Pichel provides an elegant syn-
thetic review of the role of these compounds in the evolution of cyanobacteria
(Garcia-Pichel 1998).
As well as direct UV-B damage and UV-A-induced photooxidative stress, or-
ganisms were also exposed to significant fluxes of UV -C radiation. Many com-
pounds might have provided UV -C protection. The cyanobacterial sheath com-
pound scytonemin has an absorbance peak at 250 nm, as well as its UV-A peak
that extends into the UV-B region. Experimental results showed that scytonemin
can absorb UV -C radiation to an extent that is physiologically advantageous to
photosynthetic carbon fixation in Tolypothrix sp. isolated from exposed rock sur-
faces (Adhikary and Sahu 1998) as well as Calothrix and Chroococcidiopsis sp.
(Dillon and Castenholz 1999). However, most organics possess UV-C absorbance
and so they can, without any specific selection pressure, protect against UV-C
radiation (Cockell 1998). For example, plant flavonoids have been shown to pro-
vide significant protection against UV -C-induced photosynthesis inhibition in pea
(Pisum sativum L.) seedlings (Shimazaki, Igarashi and Kondo 1988), despite the
fact that peas did not inhabit Archean Earth. Like scytonemin, flavonoids have
an absorbance peak at approximately 250 nm. It is likely that a diversity of non-
specific organics in the upper layers of microbial mats would absorb UV -C ra-
diation, particularly if the upper layers contain a dead layer of microorganisms
from which organics would be released and subsequently photolytically degraded
into smaller UV -absorbing organics.
Thus, the existing data on UV-screening compounds demonstrate that biolog-
ical protection against the complete UV range from 200 to 400 nm was proba-
bly achieved on early Earth and that, despite the high energy and biological de-
structiveness associated with UV-C radiation, the fact that it was absorbed by
most organics through which it passed probably made it one of the less chal-
lenging regions of the UV spectrum to handle. Higher wavelengths required more
specific evolutionary innovations.
The origin of these UV -screening compounds is uncertain. In analogy to the
way in which flavonoids in plants have been suggested to have evolved at low
concentrations as chemical defenses or compounds involved in chemical com-
munication between plant cells (Stafford 1991), it is likely that many microbial
UV -screening compounds evolved in other roles. Because any stable aromatic
structure is likely to provide UV screening at sufficient concentrations, it is ap-
parent that the fortuitous screening of UV radiation by a compound that provides
a physiologically significant benefit may result in its direct selection for UV
screening. The role of MAAs in osmotic response in cyanobacteria (Oren 1997)
is an example of a dual role for a UV-screening compound and a potential ex-
ample of a physical stressor (desiccation) selecting for compounds that also pro-
vide UV screening.
Furthermore, many of these compounds may have evolved from other UV-
screening and quenching requirements. For example, UV-B-screening MAAs
may have evolved early, later evolving into UV-A screens as oxygenic photo-
synthesis and therefore photooxidative damage became more prevalent (Garcia-
Pichel 1998). The UV-A-screening properties of cyanobacterial scytonemin and
the requirement for O 2 in its biosynthesis demonstrate that it may have evolved
in environments in which O2 was being produced (Garcia-Piche1 1998).
Repair of Damage
Protection, either physical or biological, is never 100% efficient and the repair
of DNA must also have been a key response to UV radiation that did penetrate
the cell. Deinococcus radiodurans is of interest in terms of Archean UV flux. In
analogy to the way in which some hyperthermophiles provide us with an upper
temperature tolerance for life, it provides a convenient upper threshold for UV
resistance. Its impressive levels of recombination repair are thought to result from
desiccation resistance (Mattimore and Battista 1996), not a direct radiation se-
lection pressure, and it is aerobic, which is inconsistent with characteristics ex-
pected of many early Archean organisms. Nevertheless, it provides a useful
benchmark for what is biochemically possible for DNA repair. When the in-
stantaneous dose that the organism is capable of surviving (Gascon et al. 1995)
is weighted to a DNA action spectrum, then it is apparent that it can survive
about half the instantaneous dose associated with the late Archean Earth (Cock-
ell 2000b).
The evidence of repair processes in the deep-branching Archaea that include
photoreactivation (Wood, Ghane and Grogan 1997), recombination repair (Seitz
et al. 1998), and evidence for excision repair (Wood, Ghane and Grogan 1997)
suggest that the major pathways of repair seen in present-day organisms were
developed in the Archean (DiRuggiero et al. 1999). Indeed, photolyase, an en-
zyme inducible at 310-500 nm that is responsible for photoreactivation, has been
suggested to be an early photoreceptor (Walter 1983). Some of these repair pro-
cesses are quite impressive. Thermococcus stetteri, for example, is two to three
times more sensitive to ')I-irradiation than is Deinococcus radiodurans (Kopylov
et al. 1993), but this is still a significant repair capability. In studies specifically
directed at Archean conditions, Pierson, Mitchell and Ruff-Roberts demonstrated
an intrinsic UV tolerance in Chloroflexus aurantiacus, an anoxygenic photo-
heterotroph from the deepest branches of the eubacterial line (Pierson, Mitchell
and Ruff-Roberts 1993). This organism only showed a decline in culture yields
when subjected to a UV exposure 20 fold greater than lethality for E. coli. Pho-
toreactivation of damage caused by 254-nm UV-C radiation was also shown in
the obligate anaerobe Clostridium sporogenes, which was suggested to be a
legacy of pre-Phanerozoic evolution (Rambler and Margulis 1980).
Thus, as well as passive protection, repair must have been an important re-
sponse to early UV radiation levels, just as it is today. A higher UV selection
pressure could well have resulted in more efficient UV repair processes than we
see today, but evidence of this will be difficult to find because more efficient
UV repair mechanisms are not reflected in preserved morphology. However, a
number of present-day organisms do exhibit repair processes that are significant
percentages of those required to contend with the instantaneous weighted irradi-
ances on early Earth. Under a stronger selection pressure, it is clear that UV re-
pair processes could have gone a significant way to coping with worse case es-
timates for UV flux on early Earth.
A further complication in developing a truly detailed knowledge of response
to a putatively higher Archean UV radiation regime is that the trade-off between
protection and repair is quite varied. It depends on the different energetic de-
mands in different organisms and probably in different habitats. In a recent study
it was found that photosynthesis in two quite taxonomically and diverse organ-
isms, the cyanobacterium Lyngbya aestuorii and a green alga, Zygogonium sp.,
was affected by ambient UV-B and UV-A radiation even though these organ-
isms do possess UV-B-screening compounds and, in the case of Lyngbya, UV-
A-screening scytonemin (Cockell and Rothschild 1999). However in the red alga
Cyanidium caldarium, which does not possess UV -screening compounds, pho-
tosynthesis inhibition by UV radiation seemed to be negligible. This may be due
to different nutritional status, but it could also be the result of higher rates of re-
pair in this organism. It is clear, therefore, that taxonomically diverse organisms
in the Archean may have possessed quite different responses to UV radiation and
that generic conclusions, such as "organisms used the matting habit" and "or-
ganisms had better repair processes," although useful in defining broad responses
to UV radiation, are probably too simplistic.
Photosynthesis in the Archean

The effects of Archean UV flux on other physiological responses can also be es-
timated. The action spectrum for photosystem II inhibition shows a markedly
greater involvement of the UV-A region than the action spectrum for thymine
dimer formation in DNA (Jones and Kok 1966). Although UV radiation can af-
fect other parts of the photosynthetic apparatus (for example, the photosynthetic
enzyme, rubisco), the PSII action spectrum is broadly similar to the action spec-
trum for inhibition of photosynthesis in whole organisms (Cullen, Neale and
Lesser 1992) and so is a useful proxy for UV-induced inhibition of photosyn-
thesis in cyanobacteria and similar organisms. The greater UV -A contribution in

its action spectrum corresponds to the greater role of reactive O2 species in pho-
tosystem damage. Because UV-A levels are actually higher today than in the
Archean because of the more luminous sun, this part of the spectrum would have
made a lesser contribution, offsetting some of the effects of greater UV-B and
UV-C flux; this is why (using the action spectra in Figure 1.2) photosystem dam-
age is less great in the Archean compared to DNA damage (Cockell 1998;
Garcia-PicheI1998) (see Table 1.1). This result suggests that for most phototrophs
DNA damage, not mitigation of photosynthesis inhibition, was the overwhelm-
ing selection pressure for UV protection. Some of this damage may have been
offset by the anoxic atmospheric conditions. However, oxygenic photosynthe-
sizers could have been producing O2 in their local microenvironments even if
the atmosphere itself was anoxic, thus contributing to UV -A-induced damage.
These calculations assume that photosystem II is a good proxy for Archean
photosystems, and although this may well be the case for oxygenic cyanobacte-
ria it is apparent that photosystems have undergone considerable change since
the earliest ancestral reaction centers (Blankenship 1992). Little is known about
the UV sensitivities of the reaction centers in Chloroflexus spp. or the green sul-
fur bacteria, and so sensitivities of other early photosynthesizers are difficult
to assess. Some even suggest that photosynthetic reaction centers originated as
UV protection compounds, evolving from a nonspecific energy dissipation sys-
tem into more refined light-capturing antenna proteins (Mulkidjanian and Junge
1997).
Beneficial Effects of High UV Radiation on Archean Earth?

UV radiation is a mutagen and thus can potentially contribute toward the gener-
ation of diversity on which environmental pressures can act to drive the process
of Darwinian evolution. So, what role did UV radiation play in the generation
of biodiversity on early Earth? The longer phylogenetic branch lengths in photic
zone phytoplankton have been speculated to exist because photic zone organisms
are exposed to high UV radiation and thus subject to greater rates of mutation
(Pawlowski et al. 1997). This suggestion, and ideas like it, form the basis of dis-
cussions on whether UV radiation has a role to play in the mode and tempo of
evolution.
Insofar as UV radiation is a mutagen, then it might be expected that a two to
three orders of magnitude higher DNA-weighted irradiance on early Earth would
lead to higher mutation rates. The extact magnitude would depend upon the ef-
ficacy of repair and protection processes and the habitat of organisms, as well as
possible differences in base pair and sequence composition (Lesk 1973). If mu-
tation rates were higher than it might be plausible to suggest that microbial bio-
diversity could have been greater or that the generation of a greater number of
advantageous mutations would have allowed faster adaptation to changing envi-
ronmental conditions. The idea is persuasive and intriguing, but qualitative evi-
dence from the Archean fossil record does not lend strong support. The micro-
bial biodiversity of the Archean is not greater than that of the Proterozoic, al-
though this may be largely a function of lack of preservation of the Archean fos-
sil record (Schopf 1994). Furthermore, cyanobacterial hyperbradytely (the
extreme lack of evolutionary change in a group of organisms) is embodied in the
morphological characteristics and habitat preferences of cyanobacterial stroma-
tolites and microfossils, both modem-day and Archean (Schopf 1994). This ev-
idence suggests that in fact many members of this phylum have not changed
much, rather than being subject to great evolutionary change during the Archean
as a result of UV -induced mutations. Indeed, evolutionary innovation, radiation,
and specialization is a characteristic of the Phanerozoic era rather than the Pre-
cambrian (Schopt, 1996).
As discussed earlier, morphometric data do not necessarily imply similar phys-
iology, and it is plausible that higher rates of mutation may simply increase the
rate of change of physiology without altering morphology. However, evolution-
ary changes and mutations normally, over time, engender morphological changes
as habitat and physiology alter in response to new environmental opportunities
and challenges. The morphologies of Archean microfossils are similar to extant
cyanobacteria, particularly the Oscillatoriaceae and Chroococcaceae. The habi-
tats also appear to be similar (such as stromatolitic formations in intertidal re-
gions). This resemblance might suggest physiological hypobradytely as well,
probably because cyanobacteria are generalists (Schopf 1994).
This evidence that mutation rates were not significantly higher is supported
by two further arguments. First, from an evolutionary perspective, selection pres-
sures must be enormous for effective DNA protection and repair. A single-point
mutation can be lethal in a unicellular organism. Although the percent of muta-
tions that are deleterious in any given organism varies, recent experiments using
transposon insertions into E. coli suggested that 80% of the mutations generated
had a negative effect on fitness (Elena et al. 1998). Under a UV radiation regime
providing a DNA-weighted irradiance three orders of magnitude higher than that
of the present day (and thus a potentially deleterious mutation rate increased by
the same factor), the dominant selection pressure is probably for improved UV
mitigation rather than increased allowance for mutations. Indeed, Drake (1991)
suggested that the nearly uniform rates of mutation among DNA-based microbes
from bacteriophages to fungi, despite the vast differences in genome size, may
be because of the balance between deleterious mutations and the physiological
costs of reducing mutation rates. UV radiation will increase physiological costs
in repair and protection but will also cause more deleterious mutations. These
two balancing forces may generate a slightly different mutation rate under greatly
elevated UV radiation, but it is not necessarily going to be much greater.
Second, so long as mutation rates are sufficient to allow adaptation to new en-
vironmental conditions, then organisms can be competitive. Many environmen-
tal changes occur on the order of days to even millenia in the case of, for ex-
ample, marine regressions and transgressions. These time periods are often orders
of magnitude greater than the doubling time of microorganisms. The doubling
times vary enormously, but in the case of phytoplankton several hours (Reddy
et al. 1993) to a few days (Binder et al. 1996; Nelson and Brzezinski 1997) are
typical. The spontaneous rate of mutation generation in a typical DNA-based mi-
crobe is 0.0033 per DNA replication (Drake 1991). Whether these rates are suf-
ficient to allow adaptation depends on the number of required mutations for any
given adaptation, so quantitative descriptions are difficult. Nevertheless, in the
case of microbes that divide quickly and have large populations, it is not clear
that an elevated UV radiation regimen would necessarily improve rates of adap-
tation, given the concomitant disadvantages of increased chance of deleterious
mutations.
UV radiation has been suggested to have other positive roles in the Archean
biosphere. It has been postulated to be a trigger for the evolution of sex (Mar-
gulis, Walker, and Rambler 1976; Rothschild 1999). The concept is an extension
of sex as an error repair mechanisms (Michod and Long 1995). Recombination
repair, whereby new genetic material may be used to repair UV-damaged DNA,
bears functional similarities to meiotic recombination and insofar as UV radia-
tion causes mutations, sex has been suggested to have been stimulated by the
need to repair UV-induced DNA damage (Rothschild 1999). Elena and Lenski
(1997) provide some evidence that mutations are likely to be antagonistic as much
as they are synergistic. They suggested that sex is not a good way to reduce mu-
tational load. Nevertheless, it is clear that a population will inexorably collect
mutations over time through unfaithful replication of information, the so-called
Muller's ratchet (Andersson and Hughes 1996). Mechanisms that potentially al-
low for an individual to reduce mutational load might be expected to be favored
in some circumstances (Rothschild 1999).
The Archean-Proterozoic Transition

During the early Proterozoic (-2.5-2 Ga ago), O2 partial pressures rose as vol-
canic outgassing of reductants was reduced and ferrous iron was depleted (Kast-
ing 1987). Biological activity and geologic rifting and orogeny (DesMarais et al.
1992) concurrently increased O 2 output. The evidence for this was discussed ear-
lier. At an atmospheric O2 level of about 10- 1 PAL (-2% O 2), a significant 0 3
shield was formed (Kasting and Donahue 1980; Levine, Boughner and Smith
1980; Kasting 1987).
The rise in 0 3 column abundance during the early Proterozoic has attracted a
number of suggestions that link reductions in UV radiation to various major evo-
lutionary advances. These ideas include the colonization of land (Berkner and
Marshall 1965; Kasting and Donahue 1980) and the rise of land plants (Lowry,
Lee and Hebant 1980), as well as the evolution of eukaryotes (Rothschild 1999).
Doubts about the importance of reduced UV radiation in the microbial colo-
nization of land have been expressed previously. Rambler and Margulis (1980)
cited the UV resistance of some anaerobic microorganisms as evidence that suf-
ficient UV response did exist in the Proterozoic to allow for the colonization of
land and that the appearance of the Metazoa was unlikely to be linked to changes
in the UV radiation environment. The theories that have been proposed linking
major evolutionary changes to the postulated change in the UV radiation en-
vironment at the Archean-Proterozoic transition may all suffer from the same
problem-overestimating the true importance of UV radiation as an evolution-
ary selection agent. Here, two of these postulates are briefly discussed.
UV and Eukaryotes
Margulis et al. (1976) argued that the aerobic requirement of eukaryotes suggests
that p02 had risen and thus UV had been reduced at the surface of the Earth well
before the eukaryotes emerged. However, O2 microenvironments might have ex-
isted well before the rise in total p02, and so it is possible to imagine a scenario
whereby eukaryotes could have emerged before reductions in UV radiation. This
concept is supported by the finding of eukaryotic membrane lipids at 2.7 Ga ago
(Brocks et al. 1999). Nevertheless, their general conclusions that the rise of eu-
karyotes was probably not linked to changing UV flux, but rather to the evolu-
tion of other biological components such as stable systems of mitosis-meiosis,
is likely to be correct.
These arguments underpin a salient fact about the Archean that is often for-
gotten: although UV flux may well have been higher on the exposed surface of
Archean Earth, there were still many habitats where UV radiation was greatly
reduced. Such habitats include deep layers in microbial mats, the subsurface of
land, the undersurface of rocks, and deep water. Thus, high UV flux cannot be
invoked as a mechanism for an organism not to evolve.
UV and the Colonization of Land

Recently, some arguments were presented against the idea that the drop in UV
radiation was critical for the colonization of land by plants (Cockell and Know-
land 1999). The most compelling argument is that if cyanobacterial stromatolites
had colonized shallow-water intertidal regions by 3.5 Ga ago then there seems
little constraint to the colonization of the land masses. The innovations associ-
ated with desiccation resistance and nutrient acquisition are likely to have con-
strained extensive ecosystems on the land masses of early Earth (Raven 1993,
1997) and probably more so than UV radiation, both for microbial ecosystems
in the Archean and, ultimately, for plants in the Silurian.
The reduction of UV radiation during the rise in p02 would certainly have al-
leviated much of the UV radiation problem; even modest column abundances of
0 3 would have been biologically significant (Francois and Gerard 1988). Some
of the protection and repair processes that might have been needed in the Archean
could have been relaxed, but a significant role for the reduction in UV flux in
driving the colonization of land is doubtful.
UV Radiation in the Proterozoic and Phanerozoic

Organisms may be exposed to different UV fluxes as a result of latitudinal, al-
tudinal, topographic, and boundary layer effects (see Xenopoulos and Schindler,
Chapter 2, this volume). Throughout the Proterozoic and Phanerozoic, ecosys-
tems have also been exposed to changes in UV flux caused by alterations in the
0 3 column itself. These changes can result from seasonal and longer-term pre-
dictable variations in the column as well as large-scale changes caused by sto-
chastic alterations in the astronomical environment. These changes are important
because they embody a view of the photobiological history of the Proterozoic-
Phanerozoic Earth that is perhaps less "constant" than the generally held view
of an Earth conveniently enshrouded in a protective 0 3 layer. In this part of this
chapter, I consider these changes in more detail and their possible ecosystem
effects.
Seasonal and Daily Changes in Ozone Column Abundances

Since the launch of the TOMS (Total Ozone Monitoring Satellite), knowledge
of the change in 0 3 column abundances has been greatly improved. In Figure
1.5,03 column abundances in Dobson units are provided for four latitudes (0°,
40°, and 80 N and 80 S) from 1990 to 1992. As is apparent from Figure 1.5, the
0 0
0 3 column is subject to natural variations in column abundance (Lean 1997 and

references therein). The annual cycle of variations is partly caused by the ec-
centric (noncircular) nature ofthe Earth's orbit, which has a value of 0.017. Thus,
the UV flux at perihelion (closest approach to the Sun) is approximately 7%
greater than at aphelion. The greater flux of UV radiation at 242 nm (which
causes O2 dissociation) will result in greater 0 3 formation. Also superimposed
is the II-year sunspot cycle and the "quasi-biennial oscillation" caused by
changes of wind direction in the tropical lower stratosphere (Angell and Kor-
shover 1973; Lean 1997). Daily variations also occur because of shifting air
masses.
The effect of such alterations is to subject organisms to a fluctuating UV reg-
imen. For example, the annual variation at 400N in 1990 between the maximum
and minimum value of 0 3 corresponds to a change in DNA-weighted irradiance
of approximately 300%, and the daily variations correspond to approximately
50% changes. These variations are within variations imposed by clouds, move-
ments of tree canopies, and other factors that alter localized UV flux. These
changes must certainly contribute to an intrinsic robustness in the biosphere
against variations in UV flux.
Ozone Column (1990-1992)
600
500
400
U)
:t=
c
:::::>
c 300
oU)
..0
o 200
o
~
100 ~ - I
I
o·
0"
o ~!---,---.---.--~--~r---.-~r-~r---.---.---r---'---'---'---'---'---~~ (Jq
(i'
e:.
~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~
~~~~~~~~~~~#~~~~~~ '"5'
#####~#####~#####~ Q
o
....
D~
FIGURE l.5. Ozone column abundances from the years 1990 to 1992 for 0°,40°, and SOON as well as SooS. The data for SooS are in- ~
complete, but the graph shows the effects of the Antarctic ozone hole on total column abundances at this latitude. The data for the north-
ern hemisphere illustrate the natural variations in the ozone column over time. The data are taken from the TOMS (Total Ozone Moni- N
toring Satellite) data set (1979-1993).
Stochastic "Catastrophic" Changes in Ozone

Column Abundances
Although the 0 3 abundance is principally determined by p02 and solar lumi-
nosity, the reactions are subject to alterations by a range of other molecules such
as NO x (nitrogen oxides) or CI- (chloride) ions. Any natural event that perturbs
the mixing ratios of these species will perturb the 0 3 column abundance with its
subsequent implications for the photobiological environment. These rapid sto-
chastic alterations are superimposed upon regular seasonal and daily variations
in the 0 3 column.
Four natural events can potentially cause large-scale 0 3 depletion: first, as-
teroid and comet impacts; second, volcanic eruptions; third, close cosmic catas-
trophes such as supernovae or neutron star mergers; and fourth, intense solar
flares. All these events share the common evolutionary significance of elevating
UV-B radiation at the surface of the Earth (Cockell 1999b) and so can be con-
sidered as common agents of photobiological change. However, the frequency
of these events as well as their duration is quite different and so their potential
ecological effects might be quite different. The effects are little known. We can
gain some insight from observations on the depletions of more than 50% ob-
served in the Antarctic. However, temperature and climatic conditions in the po-
lar regions vary over geologic time scales, so the effects of 50% or greater de-
pletion on ancient ecosystems must remain speCUlative at best.
These catastrophic mechanisms lack strong direct evidence because few have
occurred with sufficient severity during the time that 0 3 and UV measurements
have been made. However, the energetic characteristics of distant supernovae
have been observed directly, and smaller asteroid and comet impact events on
Earth have been observed. Coupled with modeling data, we can derive quite well
constrained insights into the potential photobiological effects of these events.
Here I discuss what is currently known about the contributions of each of these
types of events to evolutionary photobiology.
Impact Events
Asteroid and comet impacts have been predicted to result in stratospheric 0 3 de-
pletion with a subsequent increase in UV flux (Toon et al. 1997) and thus bio-
log~cally weighted irradiances (Cockell and Blaustein 2000). The large amounts
of NO (nitric oxide) generated by shock heating of the atmosphere would be ex-
pected to deplete the 0 3 column. Even for relatively low energy impacts, the ef-
fects could be substantial. The Tunguska meteor fall of 1908 in Siberia was a
low-energy event. Indeed, it was an airburst without an impact crater being
formed and may have had an energy of about 10 Mt (megatons; equivalent of
TNT). Nevertheless, models predict that northern hemisphere 0 3 depletion could
have been about 35%-45%. If the NO had been distributed zonally between 55°
and 65°N, 0 3 depletion in the first year could have been as high as 85% (Turco
et al. 1982). In the former case, UV-B radiation at the surface of the Earth could
be increased twofold, with important biological consequences (Cockell and

Blaustein 2000).
A number of uncertainties underpin these calculations. For example, the dis-
tribution of 0 3 depleting NO is unknown and depends on atmospheric conditions
at the time of the event. Second, the altitude at which the energy is released will
affect the extent of 0 3 depletion. Stony asteroids release their energy at low al-
titudes «15 krn) depending on energy (Toon et al. 1997), whereas short- and
long-period comets (made of "dirty" ice) break up more easily and release their
energy at higher altitudes and may therefore deliver a greater amount of energy
into the stratosphere (Toon et al. 1997), contributing to 0 3 depletion. Thus, small
comets are potentially more photobiologically damaging than small asteroids.
These types of uncertainties plague any accurate quantitative calculations of the
frequency at which natural impact-induced 0 3 depletion occurs. It is possible that
the Tunguska impactor itself was a stony asteroid (Chyba, Thomas and Zahnle
1993), in which case 0 3 depletion would have been minimal. However, the cal-
culations presented by Turco et al. (1982) can be considered a good proxy for
the effects of a comet.
These events may be quite common. Tunguska-sized objects are expected to
intersect with the Earth every 200 years. If one was to assume that for every three
asteroids there is one comet (Chapman and Morrison 1994), then significant 0 3
depletion could still occur with an average frequency of once every 800 years.
It is plausible that such elevations of UV-B radiation could be a selection pres-
sure for organisms that have UV-B tolerances greater than seasonal and diurnal
maxima (Cockell 1999b). Although there is no evidence for these depletion
events, the longevity of UV -screening compounds (Leavitt et al. 1997) might be
used as a basis for attempting to find evidence of past elevations of UV-B radi-
ation caused by changes in stratospheric 0 3 column abundance.
Larger impact events may generate great quantities of NO. For an impact of
108 Mt, similar to that purported to have contributed to the Cretaceous-Tertiary
(Kff) extinctions, NO may be some lO5_lO6 times greater than the amount es-
timated for a lO-Mt impact. This amount would potentially deplete the 0 3 col-
umn by as much as 85% during impact, causing depletion for a long period of
time afterward. However, dust and smoke loading for large-scale impacts is also
greater. For a Kff -sized impact, it is likely that light would be completely blocked
and would remain well below levels required for photosynthesis for at least 6
months to a year after impact (Pollack et al. 1983). Thus, the initial effects of
0 3 depletion will be mitigated by the stratospheric dust and soot cloud. The dis-
sipation of the dust cloud, coupled with 0 3 recovery, will cause a well-defined
temporal pattern of photobiological damage that is related to the characteristics
of different action spectra (Cockell and Blaustein 2000). We originally termed
this period "ultraviolet spring" because it follows "impact winter." Ultraviolet
spring has also been postulated to follow "nuclear winter" (Birks 1986). Figure
1.6 shows the predicted photobiological damage following a Kff -sized impact.
DNA damage could be increased by -lO times or greater and plant damage by
-5 times. How long 0 3 depletion continues after dust clearance is uncertain be-
a. , x 105
,-___'_1~~___'f~o_nm ____'~~t_..__3~r_·_M___r,OO
,. ,04
80
, x 103 ,
,,
\
60
.c , X 102 ~
..,~ c:
0
:;
..,.,
1 x 10'
~Do 40 Q.
..
.2-
c" , 20
0
~
0
, • '0"
0
1m pad wWJtel
b. I Unweighted UV - 9
~ at surface
4 U
& UV-9 levels without
N' .Ii
E dust cloud
~
~ 3 Go
m II
~ ~
II ~
..iii ,
~ .Ii"
:> I
0
"ii:
0 '"
, x ,04
Time oltor Impact (da,,)
c. 1500
Unweighled UV-9
Erythemal sunburn
---0-- Generalized DNA damage
--<:>--- Generalized plant damage
Phytoplankton ph010synthesis
inhibition
04---~~~~~~~---- __--~
Ix 10 2 1 x 103
TIme after impad (days)
FIGURE 1.6a-c. Ozone depletion and photobiological effects following a Kff-sized comet
or asteroid impact on Earth (-10 8 Mt). (a) Levels of dust loading and ozone depletion
used in the calculations. (b) UVB radiation increases associated with an "ultraviolet spring"
after "impact winter." (c) Associated increases in biologically effective irradiances for
some selected action spectra. (Data taken from Cockell and Blaustein 2000.)
cause it depends on precipitation patterns and how much of the NO is washed

out of the atmosphere along with the dust. It is plausible that the loss of NO may
occur concurrently with the rainout of the dust and thus 03 depletion may not
continue much longer after dust clearing, if at all. If this is the case, then small
impacts may be as photobiologic ally important as large impacts.
Volcanoes
The photobiological effects of volcanoes are very uncertain. Chlorine concen-
trations in magma are poorly constrained (Johnston 1980). Injection of chlorine
into the stratosphere would probably be required for significant volcanic-
induced 0 3 depletion. However, during the history of life on Earth massive
continental-scale eruptions have occurred. The Indian Deccan Traps associated
with the Kff boundary and the Siberian Traps associated with the Permian-
Triassic (P-Tr) boundary are two such examples (see Hallam and Wignall 1997
and discussions therein), although Rampino et al. estimated at least nine major
continental-scale volcanic events during the last 250 Myr (million years)
(Rampino, Self and Stothers 1988). It is plausible that protracted volcanic erup-
tions could cause extended depletions of the 0 3 column over decades or even
centuries, with long-term photobiological perturbations.
Cosmic Events
Supernova explosions are predicted to cause 0 3 depletion as well as possible cli-
matic changes resulting from the Solar System's passage through remnant events
(Kuroda 1977). Their effects are complex. Initially, the ultraviolet pulse emitted
by the collapsing progenitor star is predicted to increase 0 3 column abundance.
Aiken, Chandra and Stecher estimated that 0 3 abundances might increase by 23%
for a supernova at 10 pc (1 pc = 1 parsec = 3.26 light years) and that such an
effect would last for about a month (Aiken, Chandra and Stecher 1980). Thus,
Earth would be subject to an ultraviolet amelioration or an ozone "blanket" as
opposed to an ozone "hole." The biological effects of such a change would be
minimal over such a short time span because fluctuations of this order of mag-
nitude occur as the result of meteorological changes, such as cloud cover, on a
monthly basis. The duration of this effect is probably insignificant compared to
the reductions caused by the subsequent cosmic ray emissions from the collaps-
ing star.
The predictions on extent and duration of cosmic ray emissions vary and are
dependent on the distance of the event. However, the most recent predictions
suggest that a supernova at 10 pc would cause 60% depletion at the poles and
20% at the equator (Crutzen and Bruhl 1996) and possibly as much as 95% de-
pletion (Ellis and Schramm 1995) as a result of NO production in the strato-
sphere. These events may occur within 10 pc every 70-240 Myr (Ellis and
Schramm 1995). The duration of the depletion depends on the energy and type
of event, but original estimates suggested that it could last for about 80-300 years
(Ruderman 1974; Ellis and Schramm 1995). Evidence for supernova explosions
has so far been rather elusive, although lOBe enrichments in the Vostok ice cores
from Antarctica as well as marine cores have been discussed as possible signa-
tures of supernova explosions within 40 pc (Ellis, Fields and Schramm 1996).
Recent investigations of cosmological gamma ray bursts suggest that these too
could cause 0 3 depletion. Neutron star mergers, resulting from the gravitational
collapse of a binary neutron star system, can emit vast quantities of gamma ra-
diation (~10 53_1O 54 ergs). If such an event occurred within 1 kpc of Earth, 0 3
depletions similar to those associated with a supernova explosion occurring within
10 pc are estimated (Thorsett 1995).
Solar Flares
Finally, solar flares will also cause 0 3 depletion (Heath, Krueger and Crutzen
1977). The solar flare event of August 4, 1977, was associated with significant
polar 0 3 depletions as great as 25%. These depletions result from the production
of NO in the stratosphere by solar protons. Similar depletions between 9% and
20% were observed after the solar flares in March 1989 (Stephenson and Scour-
field 1991). Reid, McAfee and Crutzen (1978) have suggested that superflares
could occur that are about 100 times as intense as these recent intense flares and
that these could result in at least 50% 0 3 depletion. Furthermore, if they occurred
concurrently with a geomagnetic reversal, the effect would be to channel solar
protons into lower latitudes, potentially causing ozone depletion that was not lo-
calized to polar regions. The ecological consequences could be quite significant.
Relative Biological Effects of Different Mechanisms

Impact-induced 0 3 depletions are transitory and would last no more than 1-3
years after the event. Solar flares are also transitory and possibly cause 0 3 de-
pletion of perhaps days to months. In this respect, they are quite different from
the effect of human-produced chlorofluorocarbons (CFCs) that are continuously
produced and therefore contribute to a long-term, annually reoccurring 0 3 hole.
Thus, human-induced depletion has the potential to cause longer-term changes
in ecosystem structure. Impact events are more likely to contribute to shorter-
term responses. Temporary damage based on relative UV sensitivities of differ-
ent organisms rather than longer-term changes dependent on interspecies com-
petition under a changed UV regimen are the most likely response. In the case
of large impacts, however, massive ecological rearrangements associated with
other changes in atmospheric chemistry and surface conditions can occur; these
include a period of darkness and cooling (Pollack et al. 1983; Covey et al. 1994)
as well as acid rain production (Prinn and Fegley 1987) and wildfires (Wolbach,
Lewis and Anders 1985). The increases in UV-B radiation may be a minor stress
compared to the biospheric trauma associated with these other environmental
alterations.
The calculations on 0 3 depletion discussed here suggest that some impacts and
supernovae may cause the same magnitude of 0 3 depletion but that supernovae
will cause depletion over a longer period. The ecological consequences are unclear
and speculative, but one would expect that longer-duration events would have an
opportunity to cause subtle ecological changes through differences in species sen-
sitivity. Ellis and Schramm (1995) recognized that in the case of supernovae the
principal concern is the effect of these depletions on primary productivity and hence
higher trophic levels, particularly for the -300-year depletion they estimated.
Trophic-level interactions of UV -B radiation can amplify the effects of UV -B ra-
diation. Exclusion of UV radiation from a benthic diatom population was shown
to increase predation by chironomid larvae and thus reduce algal biomass (Both-
well, Sherbot and Pollock 1994), although primary productivity per unit area un-
der UV exclusion was probably greater. Similarly, plants show interspecies dif-
ferences in responses to UV radiation that may result in changes in interspecies
competition and thus the prevalence of some species in particular habitats (Fox and
Caldwell 1978). These longer-term effects can also plausibly be caused by large-
scale volcanism, although the effects on 0 3 of these events are poorly constrained.
Different species sensitivity to UV radiation among amphibians, plants, soil
microorganisms, coral morphs, and organisms in aquatic ecosystems are dis-
cussed in this book. Although the long-term ecological consequences are specu-
lative, it is clear from the information presented later in this book that quite pro-
found alterations at many trophic levels could potentially occur by increasing the
UV selection pressure.
None of these depletions is likely to cause a mass extinction. Supernova ex-
plosions have been suggested to be the cause of mass extinctions (Ellis and
Schramm 1995), but the 0 3 depletion estimates of Crutzen and Bruhl (1996),
suggesting 60% depletion at the poles for a lO-pc-distant event, do not support
the idea that depletion levels are sufficient. Experimental information on deple-
tions of the order of 60% is scant, but most experiments simulating 50% 0 3 de-
pletion of 50% or less suggest that organisms are adversely affected but may not
be killed. Anchovy larvae were severely affected by a dose equivalent to 50%
depletion, but some survived (Hunter et al. 1979). Some plants show detrimen-
tal morphological changes (stunted growth) under simulated 16%-25% 0 3 de-
pletions, but they are not killed (Teramura, Sullivan and Lydon 1990). A 50%
depletion depresses primary productivity in photic zone Antarctic phytoplankton
populations by about 12% (Smith et al. 1992). Effects on higher trophic levels
might lead to extinctions through altered competition, but large-scale mass ex-
tinctions are an unlikely consequence of UV-B radiation increases.
Insofar as fossil record evidence is concerned, a subtle biostratigraphic turn-
over is probably the most that could be expected from a long-term supernova-
induced 0 3 depletion. Indeed, it has even been suggested that past natural 0 3 de-
pletions might be the cause for the intrinsic robustness to elevated UV -B radiation
in the present-day biosphere resulting from this selection pressure (Cockell
1999b).
100
UVA
10
<;J
E
$:
X
:::J
u:
0.1
4 3 2 o
Time (Ga)
-
100
10 -:
1 -: Polar depletion for

supernova at 10 pc _____,
~ I- _ a - -
~t--1i
Tunguska-sized comet explosion
0.1 -: (Hemisphere depletion)
0.01 I I I
4 3 2 o
Time (Ga)
FIGURE 1.7a,b. The summarized photobiological history of Earth showing putative changes
in UV-C, UV-B, and UV-A at the surface of the Earth over time. Also shown are corre-
sponding changes in DNA-weighted biologically effective irradiances that might be ex-
pected from (a) a supernova explosion at 10 pc and (b) a Tunguska-equivalent comet caus-
ing depletion over a hemisphere.
Conclusion
To humans, the Earth is a photobiologically protected haven encircled by a frag-
ile 0 3 shield that has been perturbed by the activity of industry. This view of the
recent perturbation of the 0 3 column is certainly accurate, but it is clear that the
Earth has been subjected to quite varied UV regimens throughout its history. Fig-
ure 1.7 summarizes this history.
Four distinct phases of photobiological history can be recognized: the Hadean
prebiotic photobiological era, the Archean era (3.9-2.5 Ga ago), during which
UV fluxes were probably much higher than today, the transition into a period
when the 0 3 column existed, and finally the period in which we now live, when
the 0 3 column has been subjected to changes caused by natural seasonal and
daily variations as well as stochastic alterations imposed by the astronomical en-
vironment and the vagaries of human activity.
In the latter phase, natural 0 3 depletion events provide a selection pressure for
the tolerance of UV -B radiation levels well above seasonal and diurnal maxima,
and they possibly generate some intrinsic robustness against human-induced 0 3
depletion. However, none of these natural events threatens the 0 3 layer for the
time periods that human activity has the potential to affect. Regular natural 0 3
depletion throughout geologic time does not suggest that human-induced effects
are without long-term consequence.
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Acknowledgments
I would like to thank David Wynn-Williams of the British Antarctic Survey and
Lisa Belden of Oregon State University for their review of this chapter.
2
Physical Factors Determining
Ultraviolet Radiation Flux
into Ecosystems
MARGUERITE A. XENOPOULOS AND DAVID W. SCHINDLER
The shielding of the Earth from ultraviolet radiation by stratospheric ozone is

but one factor in determining the exposure of organisms in the biosphere to harm-
ful levels of UV radiation (UVR, 280-400 nm). Although depletion of strato-
spheric ozone increases the intensity of UV-B (280-315 nm), many other char-
acteristics of the atmosphere, plant canopy, and water interact to determine the
intensity of all wavelengths of UVR that reach biologically sensitive targets.
Some of these factors are also changing as the result of human-caused stressors
such as climate warming and acid precipitation. All these factors are highly vari-
able in both space and time. We review here some of the most important phys-
ical factors in determining the ultimate exposure of a biological target to UV.
Transmission of Solar UV through the Atmosphere

to the Earth's Surface
Introduction
Solar UV-B flux through the atmosphere is a function of both atmospheric and
geophysical parameters. Atmospheric transmission and radiation intensity depend
on absorption by a variety of gases, of which stratospheric ozone is by far the
most important, as well as scattering by air molecules, particulates, and clouds.
Incoming radiation is subject to absorption, reradiation, scattering, and reflection
by atmospheric constituents. The transparency of the atmosphere and clouds is
a function of height and time, aerosol type, and aerosol content. In addition, each
atmospheric constituent has its own scattering and absorption coefficients, which
vary with wavelength of solar radiation.
The geophysical parameters include solar elevation, latitude (hence seasonal-
ity and the Earth-sun distance), altitude, and plant canopy shape (Figure 2.1).
Natural UVR (ultraviolet radiation) intensity at the Earth's surface changes with
the time of day and can vary greatly. Rapid fluctuations can occur in minutes as
clouds move across the sky and over the course of the day as the elevation of
the sun changes. UVR also varies seasonally, being lower at low sun angles,
36
1/////
....
..........
'8'\\\ .....
= UVB
..... :
......
/". .,'
,,;:-.\.I.,.,.~
Solar
"\Olangle
"I It~\" ~
~
~
~.
§
[
Er
5'
~
o
'<
'"
~
'"
w
FIGURE 2.1. Summary of physical factors affecting transmission of UV-B to the air-land interface. -.I
38 Marguerite A. Xenopoulos and David W. Schindler
although seasonal variations in stratospheric ozone concentration also have

an effect.
Stratospheric Ozone Layer

The stratospheric ozone layer is the gaseous protective layer found between 15
and 35 km above the Earth's surface that paradoxically is formed by an UVR-02
interaction. Increasing concentrations of trace gases such as chlorofluorocarbons
(CFCs), halons, and NO x are emitted by human activity. As these compounds
enter the stratosphere, they lead to enhanced depletion of the ozone layer (first
hypothesized by Molina and Rowland 1974; also see Crutzen and Arnold 1986;
McElroy et al. 1986; Cox and Hayman 1988). CFCs are manufactured chemi-
cals used as coolants in refrigerators and air conditioners and as propellants in
aerosol sprays. Releases of CFCs into the atmosphere have been significantly re-
duced since the ratification of the Montreal Protocol in 1987 (Elkins et al. 1993;
Montzka et al. 1996; Environment Canada 1997). However, CFCs are very sta-
ble chemicals and have life spans of 25-400 years; CFCs already released into
the stratosphere will continue to destroy ozone for several decades (Madronich
et al. 1998). Also, halons have high ozone-depleting potential (10 times greater
than CFCs; Environment Canada 1997) and continue to pose a threat. Halons are
generally used as fire extinguishers and fire retardants.
The most notorious depletion in the ozone layer occurs at polar latitudes, es-
pecially in the Antarctic where the ozone "hole" was first discovered in 1985 by
British scientists (Farman, Gardiner and Shanklin 1985). CFCs are largely re-
leased in the Northern Hemisphere and spread around the globe. However, it is
the extreme cold and unusual polar weather that cause the rapid Antarctic ozone
depletion. Polar stratospheric clouds form during extreme cold weather ( < 190 K).
These clouds provide a site to chemically convert chlorine and bromine particles
(CFCs, halons) into reactive forms (free-radical forms). Once halogens are acti-
vated they contribute to ozone depletion through photochemical reactions (see
Kumar and Hader 1999 for more details). The magnitude of this depletion is
greatest around the austral spring when the polar air is coldest and sunlight be-
comes important. The Antarctic ozone depletion continues to deepen; the last
record low in ozone concentration «90 DU) was established in September 2000,
along with a record high in the surface area of the "hole." Recently, stratospheric
ozone depletion has also been found in the Arctic (Hofmann and Deshler 1991;
Manney et al. 1994; MUller et al. 1997; Rex et al. 1997) where the small scale
and uneven distribution of chemically reactant species plays a far greater role
than in the Antarctic (Edouard et al. 1996). Greenhouse gases also playa role in
increased stratospheric ozone losses. Although greenhouse gases warm the
Earth's surface, they cool the stratosphere (through radiative cooling), acceler-
ating ozone depletion (Shindell, Rind and Lonergan 1998). Climate change may
additionally influence Arctic ozone depletion through changes in the stratospheric
water vapor cycle (Kirk-Davidoff et al. 1999).
2. UV Radiation Flux into Ecosystems 39
Ozone depletion is not only limited to polar regions. Decreases in the stratos-
pheric ozone concentration globally are now measurable. For example, in tem-
perate northern latitudes ozone depletion is estimated to be 4%-7% per decade
(Kerr and McElroy 1993; Madronich et al. 1998). Temperate southern latitudes
are estimated to be losing ozone an average of 6% per decade (Madronich et aI.
1998). No significant decreases in stratospheric ozone have been detected in the
tropics (Madronich 1992; Niu et al. 1992), although average stratospheric ozone
concentration is generally lowest near the equator.
Global measurements of stratospheric ozone concentration have been made
since the late 1970s with the Total Ozone Mapping Spectrometer (TOMS) aboard
various satellites. The variations in stratospheric global ozone depend on the geo-
graphic location and are highly seasonal (Shoeberl, Stolarski and Krueger 1989;
Stolarski, Bloomfield and McPeters 1991; Stolarski et al. 1992; Krueger et al.
1992). The strongest trends are observed during the Antarctic spring (~50%;
Madronich et al. 1998). In the high latitudes of the Northern Hemisphere, the
largest ozone decreases occur during February and March, again following the
movements of the cold polar air. From June to December, southern high-latitude
regions have more negative trends than those in northern high-latitude regions.
A more detailed description of seasonal and monthly trends is presented by Sto-
larski et al. (1992), Madronich (1992), Niu et al. (1992) and WMO (1999). A
1% decrease in total stratospheric ozone can cause about a 2% increase in the
amount of UV-B radiation reaching the Earth's surface if weighted by the DNA
action spectrum (see following), depending on the season and zenith angle of the
sun (UNEP 1989; Herman et al. 1996).
Weighting Functions and Action Spectra

Not all UV wavelengths have the same capacity to cause biological damage or
stimulate photochemical reactions. The biological effectiveness ofUVR increases
geometrically with decreasing wavelength. This phenomenon is best described
by an action spectrum or weighting function (McKinley and Diffey 1987). Ac-
tion spectra describe the changing response of a given process through the UVR
region. The most widely accepted reference action spectra are those for erythema
in human skin or sunburn (UVerythema; McKinley and Diffey 1987), DNA dam-
age (UV DNA ; Setlow 1974), or photoinhibition (UVphot ; Jones and Kok 1966;
Cullen, Neale and Lesser 1992). These action spectra extend throughout the 290-
nm to 400-nm region, but UVerythema and UV DNA are more sensitive to shorter
UV wavelengths whereas UVphot is more affected at longer wavelengths in the
UV-A. It follows that action spectra affected by UV-B will be more sensitive to
stratospheric ozone depletion (Madronich 1992; Roy et al. 1994). For instance,
Frederick and coworkers (Frederick, Zheng and Booth 1998) compared total un-
weighted UV -B, UVerythema, and UV phot to changes in stratospheric ozone. UVphot
was insensitive to changes in ozone amounts, whereas the UVerythema and UV DNA
action spectra were more sensitive to stratospheric ozone fluctuations (also shown
by Roy et al. 1994). Bukata and Jerome (1997) showed that the change in the
UVDNA daily irradiation is considerably greater than the percentage change in
daily UV-B for a given change in stratospheric ozone. For an ozone depletion of
10%, the percent daily change in daily UV-B varied from 7% to 11 %, while the
percent in UV DNA varied from 27% to 30% (Bukata and Jerome 1997).
Clouds
Clouds play an important role in modulating UV-B levels at Earth's surface be-
cause they can lead to large variations in irradiance in time and in space (McKen-
zie, Matthews and Johnston 1991; Gautier et al. 1994; Lubin and Jensen 1995;
Frederick 1997). Thick cloud generally reduces UVR at ground level to about
10%-50% of that of clear skies (Frederick and Steele 1995; Schafer et al. 1996;
Sabziparvar, Shine and Forster 1999). Clouds trap solar radiation by internal scat-
tering so that all wavelengths take a longer effective path through a cloud. The
magnitude of changes in UVR related to cloud depends on several factors such
as cloud type, percent cover, water content, and particle distributions within the
cloud. If the cloud contains high concentrations of ozone, clouds also absorb as
well as scatter radiation (see following); this will likely be the case in industri-
alized regions. It is interesting to note that in some cases scattering from the sides
of the clouds (especially cumulus clouds) can enhance UV-B (Mims and Fred-
erick 1994; Estupifian et al. 1996).
The ratios of UV-B and UV-A to photosynthetically active radiation (PAR)
change within clouds, and higher UV-B:PAR ratios can occur under cloudy skies
(Ilyas 1987; Deckmyn and Impens 1998; Feister 1994; Frederick 1997). On sunny
days in Ontario, Canada, UV-B and UV-A represented 0.6% and 10%, respec-
tively, ofthe total irradiance. On cloudy days, however, even though the absolute
values were lower, UV-B and UV-A were higher proportions of total irradiance
(1 % and 16%, respectively; Lean 1998).
Cloud type also plays an important role in UVR transmission (Tsay and
Stamnes 1992; Lu and Khalil 1996). Tsay and Stamnes (1992) showed that low-
level stratus clouds reduced UV-A and UV-B dose rates by about 60%-75%, de-
pending on the zenith angle and ozone concentration, because strong scattering
and enhanced photon path lengths inside the cloud led to both increased reflec-
tion and enhanced absorption by ozone. In contrast, higher-level cirrus clouds
decreased UV-B only slightly compared to clear skies (Tsay and Stamnes 1992).
Absorption of UVR by Tropospheric Pollutants and Aerosols

Some investigators believe that increasing tropospheric pollutants such as 0 3 ,
S02, and aerosols (small particles suspended in air; e.g., soot, sulfate haze, dust)
will decrease UV-B, counteracting the trends caused by stratospheric ozone de-
pletions (Bri.ihl and Crutzen 1989; Bordewijk et al. 1995; Madronich et al. 1995;
Varotsos et al. 1995; Zerefos et al. 1995; Ma and Guicherit 1997; Papayannis et
al. 1998). Others have found that UV-B may increase under a polluted tropo-
sphere. Following the El Chichon volcanic eruption, which produced an H 2S04
aerosol layer, UV-B flux in the shorter wavelengths increased relative to a clear
sky (Michelangeli et al. 1992; Vogelmann, Ackerman and Turco 1992). The in-
crease in UV-B was caused by aerosol scattering (Michelangeli et al. 1992; Tsi-
tas and Yung 1996), especially for large solar zenith angles (Davies 1993). Also,
the volcanic aerosols injected into the stratosphere may induce ozone thinning
by activating chlorine into forms that catalyze ozone destruction (Vogelmann,
Ackermann and Turco 1992).
Although stratospheric ozone depletion has occurred since the late 1970s, tro-
pospheric pollutants in the Northern Hemisphere have increased twofold or more
over the past 100 years (WMO 1992, 1995). At midlatitudes of the Northern
Hemisphere, UV-B, UVerythema, and UV DNA at the Earth's surface may have in-
creased by 2%-5%, 4%-7%, and 4%-10%, respectively, as the result of strato-
spheric ozone depletion since the late 1970s (Madronich 1992; Madronich et al.
1998). Conversely, in the industrialized and nonurban polluted region by
5%-15% (UV DNA), because of tropospheric pollution during the past 50-100
years (Liu, McKeen and Madronich 1991; Madronich et al. 1998).
The optical properties of tropospheric aerosols vary significantly in space
and time due to the size distributions, optical thickness, and the different prop-
erties of the aerosols, which are wavelength dependent. The effects of the lower
tropospheric aerosols inside and over the planetary boundary layer on solar UV
radiation reaching the ground are complex. Different levels of air pollution and
aerosols will translate into different effects in reducing the UVerythema reach-
ing ground level (Liu, McKeen and Madronich 1991; Varotsos et al. 1995). So-
lar UV measurements in the Athens (Greece) basin revealed a substantial re-
duction of UV-B on days with high pollution levels (Repapis et al. 1998).
Summer UV-B levels in Athens average more than 15% below those at other
regional rural sites (Bais, Zerefos and McElroy 1996). Papayannis et al. (1998)
compared 2 days of low and high air pollution levels, but of the same stratos-
pheric ozone content, and showed a reduction of nearly 30% in the UVerythema
solar irradiance during local noon hours. Such a reduction, occurring during
days with high amounts of pollutants like 0 3 , sulfurs, N0 2, and aerosol parti-
cles, is due to both wavelength-dependent absorption and scattering. Ground
levels 0 3 absorbs UV -B radiation more efficiently than stratospheric ozone;
this is largely because scattering processes diffuse a large fraction of solar ra-
diation, increasing its pathway through the atmosphere (hence a longer path
through tropospheric than through stratospheric ozone) and consequently in-
creasing UVR absorption (Bruhl and Crutzen 1989). The influence of sulfate
aerosols and sulfur dioxide on UV -B radiation has also been addressed in some
studies (Zerefos et al. 1986; Bais et al. 1993; Ma and Guicherit 1997). More
than 90% of the sulfate is the oxidation product of anthropogenically emitted
S02 , which is also the primary contributor of regional acid deposition. Sul-
fate and S02 also absorb strongly in the UV.
42 Marguerite A. Xenopou!os and David W. Schindler
Light extinction by aerosols is highly dependent on the optical thickness of

the boundary layer. When a 25-krn visual range was used in the calculation of
total solar radiation reaching the surface, a decrease of surface solar radiation
of 10% at 310 nm and 8% at 550 nm was seen for a 2-krn boundary layer; for a
l-km boundary layer, this decrease was less: 7% at 310 nm and 6% at 550 nm
(Liu, McKeen and Madronich 1991).
Anthropogenic aerosols and pollutants have the beneficial effect of reducing
UV-B radiation at the surface, although they have known detrimental environ-
mental effects to health, visibility, and acid precipitation. However, aerosol ef-
fects from pollutants on UV-B are expected to be negligible over remote areas.
Although most UV monitoring takes place in developed countries where aero-
sols are more abundant. The largest UV -B increases caused by stratospheric ozone
reduction may actually be occurring at pristine locations where they are not mon-
itored. As a result, effects due to aerosols and other tropospheric pollutants may
make UV monitoring results difficult to interpret for large regions (Liu, Mc-
Keen and Madronich 1991). While anthropogenic sulfur, NO x, and tropospheric
ozone continue to increase in developing countries, North America and parts of
Europe have started to decrease their emissions of SOx, due to concerns for their
environmental effects, but not necessarily their NO x levels (Galloway et al. 1987;
Hedin et al. 1994; Hedin and Likens 1996; Vitousek et al. 1997a,b).
Seasonality and Solar Zenith Angle

As the sun approaches the horizon, the increased path length taken by direct sun-
light through the absorbing atmosphere increases, leading to a decline in UV ir-
radiance to the ground (Figure 2.2). The marked effect of solar altitude is ap-
parent especially in shorter UVR wavelengths (Urbach 1997). This dependence
of ground-level UV irradiance on solar elevation is related to latitude and sea-
son via the changing elevation of the sun and the duration of daylight (Freder-
ick 1997). Annual cycles are particularly pronounced at high latitudes, where the
sun fails to rise above the horizon on days near the winter solstice and 24 h per
day of sunlight occur 6 months later. At temperate latitudes, the accumulated ra-
diation dose is highest in the summer season as the result of long durations of
daylight and high elevations of the sun near local noon.
Suiface Albedo
Another geophysical factor affecting UV flux is surface albedo or reflectivity,
which determines the amount of the incident radiation that is reflected from the
Earth's surface back into the atmosphere. Some of this radiation can be returned
toward Earth's surface, increasing the incident radiation. In general, albedo is
low for the UVR region and increases with increasing wavelength. Albedo val-
ues in the UV for soil fall between 4% and 25%, depending on the type of soil,
1.60
1.40
':' 1.20
E
= 1.00
":'
E
-
S
CD
0.80
'" 0.60
=
~
...
"CI
~ 0.40
0.20 33.5 + cloudy
0.00 .6
300 312 324 336 348 360 372 384 396
Wavelength (nm)
FIGURE 2.2. UV irradiance at different wavelengths and solar angles. Data from the
Experimental Lakes Area (Northwest Ontario, Canada), June 16, 1998, taken using a
LI-COR 1800-UW Spectroradiometer.
surface roughness, and moisture content (Feister and Grewe 1995). Values for
vegetation cover average about 2% and depend on the vegetation type and age.
Water reflectivity is low but depends on the angle of the sun. The albedo of ice
(7%-75%) and snow (20%-95%) is greater but highly variable, depending on
the impurities that they contain, on surface roughness and on the angle of inci-
dence. For instance, dense dry and clean snow has a higher albedo (85%-95%)
than very porous, light-brown snow that is soaked by water (30%). Snow albedo
values can also vary with wavelength. Blumthaler and Ambach (1988) showed
that albedo values for dry new snow were 95% for the erythema dose but only
85% for the total global radiation. As the result of greater extent and duration of
snow and ice cover, high reflections generally occur in colder climates.
Surface reflections affect UV radiation both through direct reflection toward
a target and by enhancing the diffuse downwelling radiation. Beaglehole and
Carter (1992) showed that in the Antarctic the strongest skylight intensity was
for light reflected from extraterrestrial direction as the result of simple scatter-
ing in the atmosphere induced by the high snow albedo. Madronich (1993) and
Blumthaler (1993) have reviewed other measurements of surface reflectivity in
the UV range.
Plant Canopy Shape and the Influences on UV Exposures

to the Canopy
UVR reaching plant canopies is absorbed, reflected, and transmitted by vegeta-
tion. This effect produces considerable variation in UV flux, in space, time, and
spectrum in terrestrial ecosystems. Unfortunately, measurements of UVR at the
top of the canopy cannot be scaled to produce the exposure to a particular canopy
or plant part (Brown, Parker and Posner 1994; Parisi, Wong and Galea 1996).
Once the solar irradiance reaches the canopy, leaf interception and reflection and
consequent irradiance changes occur (Parisi, Wong and Randall 1998). Several
factors can influence the penetration of light through a canopy and modify the
radiation environment; these are solar elevation, the optical properties of plants
and soils, leaf area and angles, orientation, shading by adjacent plants, inclina-
tions, spectral albedo, and the degree of reflected and transmitted radiation from
foliage. In all cases, the proportion of direct and diffuse light can also greatly in-
fluence the UV -B: UV -A:P AR ratios and the UV -B irradiance reaching the leaves
at the top and the bottom of a canopy.
Taking into account plant canopy shape, a dosimetric technique was devel-
oped by Parisi and coworkers (Parisi and Wong 1994, 1996; Parisi, Wong and
Galea 1996; Parisi, Wong and Randall 1998) to compare ambient UVR exposure
to that going through canopies. Comparison of hemispherical, conical, and
pinnacle-shaped canopies demonstrates that UV exposures under the canopies
were reduced by 40%, 65%, and 83%, respectively, compared to above the canopy
(Parisi and Wong 1994). Also, for the same canopy shape, the ratio UV-B:UV-A
changed with the sun angle. The variation throughout the day was attributed to
variations in the solar zenith angle, changes in cloud cover, and other transmis-
sion properties in the atmosphere.
The ratio of UV-B to PAR also changes with canopy and leaf inclination
(because of the higher proportion of diffuse light) (Brown, Parker and Posner
1994; Deckmyn and Impens 1998). Below-canopy measurements of the UV
environment have been made under a variety of plant canopies (Lee and
Downum 1991; Grant 1991; Yang, Miller and Montgomery 1993; Brown, Parker
and Posner 1994; Grant et al. 1995). In low-density canopies and gaps of var-
ious temperate and tropical forests, UV-B is attenuated less than PAR. In con-
trast, PAR is attenuated less than UV-B in fully leafed temperate deciduous
forest canopies (Brown, Parker and Posner 1994; Yang, Miller and Montgomery
1993). Measurements under a Sorghum canopy of leaf area index of 7.0 showed
that PAR was attenuated less than UV-B when the solar zenith angle was small
and more than UV-B when the solar zenith angle was large (Grant et al. 1995).
Grass leaves below the canopy receive light with a higher UV-B:PAR ratio
(Deckmyn and Impens 1998). Grant and Heisler (1996) showed that the
UV-B penetration into the subcanopy of a suburban area differs greatly from
that of PAR. The UV-B irradiance in the shade was twofold greater than ex-
pected. In addition, some plants are more effective in screening out UV-B than
others. With the use of a fiber-optic microprobe, Day, Vogelmann and DeLu-
cia (1992) showed that the foliage of conifers was the most effective at atten-
uating UV-B as opposed to leaves of herbaceous dicots that transmitted the
highest amount of UV-B into their mesophyll. Leaves of woody dicots and
grasses were intermediate between conifers and herbaceous dicots (Day, Vo-
gelmann and DeLucia 1992).
Altitude Effects
Solar radiation, including UV-B, generally, increases with increasing altitude be-
cause it undergoes less scattering and absorption in a thinner atmosphere. At
higher altitudes the effect of tropospheric pollution on UV -B radiation is also
less. In addition, mountain-induced atmospheric gravity waves can cause local
reductions in stratospheric temperature (Carlsaw et al. 1998) and enhance chem-
ical reactions or chlorine activation that cause ozone destruction. This increase
in solar radiation with altitude is called the altitude effect and is usually given
as an increase in irradiance in percent per 1000 m relative to sea level. The mag-
nitude of the altitude effect under a clear sky depends on the wavelength, sun
angle, aerosols, and albedo of the terrain. For instance, at low sun angle the al-
titude effect is stronger than at higher solar elevations (Blumthaler, Ambach and
Ellinger 1997). As a result, the altitude effect is greater in winter (about 20% per
1000 m) than in summer (about 15% per 1000 m; Blumthaler, Ambach and
Ellinger 1997).
The increase in UVR intensity with altitude has been measured at several sites
(Blumthaler and Ambach 1990; Ambach, B1umtha1er and Wendler 1991;
Dirmhim, Sreedharan and Venugopa1 1993; Blumthaler, Ambach and Ellinger
1997; Blumthaler et al. 1994, 1996). A Florida weather station received less
UV-B than high-elevation stations (Albuquerque, New Mexico; El Paso, Texas)
located at similar altitudes (Scotto et al. 1988), although clouds are also more
important in Florida. A comparison of daily total irradiances between Jungfrau-
joch, Switzerland (3576 m above sea level [a.s.l.]) and Innsbruck, Austria (577
m a.s.l) revealed increases in irradiance with altitude of 8% per 1000 m (total ir-
radiance), 9% per 1000 m (UV-A), and 18% per 1000 m (UVerythema) during the
summer solstice (Blumthaler et al. 1997). Measurements made in Germany
showed that the altitude effect increases steadily from 9% per 1000 m (370 nm)
to 11 % per 1000 m (320 nm) and then more rapidly to 24% per 1000 m (300
nm) (Blumthaler, Ambach and Ellinger 1997).
Because UV-B irradiance increases with elevation above sea level, it was sug-
gested by a number of authors that species growing at higher altitude might be
more UV-B resistant. Some investigators have found that plant species and pop-
ulations originating from naturally high UV-B sites (high altitudes) are a less
sensitive to increased levels of UV-B than species found in low UV-B locations
(Caldwell, Robberecht and Nowak 1982; Larson, Garrison and Carlson 1990;
Sullivan, Teramura and Ziska 1992; Somersalo et al. 1998). However, others
have found little change in sensitivity with increasing UV-B exposure (Van de
Staaij et al. 1995; Rau and Hofmann 1996).
Transmission of Solar UVR Through Water

Introduction
The irradiance at a given depth and wavelength in lakes and oceans depends on
a number of parameters including the angle and intensity of surface irradiance
and the properties of the water column (Figure 2.3) (Hutchinson 1957; Kirk
1994a,b). The depth of the water required to remove 99% of the solar radiation
at 310 nm varies from about 30 m in the clearest and most colorless ocean wa-
ter to a few centimeters in brown humic lakes and rivers. In this section, we con-
sider the factors that affect UVR penetration in waters.
UVR Distribution in the Water

The transmission of UVR through the air-water interface varies with time be-
cause of changes in the distribution of UVR and the effect of surface waves
(Stramski, Booth and Mitchell 1992), which modulate both intensity at a partic-
ular depth and the amount reflected back into the air. Water reflectivity is in-
versely related to solar angle and ranges from 5% when the solar zenith angle is
greater than 30° to more than 60% when the solar altitude is less than 3°. Loss
by reflection is lowest (~2%-3%) during midday when the angle of the sun is
high (Kirk 1994b). Additionally, rough seas have a somewhat lower albedo than
calm seas, although the difference is small (Jerome and Bukata 1998).
The radiance distribution below the water surface is subject to absorption and
scattering by dissolved and particulate matter, the magnitude of which is wave-
length dependent. Pure freshwater or seawater has a high transmission in the
UVR (>87% of surface irradiance at 300 nm; Smith and Baker 1981). Most of
the UV -B photons in natural waters are absorbed by dissolved (gelbstoJf or gilvin)
and particulate organic substances, present in all natural waters, and originating
mainly from the breakdown of terrestrial plant biomass in the soils of the catch-
ments from which the waters are derived.
The concentration of dissolved organic carbon (DOC) compounds and sus-
pended particles primarily influence UVR transmission, leading to large differ-
ences in UV transparency among water bodies. In the euphotic zone, UV-B ra-
diation is much more rapidly attenuated than PAR. Similarly, UV DNA is
attenuated more rapidly than unweighted UV-B (Jerome and Bukata 1998). With
the exception of some high-altitude alpine lakes or high-latitude polar lakes, in-
land waters, because of their higher humic content, attenuate UV-B more in-
tensely than marine waters. However, marine waters can also show large differ-
ences in their optical properties in UVR. The concentrations of dissolved
absorbing substances undergo a drastic change from oceanic to coastal water
types. Jerlov (1950) found that UV-B (310 nm) was reduced by only 14% m- I
in the middle of the Mediterranean Sea but that this reduction increases to more
than 90% m - 1 in a more coastal area. This difference in UV attenuation between
oceanic and coastal stations has also been observed off the central Chilean coast
Drought "
Fires
-
!V
~
~
e:
~.
o
::l
vegetation
characteristics ~
~.
~
o
'<
'"
'"~
3
'"
.j>.
FIGURE 2.3. Summary of factors affecting transmission of UVR to the air-water interface and through the water. -..I
(Montecino and Pizarro 1995) and in the Baltic Sea (Piazena and Hader 1997).
Jerlov (1968) further classified marine waters into several types of coastal and
oceanic waters depending on their transmission (but see Piazena and Hader 1997).
Optical Properties of Natural Water and

UV-Absorbing Substances
The absorption of light by a given molecule occurs when the molecule's elec-
trons resonate at frequencies that correspond to a photon's energy state. DOC
contains chemical structures or chromophores that highly absorb light and is by
far the most important absorber of UVR. The most common DOC classes are
fulvic acids, tannic acids, and lignins, compounds that are composed of aromatic
groups and aliphatic chains in different proportions. The aromatic group absorbs
more light than the aliphatic portion of the DOC.
One of the biggest difficulties today is attempting to chemically classify DOC.
This is due in part to large differences in absorption coefficients and chemical
and optical characteristics of DOC among sites (Bricaud, Morel and Prieur 1981;
Malcolm 1990; McKnight, Aiken and Smith 1991; McKnight et al. 1994; Jerome
and Bukata 1998). A large range of variation is reported in aquatic environments
(Malcolm 1990; McKnight, Aiken and Smith 1991; McKnight et al. 1994), fur-
ther complicating comparisons between sites.
DOC sources are generally qualified as either allochthonous (terrestrially de-
rived) or autochthonous (derived from in-lake metabolism) and have very dif-
ferent optical properties. Allochthonous DOC is colored, of high molecular
weight, and contains a high proportion of aromatic residues. It is derived from
vegetation and terrestrial soils and is composed of differing proportions of aro-
matic humic and fulvic acids. Autochthonous DOC is microbially derived, usu-
ally from algal-rich environments. This type of DOC has higher nitrogen con-
tent and less aromaticity than terrestrially derived material.
Specific absorbance is but one optical property of DOC. It is known that DOC
is very highly absorptive in the UVR (Scully and Lean 1994; Morris et al. 1995).
DOC absorbance can vary greatly between sites. For example, DOC in prairie
saline lakes (or closed-basin lakes) is more "transparent" then DOC from boreal
forest lakes (Curtis and Schindler 1997; Jerome and Bukata 1998). This type of
DOC contains far fewer aromatic structures than DOC from a boreal system.
Closed-basin lakes have longer water renewal times (100 years or more), result-
ing in decades or even centuries of photobleaching (Curtis and Adams 1995).
Photobleaching is the interaction of DOC and light, resulting in the loss of con-
jugated double bonds (aromaticity) and photolysis of larger molecules (Wetzel,
Hatcher and Bianchi 1995), increasing UV penetration. Fluorescence, another op-
tical property of DOC, is useful for distinguishing between bleached allochtho-
nuus and autochthonous DOC (Donahue et al. 1998, McKnight et al. in press)
as its intensity is lower for autochthonous DOC. It is interesting to note that pho-
tolysis of DOC yields biologically available products (e.g., glyxolate and pyru-
vate) that are readily taken up by bacterioplankton, thus enhancing microbial ac-
tivity (Wetzel, Hatcher and Bianchi 1995; HemdI1997). In spite of that, the pho-
tochemical breakdown of DOC exceeds the microbial degradation of DOC by
several orders of magnitude (Molot and Dillon 1997).
Catchment characteristics are important in determining DOC type and con-
centrations. Lakes and streams at high altitudes and latitudes generally have catch-
ments with little vegetation and soils containing little organic material (Schindler
and Curtis 1997; McKnight et al. 1997). Similarly, DOC from polar desert catch-
ments has a reduced ratio of aromatic to aliphatic organic residue (McKnight et
al. 1994). Typically, wetlands have the highest DOC concentration (10-50 mg
C 1-1; Curtis 1998) and alpine lakes the lowest (0.05-3.0 mg C I-I; Baron, McK-
night and Denning 1991). Rates of export of DOC are high in peatlands and bogs,
having a profound impact on lake color (Urban, Bayley and Eisenreich 1989).
Furthermore, DOC from bogs contains a greater fraction of aromatic fulvic acids
(McKnight et al. 1985). In general, there is a positive relationship between the
relative drainage area (catchment area/lake surface area) and DOC inputs (Ras-
mussen, Godbout and Shallenberg 1989; Curtis and Schindler 1997; Curtis 1998),
whereas water color (and DOC content) are inversely proportional to water res-
idence time (Curtis and Schindler 1997; Dillon and Molot 1997).
Climate also interacts with topography and geology to modify DOC loadings
in aquatic systems (Curtis 1998). This relationship invariably causes high inter-
annual variability in DOC inputs resulting from differences in precipitation,
streamflow, and residence in lakes (Schindler and Curtis 1997; Schindler et al.
1997). Typically, DOC content (Hessen et al. 1997) and photoreactivity (Lindell,
Graneli and Bertilsson 2000) declines from spring to fall (Hessen et al. 1997).
However, a single storm event can increase DOC inputs by as much as approx-
imately 400% in streams (Hinton, Schiff and English 1997).
Very little information exists on absorption and scattering of UV by phyto-
plankton, other particulates, or suspended minerals or sediments. Particulate ma-
terial is an important UV attennator in marine systems and in the Laurentian
Great Lakes where there is little attenuation by dissolved substances (Kirk 1994a;
Smith et al. 1999), but not in smaller lakes where the correlation with chloro-
phyll is rather weak (Scully and Lean 1994) and most attenuation of all solar
wavelengths is by colored organic matter (Schindler 1971). However, it is known
that certain algae, macroalgae, and cyanobacteria can synthesize a variety of com-
pounds that strongly absorb in the UV. Such compounds are scytonemin (Gar-
cia-Pichel and Castenholz 1991) and mycosporine-like amino acids (Garcia-
Pichel and Castenholz 1993). These compounds are also found in consumers who
ingest/assimilate them with their food.
The fraction of photons absorbed by chlorophyll and DOC is wavelength de-
pendent. As shown by the Jerome and Bukata (1998) photon budget for inland
waters, only 5% of UV-A and UV-B photons are reflected by the air-water in-
terface and absorbed by pure water. The remaining 90% are absorbed by DOC
(55%-86%) and phytoplankton (5%-35%), depending on the wavelength.
Chlorophyll absorbs only a small fraction (-5%) ofUV-B photons but displays
two absorption peaks at 338 nm (25%) and 400 nm (35%), wavelengths at which
DOC displays minima in absorption.
Vertical Attenuation Coefficients and Measurements

Vertical attenuation coefficients (Kd) for solar radiation are calculated from the
slope of the regression of the rate of decrease in UVR penetration with depth be-
low the zone where surface reflectance affects measurements. Coefficients range
from 0.05 m- I in the clearest waters to more than 30 m- I in dark-brown, hu-
mic waters. These ranges translate in UVR penetration depths from several dozen
meters in the clearest ocean waters (Gieskes and Kray 1990; Smith et al. 1992;
Booth and Morrow 1997) to a few centimeters in humic lakes (Lean 1998).
Empirical models that predict the Kd have been devised by Smith and Baker
(1981) to allow prediction of attenuation and irradiance penetration from water
column content of DOC and suspended constituents (chlorophyll). Scully and
Lean (1994) described the relationship of the attenuation of UV in lakes between
chlorophyll, dissolved organic carbon (DOC), and particulate organic carbon
(POC) and found that attenuation coefficients of UV-B and UV-A could be pre-
dicted using empirically derived equations. Kd (UV-B and UV-A) correlated best
with DOC and was found to be a power function of the concentration of DOC
(Scully and Lean 1994):
KdUV-B = 0.415 (DOC)1.86 ; r2 = 0.97 (1)
KdUV-A = 0.299 (DOC)1.53 ; r2 = 0.95 (2)
Schindler et al. (1996b) refitted the data to predict the maximum (1 % surface)
depth of UV-B penetration, using a slightly more complex equation:
1% UV -B = 5.173 (DOC) -0.706 - 1.029; r2 = 0.98
These empirical relationships are poor for lakes with DOC concentrations greater
than 8 mg C I-I (Lean 1998) or for closed-basin lakes (where DOC is highly
photobleached) (Arts et al. 2000), but serve as a useful approximation of optical
properties in the UV range for most lakes. Empirical relationships for UVR at-
tenuation of saline lakes are presented by Arts et al. (2000).
Freshwater lakes show tremendous variability with respect to penetration and
attenuation of UVR, almost 1000 fold (Figure 2.4). Concentrations of DOC range
from less than 1 mg C I-I in transparent lakes (mainly alpine or polar lakes) to
50 mg C I-I in bog waters. Of the 16 Canadian and alpine lakes from the Scully
and Lean (1994) study, all but one lake exhibited Kd values in the UV-B greater
than 1.0 m- I . Morris et al. (1995) conducted a similar study with 59 lakes from
the Northeastern United States, Colorado, Alaska, and Argentina for which DOC
concentrations were between 0.2 and 23 mg C I-I and Kd305 between about 0.2
m -I and 130 m - I. The lowest Kd value (0.2 m -I) was for an alpine lake in the
high Andes, and the observed highest values were in high-DOC humic lakes.
Similarly, high-latitude lakes from the Canadian high Arctic and subarctic Que-
bec exhibited K d305 values between less than I m -[ and about 40 m -[ (Laurion,
Vincent and Lean 1997).
Even a few centimeters of snow cover would effectively block UV from en-
tering lakes and oceans, as it does for PAR (Schindler and Nighswander 1970).
However, in the absence of snow, ice is highly transparent to UV in lakes (Vin-
cent et al. 1998) and oceans (Trodahl and Buckley 1990). In a comparison of
four Antarctic permanently ice-covered lakes, Vincent et al. (1998) found that
UVR penetrated well beneath the ice in all four lakes. Because of their polar
desert catchments, which are devoid of any vegetation, these lakes receive very
small amounts of allochthonous DOC. Attenuation coefficients for Lake Yanda,
an ultraoligotrophic Antarctic lake, were the lowest published (Figure 2.4). UV-B
(305 nm) penetrated past 30 m and UV-A (380 nm) was recorded at 60 m.
100
.... ---
---
10
- --
g
.
c
==.
·u
.
co
c
co
Tic
~ 0.1
0.01
300 320 340 360 380
Wavelength (nm)
_ _ G,'os (Nonh••" USA)·' --6-- Meadow C, .. k (CoIo_)· 1

- - lacawac (Norlll".,. USA)·' - . . Tool (AI" ..)·,
--+-- lae ""u Clal.. (Non",,, 0.'1«)·2 _ "" (fue.,o)·2
- -Cromwell (Ouebe<:r3 -O-- Correntoso ~ArOflnllnaH
~ Snowflate ~Alpme Alberta)-3 - + -Vanda (Antarctlc}-'"
- a - 1224 (Norlll,.." OnWlo)·5 _ _ L239INorlllW<!" 0."'10)·5
FIGURE 2.4. Attenuation coefficients for various lakes differing in DOC concentration.
Data from (1) Morris et al. 1995; (2) Laurion, Vincent and Lean 1997; (3) Scully and
Lean 1994; (4) Vincent et al. 1998; and (5) S.I. Page, Freshwater Institute, Winnipeg,
Canada, unpublished data
Declines in DOC levels resulting from climatic warming and acid precipita-
tion (see following) can dramatically increase penetration of UV-B and PAR.
Below a threshold of 2-3 mg DOC 1-1, UV penetration increases rapidly (Lau-
rion, Vincent and Lean 1997; Morris et al. 1995; Schindler et al. 1996a;
Williamson et al. 1996). These DOC levels are typical in about a third of the
lakes in North America's boreal forest but in a higher proportion of alpine and
polar lakes. Low DOC levels could be a stimulus for pigment formation in zoo-
plankton (Byron 1982; Hessen 1993; Vinebrooke and Leavitt 1999) and algae
(Leavitt et al. 1997) in alpine lakes.
Vertical Stratification, Mixing, and Flowing Waters

Shallow depths and seasonal stratification can potentially expose plankton and
benthos to harsh UV environments. In shallow clear alpine lakes and ponds, high
UV can penetrate the entire water column. Seasonal stratification is also likely
to affect exposure in lakes, especially when near-surface shallow stratification
occurs in lakes (Milot-Roy and Vincent 1994; Xenopoulos, Prairie and Bird
2000). Near-surface thermoclines are frequent in boreal lakes, particularly in
small lakes (Xenopoulos and Schindler, unpublished data).
Meteorological conditions can influence the variability of underwater irradi-
ance. Under sunny skies and slightly windy conditions, PAR and UVR values
were more variable than during sunny and windless conditions (Laurion, Vin-
cent and Lean 1997). This variation was spectrally dependent; PAR values at 30-
cm depth varied by about 20% whereas UVR varied only by 5% (Laurion, Vin-
cent and Lean 1997). Piazena and Hader (1994) noted some noise in their
irradiance curves when waves and clouds were present. They also showed that
both total mixing and strong surface stratification can influence the UV fluence
rates in coastal lagoons.
DOC is also probably the most important factor determining the amount of
UVR exposure on streams and rivers. The larger fraction of DOC in streams is
the refractory allochthonous DOC (McDowell and Fisher 1976). However, shad-
ing by the forest riparian canopy is potentially another important factor affect-
ing UV exposure in flowing waters (DeNicola, Hoagland and Roemer 1992). Re-
moving an entire canopy increased the UV-B reaching streams by 500% (DJ.
Kelly, University of Alberta, unpublished data). This increase in UV-B can lead
to dramatic reorganization of invertebrate and algal communities (Bothwell, Sher-
bot and Pollock 1994; Donahue and Schindler 1998).
Synergistic Interactions of UV Radiation and

Climate Change
Because of the negative exponential relationship between DOC and UV, lakes
with less than 2-3 mg C 1-1 allow high exposure of aquatic communities to UVR.
There are now records of declining levels of DOC following climate warming
(Schindler 1997; Schindler et al. 1996a,b, 1997). Schindler et al. (1996a) reported
a warming trend of 1.6°C for the boreal forest of northwestern Ontario during a
20-year period (1970-1990) and a coincident decrease in DOC concentration as
a result of reduced inputs via streamflow and increased in-lake degradation
(Schindler et al. 1997). In particular, precipitation decreased by 25% and evap-
oration and forest fires increased. Forest fires cause decreased DOC inputs by
increasing mineralization of soils (Schindler et al. 1997). Also, water renewal
times of lakes were increased, enhancing photobleaching and mineralization of
DOC to carbon dioxide (Dillon and Molot 1997). Overall, climatic warming
caused DOC to decline 15%-25% (Schindler et al. 1996b, 1997) and increased
UV penetration by 30% in boreal lakes. Such patterns are expected to be mag-
nified in alpine, arctic, or acidified lakes where low DOC content provides less
protection to the biota.
Synergistic Interactions of UV and Acid Rain

Acidified lakes are known to lose DOC (Davis, Anderson and Berge 1985; Ef-
fler, Schafran and Driscoll 1985; Schindler et al. 1996b, 1997; Yan et al. 1996).
Both precipitation and mineralization of DOC are increased (Dillon and Molot
1997; Schindler et al. 1997). DOC declined 80% in an experimentally acidified
lake of the Experimental Lakes Area in Ontario, Canada (Schindler et al. 1997;
Schindler 1998), increasing UV penetration by nearly 900% (Donahue et al.
1998). Humic acids are coagulated and precipitated into the sediments following
protonation from acidity. However, acidification does not only affect the quan-
tity of DOC, it also changes its optical properties significantly, reducing its ca-
pacity to absorb light (Donahue et al. 1998). It was hypothesized that the de-
crease in pH increased the oxidation of humic DOC, leaving only the aliphatic
portion of the aromatic ring (Donahue et al. 1998).
Conclusion
UV -B represents less than 1% of the total solar flux reaching the Earth's surface.
However, it is highly energetic and its impact on organisms can be substantial,
from damaging macromolecular cellular structures to possible alterations in pri-
mary productivity and structure and function of ecosystems. Consequently, it is
essential to understand and have accurate characterization of UV-B transmitting
through the atmosphere and reaching the Earth's boundary layer and aquatic
ecosystems. Physical factors in atmosphere and water affect the UV exposure of
organisms in a complex matter. When determining UV exposure, one cannot con-
sider stratospheric ozone concentration alone. Air pollution, clouds, plant canopy,
and albedo can all interact with stratospheric ozone depletion and influence UV
exposure on ecosystems. In aquatic systems, a range of factors also interact to-
gether to determine UV exposure, such as basin size and dissolved organic sub-
stances. Gorham (1996) referred to the complex interaction of a depleting strato-
spheric ozone, climate warming, and acidification as the "three-pronged attack."
54 Marguerite A Xenopoulos and David W. Schindler
All three are anthropogenic-induced stressors and contribute together in exacer-

bating the effects of increased UV exposure of aquatic systems.
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3
Ultraviolet Radiation and Amphibians
ANDREW R. BLAUSTEIN, LISA K. BELDEN, AUDREY C. HATCH,
LEE B. KATS, PETER D. HOFFMAN, JOHN B. HAYS, ADOLFO MARCO,
DOUGLAS P. CHIVERS, AND JOSEPH M. KffiSECKER
Environmental changes, including those associated with the atmosphere, may sig-
nificantly affect individual animals, populations, and ultimately communities. Ul-
traviolet-B (UV-B) radiation, increasing because of stratospheric ozone deple-
tion, has been suggested as causing mortality and a variety of sublethal effects
in a number of organisms, including amphibians. At the terrestrial surface, UV-B
(280-315 om) radiation is extremely important biologically. Critical biomole-
cules absorb light of higher wavelength less efficiently, and stratospheric ozone
absorbs most light of lower wavelength (Blaustein et al. 1994a).
The eggs of certain amphibian species hatch at significantly lower rates if they
are exposed to ambient UV-B light (e.g., Blaustein et al. 1994a; Anzalone, Kats
and Gordon 1998; Lizana and Pedraza 1998; Broomhall, Osborne and Cunning-
ham, 2000). In addition to causing mortality in embryos, UV-B radiation induces
sublethal effects in amphibians. These effects include lowered rates of growth
and development, increased developmental and physiological deformities, and
behavioral changes (Worrest and Kimeldorf 1976; Hays et al. 1996; Nagl and
Hofer 1997; Fite et aI. 1998; Belden, Wildy and Blaustein, 2000; Blaustein et
aI., 2000; Kats et al., 2000).
Amphibians can cope with the harmful effects of UV -B radiation in a number
of ways, which include behavioral and molecular mechanisms. For example, noc-
turnal amphibians or those that live under dense foliage may avoid UV-B radi-
ation. If amphibians lay their eggs under logs, under forest debris, or in relatively
deep water, their exposure to UV -B radiation is limited. Some species can change
color when exposed to UV radiation. Color change, such as skin darkening, may
protect amphibians from the harmful effects of UV radiation. Certain species
have pigmented eggs and a surrounding jelly coat that may impede UV radia-
tion. Moreover, some species have an efficient capacity to remove UV-induced
DNA damage at the molecular level.
Adverse effects of UV radiation on amphibians may have significant effects
on their populations and ultimately on the communities in which they live. Be-
cause there are significant interspecific differences in response to UV radiation
in amphibians, adverse effects on some species may alter populations of other
species.
63
64 Andrew R. Blaustein, Lisa K. Belden, Audrey C. Hatch, et al.
In this chapter, we (1) briefly review the results of field experiments that have
tested the effects of ambient UV radiation on amphibian hatching success;
(2) provide examples of sublethal UV damage to amphibians; (3) discuss how
UV may interact synergistically with other factors, including pathogens and
chemical pollutants; (4) provide examples of defenses that amphibians may use
to limit their damage or exposure to UV radiation, and (5) consider how UV ra-
diation may affect amphibian populations and ultimately the communities in
which they live,
Effects of UV -B Radiation in the Field

We predicted that the effects ofUV-B radiation on eggs and embryos would vary
according to their natural exposure to sunlight and their ability to repair UV-
induced DNA damage (Blaustein et al. 1994a). Thus, we suggested that the eggs
of species with a relatively high capacity to repair UV-induced DNA damage
would be more resistant to UV-B than those with a lower capacity.
Our predictions on the effects of UV exposure on developing amphibian em-
bryos were initially tested using field experiments (Blaustein et al. 1994a). Since
our initial studies, a number of similar field experiments have been conduct~d
by other laboratories (reviewed in Blaustein et al. 1998). In general, these stud-
ies investigated the effects of UV-B radiation on fertilized eggs that were placed
in enclosures that varied in size and shape between studies. Filters that remove
UV-B radiation were placed on the tops of some enclosures, and filters that al-
lowed UV-B to penetrate were placed over other enclosures (control filters)
(Blaustein et al. 1998). In some studies, enclosures with no filters were used as
an additional control. Researchers compared the hatching success of eggs under
each regimen.
These studies have demonstrated that the embryos of some species are more
resistant to UV-B radiation than others (Blaustein et al. 1998) (Table 3.1). For ex-
ample, in Oregon, the hatching success of Cascades frogs (Rana cascadae), west-
ern toads (Bufo boreas), and long-toed (Ambystoma macrodactylum) and North-
western (A. gracile) salamanders was lower when exposed to ambient UV-B
radiation than when eggs were shielded from UV-B (Blaustein et al. 1998). How-
ever, the hatching success of spotted (R. pretiosa and R. luteiventris), red-legged
(R. aurora), and Pacific tree (Hyla regilla) frogs was not significantly different
among the UV -shielded and UV -exposed treatments (Blaustein et al. 1998). In-
terspecific differences in hatching success have been found in a number of stud-
ies at various locations around the world (Ovaska, Davis and Flamarique 1997;
Anzalone, Kats and Gordon 1998; Lizana and Pedraza 1998) (see Table 3.1).
Although hatching rates of some species may appear unaffected by ambient
UV radiation in field experiments, the interpretation of such 'negative' results
should be done with caution. For example, UV radiation may induce sublethal
effects that may not be apparent until later life history stages (discussed later;
see also Table 3.1). It is also possible that the eggs used in some studies are
3. Ultraviolet Radiation and Amphibians 65
TABLE 3.1. Examples of studies showing lethal and sublethal effects of ultraviolet
radiation alone or in synergism with other factors on amphibians.
Synergistic effects
Species Effect ofUV with UV References
Frogs and Toads
BuJo boreas Increases embryo With Saprolegnia Worrest and
mortality; (fungus) increases Kimeldorf 1976;
developmental embryo mortality Blaustein et al
abnormalities; 1994a; Kats et al
hampers 2000
anti predator
behavior
BuJo buJo Increases embryo Lizana and Pedraza
mortality 1998
Crineria signifera Increases embryo Broornhall, Osborne
mortality and Cunningham
2000
Hyla arborea Causes skin Langhelle, Lyndell
darkening and Nystrom 1999
Hyla cadaverina Increases embryo Anzalone, Kats and
mortality Gordon 1998
Hyla chrysoscelis Embryonic Starnes, Kennedy
deformities and Petranka 2000
Hyla regUla Developmental and Hays et al 1996
physiological
abnormalities
Hyla versicolor Causes skin With carbaryl Zaga et al 1998
darkening; decreases
decreases swimming activity
swimming activity
Litoria aurea Behavioral van de Mortel and
avoidance of UV Buttemer 1998
Littoria peronii Behavioral van de Mortel and
avoidance of UV Buttemer 1998
Litoria verreauxii Increases embryo Broornhall, Osborne
mortality and Cunningham
2000
Pseudacris triseriata Embryonic Starnes, Kennedy
deformities and Petranka 2000
Rana catesbeiana Witb fluorantbene Walker, Taylor and
causes skin Oris 1998
damage and
hyperactivity
Rana clamitans Delayed Grant and Licht
development; 1995
morphological
abnormalities
66 Andrew R. Blaustein, Lisa K. Belden, Audrey C. Hatch, et a1.
TABLE 3.1. Continued

Synergistic effects
Species Effect of UV with UV References
Rana cascadae Increases embryo With Saprolegnia Blaustein et al
mortality; retinal (fungus) increases 1994a; Hays et al
damage; embryo mortality 1996; Fite et al
developmental and 1998; Kats et al
physiological 2000
abnormalities;
hampers
anti predator
behavior
Rana pipiens Causes deformities With low pH Long, Saylor and
in larvae and reduces hatching Soule' 1995;Aulldey
juveniles success; With et al 1998; Hatch
fluoranthene and Burton 1998;
causes deformities Monson et al 1998
Rana sylvatica A voids high doses Grant and Licht
of UV; causes skin 1995; Roth et al
darkening; 1996
morphological and
behavioral
abnormalities
Xenopus laevis Causes skin With fluoranthene Bruggeman, Bantle
darkening; causes deformities; and Goad 1998;
decreases with carbaryl Hatch and Burton
swimming activity; changes swimming 1998; Zaga et al
reduces growth behavior 1998
Salamanders
Ambystoma gracile Increases embryo Blaustein et al 1995
mortality
Ambystoma. Increases embryo Blaustein et al 1997;
macrodactylum mortality; causes Belden, Wildy and
deformities; slows Blaustein 2000
growth
Taricha granulosa Increases activity Blaustein et al 2000
Taricha torosa Increases embryo Anzalone, Kats and
mortality Gordon 1998
Triturus alpestris Skin damage; Nagl and Hofer
causes erratic 1997
swimming behavior
Triturus cristatus Skin damage; Langhelle, Lyndell
causes erratic and Nystrom 1999
swimming behavior
Triturus marmoratus Increases embryo Marco et al
mortality; causes unpublished
deformities
resistant remnants of a population whose eggs were less resistant and that per-
ished. However, studies of the same species at different sites lend credence that
negative results (no UV effect) are real. For example, three studies in different re-
gions failed to find an effect of UV on hatching success in Pacific treefrogs (Hyla
regilla) (Blaustein et al. 1994a; Ovaska, Davis and Flamarique 1997; Anzalone,
Kats and Gordon 1998). Even though the methods used between studies were dif-
ferent and we believe comparisons between studies should be made with caution,
based on the number of locales used and consistency of the results, we conclude
that ambient UV radiation does not affect the hatching success of H. regilla.
Sublethal Effects
Mortality is the most extreme effect of UV-B radiation. However, sublethal ef-
fects may also be important. Sublethal effects can alter growth, development, and
behavior. For example, in field experiments, long-toed salamander (Ambystoma
macrodactylum) embryos exposed to UV-B radiation not only hatched at a much
lower frequency than those shielded from UV -B but also displayed a much higher
proportion of deformities (Blaustein et al. 1997). Thus, only 14.5% of the em-
bryos survived when exposed to UV-B radiation compared with 95% survival
in the shielded regimes. Moreover, more than 90% of the survivors exposed to
UV-B radiation were deformed, compared with only 0.5% that were deformed
under UV -blocking shields. Under laboratory conditions, larval A. macrodacty-
lum exposed to simulated low levels of UV-B radiation had slower growth rates
than those shielded from UV-B (Belden, Wildy and Blaustein, 2000).
Changes in behavior after exposure to UV-B radiation are reported in a num-
ber of studies. For example, exposure of roughskin newts (Taricha granulosa)
to UV -B radiation in the laboratory caused them to increase their activity
(Blaustein et aI., 2000). Changes in activity patterns after exposure to UV-B ra-
diation have been observed in a number of other species as well (Nagl and Hofer
1997; Zag a et al. 1998) (see Table 3.1). Antipredator behaviors may also be af-
fected by exposure to UV-B radiation. For example, Cascades (Rana cascadae)
frog tadpoles and juvenile western toads (Bufo boreas) exposed to low levels of
UV radiation did not respond to the chemical cues of predators as quickly as
those that were not exposed to UV radiation (Kats, et al. 2000).
Low-level exposure to UV-B radiation in the laboratory causes a number of
developmental and physiological deformities in frogs and toads (Worrest and
Kimeldorf 1976; Hays et al. 1996) (Table 3.1). These abnormalities include
edema, skeletal anomalies, and eye damage. Adult Cascades (R. cascadae) frogs
from Oregon have distinctive outer retinal abnormalities in the inferior retina that
include the abnormal distribution of retinal pigment, damaged photoreceptors,
and the presence of large pigment-filled macrophages consistent with damage by
solar radiation (Fite et al. 1998). Fite et al. (1998) suggested that this damage
may significantly impair the vision of R. cascadae that bask in sunlight at rela-
tively high altitudes.
The impairment of vision or the inability to perceive chemical cues of preda-

tors after exposure to relatively small doses of UV radiation may have profound
implications for amphibians. Obviously, individuals that cannot perceive preda-
tors will be at a significant disadvantage compared with those individuals that
can. Moreover, if such impairments occur in a number of species, the amphib-
ian component of certain ecological communities may be at risk.
Synergistic Effects
In nature, multiple environmental agents may affect amphibians as they develop.
We next provide examples of how UV-B radiation may interact synergistically
with other factors.
The fungus Saprolegnia ferax has contributed to mortality in several amphib-
ian species in the Pacific Northwest (Blaustein et al. 1994b; Kiesecker and
Blaustein 1997, 1999). In field experiments, Kiesecker and Blaustein (1995) dem-
onstrated a synergism between UV-B radiation and Saprolegnia. Rana cascadae
and B. boreas had reduced hatching success in the presence of Saprolegnia. In
addition, when exposed to both Saprolegnia and UV-B, embryos of R. cascadae
and B. boreas experienced significantly higher mortality than when they were
exposed to either factor alone.
It is possible that UV-B radiation weakens the disease defense mechanisms of
developing embryos, making them more susceptible to infection. Because
pathogens may play an important role in some amphibian population declines
(Blaustein et al. 1994b; Kiesecker and Blaustein 1997; Daszak et al. 1999), it is
important to conduct experimental studies, preferably in the field, to determine
if UV-B radiation enhances the effects of specific pathogens.
Several studies have examined synergistic interactions between UV and chem-
ical contaminants on developing amphibians (Kagan, Kagan and Buhse 1984;
Ankley et al. 1998; Hatch and Burton 1998; Walker, Taylor and Oris 1998; Zaga
et al. 1998; Daszak et al. 1999; Monson et al. 1999) (see Table 3.1). Synergism
may occur when developing amphibians have reduced ability to respond to one
stressor in the presence of another. For example, increasing levels of UV-B ra-
diation may reduce the ability of developing amphibians to cope with other en-
vironmental insults such as acidification. Because acidification alone can ad-
versely affect amphibians (Pierce 1985; Harte and Hoffman 1989; Dunson,
Wyman and Corbett 1992; Kiesecker 1996), in regions where acid pollution is a
concern there may be synergistic effects between low pH and UV-B radiation.
Long, Saylor and Soule (1995) studied the combined effects of UV-B and low
pH and observed detrimental effects on survival when UV intensity was increased
to levels expected at high elevations and low pH. No significant effects were at-
tributed to either factor alone. Synergism between UV and environmental pollu-
tants may also occur when one factor enhances the toxicity of the other agent.
Thus, chemical contaminants that absorb strongly in some portion of the UV
spectrum are particularly likely to be phototoxic. Because UV may penetrate

freshwater to significant depths, phototoxicity is environmentally relevant.
Chemical contaminants and UV can interact by one of two general mecha-
nisms. When toxicity is caused by bioaccumulated chemical interactions with
UV, greater toxicity will be observed when animals are exposed to both UV and
the chemical or to the chemical first and then to UV light, as in the case of poly-
cyclic aromatic hydrocarbons (PAHs). Toxicity may also occur when UV directly
alters a chemical to become more toxic, as in the case of the insecticide carbaryl.
PAHs are multiple-ringed hydrocarbons that contaminate ponds and streams via
road runoff, direct industrial discharge, or atmospheric deposition. PAHs absorb
UV-A (320-400 nm) and are acutely toxic by causing singlet oxygen to form
within the cell. In the presence of sunlight, some PAHs (such as anthracene,
benzo(a)pyrene, and fluoranthene) can be highly toxic to aquatic animals at en-
vironmentally realistic levels (Bowling et al. 1983), including amphibians (Ka-
gan et al. 1987; Hatch and Burton 1998; Monson et al. 1999; Walker, Taylor and
Oris 1998). UV -A enhanced the toxicity of anthracene, benzo(a)pyrene, and 1,12-
benz(a)anthraquinone to larval newts (Pleurodeles waltl) exposed in the labora-
tory for 6 days (Fernandez and l'Haridon 1992). Similarly, exposure to UV-A
after newts were exposed to benzo(a)pyrene resulted in greater toxicity than did
exposure to benzo(a)pyrene alone (Fernandez and I'Haridon 1994). These results
demonstrated that the toxic mechanism involves a reaction that occurs within bi-
ological tissue, rather than an external alteration of PAH chemical structure by
UV-A.
Hatch and Burton (1998) investigated the effects of fluoranthene with and
without UV on amphibians in both laboratory and outdoor exposures. In the lab-
oratory, African clawed frogs (Xenopus laevis) exhibited the most deformities
(including abdominal edema and gut malformations) due to the combination of
UV and fluoranthene while the spotted salamander (Ambystoma maculatum) ex-
hibited no deformities. Outdoor experiments demonstrated that newly hatched
larvae were more sensitive than embryos to phototoxic fluoranthene. The mor-
tality risk was correlated with fluoranthene and UV intensity levels. Full sunlight
exposures and increasing fluoranthene levels greatly increased mortality rates for
A. maculatum and X. laevis. Walker, Taylor and Oris (1998) found behavioral
and histological effects of fluoranthene in the presence of UV on bullfrog (Rana
catesbeiana) larvae. A 2-day exposure to low levels of fluoranthene in the pres-
ence of UV caused structural disorganization at the microscopic level in the skin.
After 2 days of high fluoranthene exposure with UV, larvae exhibited hyper-
activity.
The insecticide carbaryl strongly absorbs UV-B. Zaga et al. (1998) investi-
gated synergism between carbaryl and UV-B on X. laevis and grey tree frog (Hyla
versicolor) embryos and larvae using a solar simulator. Swimming activity of
larvae was decreased by UV-B alone and by UV-B in combination with carbaryl.
Xenopus laevis demonstrated increased swimming with increasing carbaryl con-
centration; this response was reversed with concurrent exposure to UV-B, and
the larvae reduced their activity. Zaga et al. (1998) further investigated the pho-
toactivation of carbaryl and the photosensitization of X. laevis by irradiating car-
baryl before exposure to amphibians. Mortality increased significantly when the
chemical was irradiated, suggesting that the mechanism of toxicity involved pho-
toproducts of carbaryl. The photosensitization experiment exposed X. laevis to
nonirradiated carbaryl without UV and then transferred animals to clean water
with concurrent UV exposure. Mortality was correlated with increasing levels of
carbaryl and UV-B.
These studies demonstrate potentially dramatic interactions between UV
and environmental contaminants. Understanding the mechanisms of the UV-
chemical interactions is vital to predicting the potential effects of phototoxic
chemicals on amphibians in the environment.
Amphibian Defenses Against UV -B radiation

One reason why some species of amphibians are more sensitive to UV-B radia-
tion than others is that there were strong selection pressures, over evolutionary
time, for certain species to evolve mechanisms that counteract the harmful ef-
fects of UV-B radiation. There are two strategies to cope with the harmful ef-
fects of exposure to UV-B radiation: prevent damage from occurring or repair
damage once it occurs (Epel et al. 1999). Damage by UV-B radiation can be pre-
vented behaviorally by spatially or temporally avoiding exposure. For example,
adult amphibians that are nocturnal or live under forest debris or in closed-canopy
forests effectively avoid UV-B exposure. Amphibian larvae that are able to move
in response to environmental stimuli can also potentially avoid exposure. Fe-
males that lay eggs in low-UV environments, such as under logs or in deep wa-
ter, limit exposure of their eggs and embryos to UV-B radiation. In species that
lay their eggs in clear, shallow water, the jelly matrix/coat surrounding the eggs
may prevent UV damage by absorbing damaging wavelengths of light before
they reach the embryo. This hypothesis has some support because the jellies of
several species appear to absorb wavelengths in the UV -B range (Grant and Licht
1995; Ovaska, Davis and Flamarique 1997).
Physiological and morphological mechanisms may also limit UV exposure.
For example, pigments in the skin, such as melanin, provide some protection
from UV-induced DNA damage in mammals (Kollias et al. 1991). However,
these mechanisms have not been well studied in amphibians. A recent hypothe-
sis suggested that melanin production may protect developing amphibian em-
bryos from neural tube defects by acting as a natural sunscreen (Jablonski 1998).
Jablonski (1998) suggested that melanin is a relatively inexpensive way to pre-
vent critical metabolites, such as folate, from being degraded by UV light dur-
ing development. In addition, amphibians can change color in response to dif-
ferent light regimes and background coloration (Bagnara and Hadley 1973 and
references therein). It is possible that these color changes afford protection from
UV light. Some evidence suggests that certain amphibians may darken in re-
sponse to UV-B irradiance (Roth et al. 1996; Hatch and Burton 1998; Zaga et
al. 1998, Langhelle, Lindell and Nystrom 1999). Whether this response protects
the individuals from UV-B damage is not known.
DNA Repair
When UV radiation penetrates a cell, DNA photoproducts may form that can lead
to mutations or cell death. Embryos of some amphibian species may be more re-
sistant to UV-B because they can remove UV damage from DNA more effi-
ciently than others. One important repair process is enzymatic photoreactivation.
One enzyme, CPD-photolyase, uses visible light energy (300-500 nm) to remove
the most frequent UV-induced lesion in DNA, cyclobutane pyrimidine dimers
(CPDs) (Friedberg, Walker and Siede 1995). A second related enzyme, [6-4]-
photolyase, similarly uses light energy to reverse pyrimidine-[6-4']-pyrimidone
photoproducts ([6-4] photoproducts). Moreover, multiprotein broad specificity
excision repair processes can remove CPDs and [6-4] photoproducts. Both mech-
anisms may be used simultaneously, but excision repair is typically more effi-
cient for [6-4] photoproducts than for CPDs. Thus, CPD-photolyase appears to
be the first level of defense against CPDs for many organisms exposed to sun-
light (Pang and Hays 1991; Friedberg, Walker and Siede 1995).
We suggest that greater photolyase activities make some amphibian species
more resistant to UV-B radiation than others by removing more primary
cytotoxic/mutagenic photoproducts from their DNA. If eggs are damaged by
UV-B in field experiments, obviously none of the repair mechanisms are work-
ing efficiently enough to repair the damage. However, if eggs are resistant, it is
difficult to determine which combination of excision repair and photolyases is
removing damage. Because photoreactivation is probably the most important re-
pair mechanism in amphibians, a parsimonious explanation is that those species
with the highest photolyase activities are the most resistant to UV damage. In-
deed, the amount of CPD photolyase in eggs is positively correlated with sur-
vival of embryos in field experiments (Tables 3.1 and 3.2). For example, eggs
of the most resistant species in field experiments in Oregon (e.g., H. regilla, R.
aurora, R. pretiosa, and R. luteiventris) have higher CPD photolyase activity than
eggs of more susceptible species (e.g., R. cascadae, B. boreas, A. macrodacty-
lum, A. gracile) (Blaustein et al. 1998).
Even if eggs are laid in the open at high altitudes (where under certain con-
ditions UV levels may be high) and have long developmental periods in which
they are subjected to prolonged UV-B exposure, they may not be adversely af-
fected by UV-B radiation if they have efficient DNA repair mechanisms. Con-
versely, species with low photolyase levels may be quite sensitive to UV-B ra-
diation even if they live at very low altitudes (Blaustein et al. 1995).
Within a species, it is possible that individuals from one popUlation may dif-
fer from members of another population in their sensitivity to UV-B radiation.
This variation may be due to differences in their ability to repair DNA damage
TABLE 3.2. Photolyase activities and egg-laying behavior in North American amphibians.
Specific activitya of Egg-laying
photolyase 1011 behavior/exposure to
Species CPDs h- 1 f-Lg- 1 sunlightb
Frogs and toads
Ascaphus truei <0.1 Eggs laid under stones/unexposed
Bufo boreas 1.3 Eggs laid in open often shallow
waterlhigh exposure
Hyla cadaverina 3.5 Eggs laid near surface attached to twigs
or other debris/exposed
H. regilla 7.5 Eggs laid in open shallow waterlhigh
exposure
H. squirella 5.0 Eggs laid near bottom of pondsllimited
exposure
Rana aurora 6.1 Eggs often attached to stiff submerged
stem/variable exposure
R. cascadae 2.4 Eggs laid in open shallow waterlhigh
exposure
R. luteiventris 6.8 Eggs laid in open shallow waterlhigh
exposure
R. pretiosa 6.6 Eggs laid in open shallow waterlhigh
exposure
Xenopus laevis 0.1 In nature eggs laid under vegetationllimited
exposure
Salamanders
Ambystoma gracile 1.0 Eggs often laid in open water/some
exposure
A. macrodactylum 0.8 Eggs often laid in open water/some
exposure
Aneides ferreus 0.4 Eggs laid in cavities in logs or crevices in
rocks/not exposed
Batrachoseps wrighti 0.7 Eggs laid in or under logs/not exposed
Plethodon dunni <0.1 Eggs hidden/not exposed
P. vehiculum 0.5 Eggs hidden/not exposed
Rhyacotriton olympicus 0.3 Eggs laid in cracks in rocks/not exposed
Taricha granulosa 0.2 Eggs hiddenllimited exposure
CPDs, cyclobutane pyrimidine dimers.

aMethods used to calculate photolyase activities are given in Blaustein et al. 1994a and Hays and
Hoffman 1999.
bEgg-laying behavior information is from Behler and King 1979, Ashton and Ashton 1988, Nuss-
baum, Brodie and Storm 1983, and Walls 1992.
or to differences in individual egg-laying behavior. Thus, the eggs of one species

may differ between populations in their exposure to solar radiation. For exam-
ple, long-toed salamanders (A. macrodactylum) deposit their eggs in small dis-
crete clutches in shallow temporary ponds in the Willamette Valley of Oregon.
However, in the Cascade Range of Oregon they scatter eggs singly, with some
being laid in open shallow water and others in deeper water under rocks in tem-
porary or permanent ponds (personal observations, A.R.B.).
Ecological Consequences of Ultraviolet Damage

to Amphibians
The lethal effects of UV radiation on amphibians may eventually be observed at
the level of the population that can lead to profound changes in ecosystems. Am-
phibians are integral components of many ecosystems and may comprise a sig-
nificant proportion of the biomass (Burton and Likens 1975). Through their
trophic dynamics in ecological communities, a loss of amphibians could poten-
tially affect many other organisms (Stebbins and Cohen 1995). Adult amphib-
ians are important predators and prey in many ecosystems (Duellman and Trueb
1986), and larval amphibians are important herbivores and prey species in aquatic
habitats (Dickman 1968; Seale 1980; Morin, Lawlor and Johnson 1990). As they
move about and forage, larval amphibians may alter both the biological and phys-
ical parameters oflakes and ponds (Seale 1980; Morin, Lawlor and Johnson 1990;
Leibold and Wilbur 1992). Moreover, larvae are important regulators of primary
production (Dickman 1968; Seale 1980; Stebbins and Cohen 1995). As tadpole
numbers fluctuate, shifts in nutrient cycling, algal standing crops, and suspended
particle concentration may change (Seale 1980). Therefore, declines in numbers
of larval amphibians may lead to significant physical and biological changes in
some ecosystems.
Sublethal UV effects that alter behavior, growth, or development may ulti-
mately lead to the death of individual larvae if affected larvae cannot find food,
avoid predators, or find shelter effectively. Larvae with sublethal damage that
live for a while and whose behavior is adversely affected after UV exposure could
influence the structure of populations and entire communities. For example, if
antipredator behaviors were altered by exposure to UV-B radiation (Blaustein et
aI., 2000), individuals might be eaten more readily and populations might be sub-
jected to increased predation pressure. Furthermore, groups of tadpoles exposed
to UV-B may not be able to efficiently stir the substrate and therefore suspended
food may not be as available for them to filter.
Interspecific differences in susceptibility to UV radiation can potentially lead
to losses of some species within communities. As certain species disappear, sig-
nificant changes in ecosystems may occur. Changes in community structure will
depend upon the species that are affected because different species eat different
food items and have different predators. For example, in Oregon, the embryos
of R. cascadae and B. boreas are highly susceptible to UV-B radiation (Blaustein
et aI. 1994a). However, the embryos of H. regilla are resistant to UV-B radia-
tion. In communities where these species co-occur, there is great potential for
change. Continued mortality at the embryo stage in UV-sensitive R. cascadae
and B. boreas could lead to declining numbers of larvae and adults.
Studies of interspecific differences in susceptibility to a specific agent illus-
trate how differential susceptibility to UV-B radiation could affect competitive
interactions between amphibians. For example, in Oregon, in the absence of the
fungus SaproZegnia, R. cascadae larvae are superior competitors to H. regilla
larvae (Kiesecker and Blaustein 1999). However, in the presence of SaproZeg-
nia, the outcome of competitive interactions is reversed because H. regilla is not

susceptible to the fungal infection (Kiesecker and Blaustein 1999). It is possible
that competitive interactions between R. cascadae and H. regilla may also be re-
versed in the presence of UV-B radiation because R. cascadae is highly suscep-
tible to UV-B radiation whereas H. regilla is not.
Similarly, in Oregon, B. boreas is susceptible to UV-B radiation in the same
ponds where H. regilla is resistant to UV-B. A complex situation may become
manifest if B. boreas populations decline. Bufo boreas tadpoles are unpalatable
to many vertebrate predators (Peterson and Blaustein 1991). If B. boreas declines
in numbers, the larvae of the highly palatable species, H. regilla (Peterson and
Blaustein 1991), may persist or even increase; this could lead to an increase in
the number of predators that are attracted to H. regilla as prey.
Potentially, because of interspecific differences in susceptibility to UV radia-
tion, many of the ponds and lakes in Oregon, and perhaps in other regions, could
change from multi species amphibian systems to systems with fewer species. It
is also possible that the number of species will remain the same but the species
composition will differ. Synergistic interactions with UV radiation and other fac-
tors may also play a role in changing the amphibian component of ecological
communities. However, the population and community dynamics of such changes
are complex and difficult to predict. For example, if populations of H. regilla in
Oregon increase as the result of competitive release with R. cascadae and B.
boreas, increasing predation pressure may regulate their expanding populations
and their numbers may be kept low.
When changes in species composition occur, the physical parameters of the
aquatic habitat may also change. For example, large schools of toad tadpoles
chum water and move substrate as they forage for food (Wilbur 1977). If toads
susceptible to UV-B radiation experience declining numbers, this change could
affect foraging and other aspects of the biology of sympatric aquatic inverte-
brates, fishes, and plants. The disappearance of even a single amphibian species
could have profound affects on communities. Recent studies in other systems
have shown how UV sensitivity in one species may lead to significant changes
within a community (Bothwell, Sherbott and Pollock 1994).
Disturbances May Exacerbate the Effects of UV -B Radiation

Free-moving amphibians obviously may be able to detect solar radiation and
avoid large doses of UV-B in nature. However, over evolutionary time, behav-
iors may have been selected for that expose amphibians to prolonged bouts of
UV-B. Thus, in the Oregon Cascades and in many other regions, certain species
lay their eggs in open shallow water, their tadpoles aggregate in open shallow
water, and adults may bask in sunlight (O'Hara 1981; Blaustein et al. 1994a; Fite
et al. 1998). Furthermore, unlike adults, eggs, and under certain conditions, lar-
vae, cannot avoid sunlight.
Disturbances may exacerbate the effects of UV-B. For example, in southern

California, periodic fires may influence how amphibians lay their eggs and find
shelter (Gamradt and Kats 1997; Kerby and Kats 1997). Decreased canopy cover
as the result of fire may temporally subject eggs, larvae, and adults to increased
doses of ambient UV-B, which may hamper egg development, alter behavior,
and potentially affect local populations (Kerby and Kats 1997). Similarly, clear-
cutting in the Pacific Northwest has drastically decreased forest canopy cover
(Norse 1990; Noss and Peters 1995) where amphibians may find shelter (Walls,
Blaustein and Beatty 1992). Unlike eastern forests that have been cut a little at
a time over centuries, the northwestern forests have been clear cut in large tracts,
over decades (Ehrlich 1997). Thus, in a relatively short time, amphibians have
been subjected to significant loss of habitat from which they can obtain shelter
from solar radiation.
In other regions, including the tropics where habitat destruction opens gaps in
forest canopies, amphibians may be subjected to relatively large doses of solar
radiation. Temperature shifts and associated precipitation changes, which may
contribute to population declines of amphibians in the tropics (Pounds, Fogden
and Campbell 1999), may synergistically interact with UV to cause adverse af-
fects on amphibians.
Conclusions
The results of recent field experiments strongly suggest that ambient levels of
UV-B radiation are presently harming certain species of amphibians in many lo-
cations around the world. Results from laboratory experiments also show that
UV radiation damages amphibians. However, some species are more affected by
UV radiation than others. The effects may be lethal or sublethal and may occur
in embryos, larvae, juvenile, or adult life stages. Sublethal damage includes
slowed growth and development, skin damage, eye damage, and malformations
of the body. Moreover, exposure to UV radiation may change the behavior of
amphibians. For example, it may alter activity patterns or hamper antipredator
behaviors. Synergistic interactions of UV radiation with other factors are also
important. Pathogens and chemical contaminants interact with UV, causing lethal
and sublethal damage to amphibians.
Amphibians exhibit behaviors that may limit their exposure to UV radiation.
These activities include movement away from sunlight and laying eggs in deep
water, under logs, or in crevices. Amphibians may lay eggs with pigments or
jelly coats that protect them from the harmful affects of UV radiation. Some am-
phibians change color when exposed to UV radiation, which may act as a de-
fense mechanism. Amphibians may be able to remove UV-induced photoprod-
ucts from DNA via molecular mechanisms. Yet, there are distinct interspecific
differences in repair capacity.
UV radiation may contribute to some of the population declines of amphib-
ians that have been documented worldwide. Interspecific differences in suscep-

tibility to UV radiation may result in profound changes within ecological com-
munities. Populations of susceptible species may decline whereas populations of
more resistant species may persist or increase in numbers. Changes in the am-
phibian component of ecological communities may result in drastic changes in
overall community structure and in the physical properties of the habitat.
Acknowledgments. We thank D. Grant Hokit for critically reading this chapter.

We thank the National Science Foundation (IBN-9907732 to A.R.B. and L.B.K.)
and Katherine Bisbee II Fund of the Oregon Community Foundation for support.
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4
Ultraviolet Radiation and
Plant Ecosystems
THOMAS A. DAY
This chapter addresses the impact of ambient and enhanced levels of ultraviolet-
B radiation (UV-B, 280-320 nm) on terrestrial vascular plants, with a focus on
findings published during the past 5 years. It discusses some of the more recent
ideas regarding plant responses to ambient and enhanced UV-B levels and the
possible mechanisms involved. This review is not meant to be exhaustive, and
for additional topics readers are referred to Caldwell and Flint (1994), Bjorn
(1996), Bjorn et al. (1996, 1997), Lumdsen (1997), Rozema et al. (1997a,b), and
Caldwell et al. (1998). The past, current, and future UV-B environment of ter-
restrial plants is briefly reviewed. Because of difficulties in extrapolating from
indoor studies to field situations, I focus on recent findings from field studies,
with particular reference to those employing ambient UV-B filter exclusions and
modulated UV-B supplements.
Among the most consistently observed responses to higher UV-B levels in
these studies were increases in leaf concentrations of UV -B-absorbing compounds
and reductions in leaf or hypocotyl size. The significance of increases in UV-B-
absorbing compounds is discussed, and the assumption that these increases trans-
late into improved UV-B-screening effectiveness that mitigates damage is as-
sessed. The putative role of these compounds as antioxidants is also reviewed.
The significance of oxidative and DNA damage, as well as impaired photosyn-
thesis, in explaining plant responses to UV-B are also considered. Last, the in-
fluence of UV-B plant exposure on other trophic-level processes such as litter
decomposition and insect herbivory is reviewed. Although the effects of UV-B
on plants should ultimately be viewed in conjunction with other abiotic factors,
because of the many uncertainties involved in generalizing about plants and en-
hanced UV-B, these additional interactions are not addressed.
UV-B Environment of Terrestrial Plants

Current UV-B Environment
In general, most terrestrial plants receive appreciably larger cumulative doses of
UV-B than other organisms. The dependence of these plants on visible radiation
for photosynthesis precludes the strategy to grow in deeply shaded, low-UV-B
80
4. Ultraviolet Radiation and Plant Ecosystems 81
environments for many species. Furthermore, unlike many animals, terrestrial

plants are sessile and unable to avoid periods of high UV-B. In the case of ever-
green foliage, which may persist over several years, the large cumulative UV-B
dose this foliage may receive and must dissipate is impressive, considering the
UV-B photodamage that occurs in many materials permanently exposed to sun-
light (Andrady et al. 1995).
Although these traits certainly speak to the potential for plants to receive very
large UV-B doses, their UV-B environment is quite heterogenous in time and
space. UV-B levels and doses vary temporally over diurnal and annual cycles as
the result of changes in solar angle and day length, and along with these cycles
are more stochastic changes brought about by clouds that can lead to rapid, of-
ten dramatic, changes in UV-B irradiance. Although cloud cover usually reduces
absolute UV -B levels, clouds generally reduce UV -B to a lesser extent than higher
wavelengths because a greater proportion of incoming UV -B is diffuse rather
than collimated radiation compared to UV-A (320-400 nm) and visible or pho-
tosynthetically active radiation (PAR; 400-700 nm). Hence, ratios ofUV-B:UV-
A and UV-B:PAR typically increase under clouds, although this effect is very
dependent on solar angle and the degree and type of cloud cover (Thiel, Steiner
and Seidlitz 1997; Kuchinke and Nunez 1999).
Spatially, UV-B levels decline over large scales such as with increasing lati-
tude due to lower solar angles. At smaller spatial scales, UV -B levels typically
increase with elevation because of a thinner atmosphere, as well as the relatively
unpolluted, more transparent atmosphere found in many mountainous regions
(Caldwell, Robberecht and Billings 1980; Blumthaler, Ambach and Huber 1993;
Cabrera, Bozzo and Fuenzalida 1995; Bjorn et al. 1998). UV-B levels are also
likely to increase with distance from tropospheric air pollution sources such as
urban areas (Frederick et al. 1993). At still smaller scales, absolute UV-B levels
can decline dramatically within a plant canopy. Because of the greater diffuse
component of incoming UV-B, the ratio of UV-B:PAR is typically higher within
the canopy than outside (DeLucia, Day and Vogelmann 1991; Brown, Parker and
Posner 1994; Grant and Heisler 1996; Grant 1997; Flint and Caldwell 1998).
However, this difference depends on canopy architecture and location within the
canopy, and although the ratio of UV-B:PAR is usually higher within shaded ar-
eas of canopies, it can be lower in sunlight portions of canopy gaps (Brown,
Parker and Posner 1994; Flint and Caldwell 1998).
Plants may respond not only to changes in absolute UV -B levels but also to
changes in the ratio of UV-B:PAR (Deckmyn, Martens and Impens 1994; Deck-
myn and Impens 1997). Should this be the case, plants growing in shaded un-
derstorys or frequently cloudy areas where UV-B levels are low may not neces-
sarily be immune from UV-B effects.
Ozone Depletion and Enhanced UV-B

Superimposed on this dynamic UV-B environment are increases in UV-B driven
by depletion of stratospheric ozone caused by anthropogenic emissions. This pro-
cess has lead to marked declines in total ozone concentrations over many regions
82 Thomas A. Day
beginning about 1980, and since that time it appears responsible for about a 10%
decline in global stratospheric ozone (Solomon 1999). Ozone depletion events
are most pronounced over polar regions during springtime, and are most severe
over Antarctica where roughly one-half the ozone column is currently depleted
each austral spring (Jones and Shanklin 1995; Solomon 1999). Ozone-depleted
air masses from polar regions disperse in spring and can ultimately dilute ozone
concentrations over more temperate latitudes. Declines of about 5%-10% in the
ozone column have occurred through the 1990s at midlatitudes (Solomon 1999),
and these depletions have been documented not only in winter and spring but in
summer as well (Stolarski et al. 1991; McPeters and Labow 1996; Harris et al.
1997; Staehelin, Kegel and Harris 1998). These declines appear to involve
not only the mixing of ozone-depleted air from polar regions but also depletion
events at these midlatitudes. This depletion may be enhanced by particles from
volcanic eruptions but appears to be ultimately related to and dependent on
chlorofluorocarbon-driven ozone depletion (Solomon 1999).
Since the downward trend in stratospheric ozone concentrations began about
1980, biologically effective (erythemal) levels of UV-B appear to have increased
at Northern midlatitudes about 7% in the winter-spring and 4% in the summer-fall,
6% at Southern midlatitudes year around, 130% in Antarctica in spring, and 22%
in the arctic in spring (Madronich et al. 1998). Currently, experts suggest that ozone-
depleting chemicals will reach peak loads around 2000, followed by maximal ozone
depletion and peak UV-B levels during the next decade, with a return to pre-1980
levels of stratospheric ozone and UV-B occurring over the next half-century, al-
though many factors could delay this (Solomon and Daniel 1996; Madronich et al.
1998; Fraser and Prather 1999; Montzka et al. 1999). For example, Shindell, Rind
and Lonergan (1998) suggested that increasing concentrations of greenhouse gases
not only cool the stratosphere but may also reduce the frequency of stratospheric
warming events, leading to a more stable polar vortex and greater ozone depletion,
ultimately delaying peak ozone depletion until 2010--2019.
One simplistic way to consider how great this impact might be on plants is to
examine whether current levels of enhanced UV-B associated with anthropogenic
ozone depletion represent a unique situation for terrestrial plants. In geologic
time scales, the answer is likely no. The release of oxygen from aquatic pho-
toautotrophs into the atmosphere and subsequent development of ozone, which
very effectively absorbs solar UV-C and to a lesser extent UV-B, is thought to
have been a critical step in allowing plants to colonize terrestrial environments
about 470 million years ago (Lowry, Lee and Hebant 1980; Caldwell 1979; Gra-
ham 1993; Rozema et al. 1997a). Nevertheless, the atmosphere of these early
land plants likely contained less oxygen and ozone than currently, and UV-B lev-
els were likely to have been appreciably higher than present. On a smaller time
scale covering the past 100 million years, when many members of current flo-
ras evolved, it is difficult to assess how ozone levels and UV-B might have var-
ied, although the suggestion has been made that certain events such as asteroid
or comet impacts or certain large-scale volcanic eruptions may have lead to short-
term declines in ozone and appreciable increases in UV-B (Cockell 1999). On a
more contemporary time scale, it seems probable that depleted stratospheric ozone
levels during the 1990s have led to occasional peaks and short-term UV-B doses
that have exceeded those experienced by plants during the past century. Whether
this in tum has lead to higher seasonal or annual doses is unclear because of the
influence of other factors such as cloud cover. In summary, during the past decade
terrestrial plants at many higher latitudes and possibly midlatitudes, particularly
in the Southern Hemisphere, have probably experienced higher short-term
UV-B levels than at any time over the past 100 years.
Approaches to Studying Plant Responses to UV-B

In spite of the large amount of research during the past 15 years addressing how
ambient and enhanced UV-B levels affect plants, generalizations have been ten-
uous and many questions remain open to debate. This situation stems from sev-
eral reasons, including (1) technical challenges in predicting, measuring, and ap-
plying realistic UV-B levels and the strong interactions that UV-B can have with
UV-A and PAR in plant responses, and (2) our poor understanding of the targets
and mechanisms involved in plant responses to UV-B. Regarding the first point,
many growth chamber and greenhouse studies have exposed plants to UV-B
(sometimes at unrealistically high levels) under a background oflow UV-A and
PAR. Although these studies can provide useful information on UV-B targets
and mechanisms, UV-B effects on plants are typically exaggerated under such
conditions. This topic, as well as UV-B methodology in general, has received con-
siderable attention, and readers are referred to Warner and Caldwell (1983),
Mirecki and Teramura (1984), Middleton and Teramura (1993), Caldwell and Flint
(1994, 1997), Caldwell, Flint and Searles (1994), Rozema et al. (1997a,b), and
McLeod (1997). The significance of indoor plant responses under the high ratios
of UV-B:UV-A and UV-B:visible irradiance to those under outdoor spectral
regimes are questionable, and extrapolation to outdoor responses needs to be done
cautiously, particularly without supporting evidence from parallel field studies.
Fortunately, these concerns generated an emphasis on experiments conducted
under more realistic UV and visible irradiance regimens that have provided some
new insights into whether plants are responsive to current as well as to enhanced
UV-B levels predicted with continued ozone depletion. The two most widely
used approaches in outdoor or field UV-B studies involve either reducing or ex-
cluding some of the ambient UV-B reaching plants through the use of UV-B-
absorbing filters (exclusion studies) or supplementing ambient UV-B levels with
filtered UV-B lamps (lampbank studies). Exclusion studies are much simpler and
cheaper to conduct and make use of the natural solar spectrum but only allow
one to reduce natural UV -B levels. Thus, these studies typically test for the re-
sponse to ambient UV-B, although they can conceivably provide some informa-
tion about the influence of enhanced UV-B associated with ozone depletion
should they be conducted during documented ozone depletion events. In addi-
tion to UV-B, filter exclosures also modify other microclimatic factors such as
temperature and precipitation and require appropriate controls to account for these
effects.
84 Thomas A. Day
In contrast to exclusion studies, lampbank studies supplement current UV-B

levels in an attempt to mimic future enhancements in UV-B associated with ozone
depletion. This approach comes at appreciable cost and complexity and is not
immune from problems regarding how realistically lamps mimic natural UV-B
enhancements. When the levels of UV-B supplements are not continuously ad-
justed for background or ambient levels of radiation, large levels of UV-B can
be supplemented during periods of low ambient levels of UV-A and PAR, and
UV-B effects may be exaggerated (Sullivan et al. 1994). Modulated lampbank
systems, which continuously measure ambient solar irradiance (typically UV-B)
and adjust lamp output to compensate for low background UV-B, have largely
overcome this problem. However, even in these systems filtered UV-B sunlamps
provide an imperfect spectral supplement, although the significance of this is not
thoroughly understood (Caldwell and Flint 1997). Newsham et al. (1996) com-
pared the effects of UV -B lamps filtered with cellulose diacetate (a standard pro-
tocol that absorbs UV-C from the lamps but transmits most UV-B, and UV-A)
to those filtered with Mylar polyester (which absorbs most UV-B but transmits
most UV -A) and found that the majority of plant responses seen under the for-
mer were also observed under latter treatments, suggesting that the plants were
responding to the supplemental UV-A provided by the lamps.
In nearly all field studies to date, the percentage of ambient UV-B that is ex-
cluded by filters or supplemented with lampbanks remains constant throughout
the experimental period or growing season. However, ozone concentrations and
UV-B levels vary through the year, often showing large seasonal trends. For ex-
ample, Musil et al. (1999) used satellite ozone data from 1979 to 1991 with the
model of Bjorn and Murphy (1985) to estimate trends in UV-B BE (biologically
effective UV-B) at Southern midlatitudes. They found that the intra-annual or
seasonal variations in both ozone depletion and UV-BBE were greater than the
changes in mean annual ozone depletion and UV-BBE during this period. Hence,
a further refinement in approach would involve incorporating seasonal trends in
ozone concentrations and UV-B enhancements into UV-B treatment protocols,
as was done by Mepsted et al. (1996) and Stephen et al. (1999).
Although imperfect, exclusion studies and modulated supplement studies in
some ways complement each other in their shortcomings and currently provide
our most realistic insights into how plants respond to ambient and enhanced lev-
els of solar UV-B. What follows is a brief survey and an attempt at synthesis of
some recent findings using these two approaches. For the sake of including a rea-
sonable number of studies in this survey, concerns about treatment pseudorepli-
cation were not considered.
Are Plants Responsive to Current Levels of UV-B?

Some recent outdoor UV-B exclusion studies are summarized in Table 4.1. All
studies found that at least one of the species examined was responsive in some
way to reductions in ambient UV-B. This finding may not necessarily mean that
most plant species are responsive to UV-B, because in some of these studies
these responses were only detected in one of several species, cultivars, or clones
that were examined. These studies may also conceivably represent a biased view
of plant responsiveness as there is probably a greater likelihood that studies in
which no responses were detected go unpublished. However, the results from
these studies clearly illustrate that some species are responsive to current levels
of UV-B.
Among the most consistent responses among the studies presented in Table
4.1 was a reduction in leaf or hypocotyl elongation or length: more than half the
studies examining this parameter (5 of 8 studies) detected a reduction in length
in at least one species under the higher UV-B level. Additionally, 5 of the 10
studies examining total biomass production or concentrations of soluble leaf
UV-B-absorbing compounds detected a reduction in the former and an increase
in the latter.
Are Plants Responsive to Enhanced UV-B Levels?

Some recent outdoor UV-B supplementation studies involving modulated lamp-
banks are summarized in Table 4.2. Although every study detected at least one
significant response, in general, plant responses to UV-B were less frequent and
more subtle than in the exclusion studies. In no case did supplemental UV-B re-
duce total biomass production. The most consistent response was an increase in
concentrations of soluble leaf UV-B-absorbing compounds; four of seven stud-
ies found evidence of an increase, although in some cases they were only de-
tectable in the adaxial epidermis of certain leaf age classes (Day, Howells and
Ruhland 1996), or during certain times coinciding with high levels of background
UV-B (Stephen et al. 1999). In summary, the results of these supplemental
UV-B studies suggest that some plants are responsive to supplemental UV-B, al-
though the responses are subtle and total biomass production is not impaired.
Why do plants appear more responsive to UV-B in the exclusion studies than
in the modulated lampbank studies? One possibility is that differences in the UV-
B levels between treatments were greater in the exclusion than the lampbank
studies. However, the differences in UV-B BE between treatments in the exclu-
sion studies averaged 67% while those in the lampbank studies averaged 57%.
These differences in UV -BBE treatment levels are quite similar between the two
groups of studies. Furthermore, the exclusion studies that involved the smallest
differences in UV-BBE levels between treatments «15%; Deckmyn and Impens
1995; Mark, Saile-Mark and Tevini 1996) still detected some treatment effects.
Ballare et al. (1996) used exclusions that filtered approximately 0%, 25%, 50%,
75%, and 100% of ambient UV -B levels and noted that many responses increased
in parallel with the UV-B level. These small reductions in ambient UV-B levels
are within the range associated with ozone. Hence, the greater responsiveness of
plants in the exclusion studies does not appear to be the result of greater absolute
differences in UV-BBE levels between their treatments. A more likely explana-
00 TABLE 4.1. Summary of some recent studies examining the influence of UV-B exclusion on plant performance.
0-
Treatments:
% ambient
UV-BBE
(increase in Leaf size, UV-B
% ambient Biomass Total leaf leaflbranch absorbing
Author Species UV-BBE) total Height area production compounds Photosynthesis Reproduction
Deckmyn Phaseolus 78% vs. Reduced 13% Reduced NS (Pn) Increased pod mass
and Impens vulgaris 86% in vegetative 19% in 15%
1995 (8%) stage, but vegetative
increased 5% stage
in reproductive
stage
Searles Five tropical 0% vs. Reduced 19% in Reduced Reduced leaf Increased NS (chi fl)
et al. 1995 forest 92% 1 of 5 species to 20% length to in 4 of 5
species (92%) in 30f 5 29% in 2 of species
species 5 species
Ballare Datura 4% vs. Reduced 9% Reduced Reduced
et al. ferox 78% 29% hypocotyl
1996 (74%) up to 29%
Mark Zea mays, 88% vs. NS, Reduced NS NS Slower flower
et al. 8 cvs =100% but reduced in 6 of 8 (reduced development,
1996 (12%) in spring cultivars in spring) seed yield
reduced 28%
Tosserams Four native 10% vs. NS NS NS Increased NS (Pn)
et al. grassland 100% in 3 of 4
1996 species (90%) species
Krizek Cucumis 13% vs. Reduced 28% Reduced Reduced NS
et al. sativus, 75% 21% 26%
1997 4 cvs (62%)
Schumaker Populus <1% vs. NS NS NS Leaves thinner Increased Reduced Pn
et al. trichocarpa, =90% in 1 clone
1997 2 clones (89%)
Deckmyn Bromus 0% vs. Increased 15 % Reduced 7% NS Increased tiller NS Increased seed
and Impens catharticus 80% in summer in spring, production, mass 63% per
1998 (80%) increased 35% plant, 16% per
6% in seed, and seed
summer production 45%
Krizek Lactuca 9% vs. Reduced 35% Reduced Reduced leaf Increased
et al. sativa 87% expansion
1998 (78%) and production
Day Two native 22% vs. Reduced leaf NS NS (Pn) Faster development,
et al. Antarctic 87% length, 24%, 11 %-52% more
1999 vascular (65%) and leaf and structures reached
species branch maturity
production,
17%-35%
Mazza Hordeum 5% vs. Reduced 18% Reduced leaf Increased Reduced grain
et al. vulgare =90% length, 9% mass, 21%;
1999a (85%) and tiller reduced spike
production, production,
17% 17%
Searles One moss and 20% vs. NS NS NS Reduced spikelet
et al. 5 vascular 90% length in 1 of 2
1999 plant (70%) Carex spp., but
species NS on seed
production!
viability
NS, no significant difference (p > 0.05); Pn, net CO 2 uptake; chI fl, chlorophyll fluorescence; CV, cultivar.
Response refers to plants under the higher, near-ambient UV -B.
In studies in which more than two UV-B levels were examined, the results summarized are based on a comparison of the two most extreme UV-B-Ievel treatments.
UV-BBE refers to biologically effective UV-B based on the generalized plant damage action spectrum normalized to 300 nm (Caldwell 1971), where available. The %UV-
BBE under near-ambient controls was estimated when not available.
00
-..J
00
00
TABLE 4.2. Summary of some recent studies examining the influence of a modulated UV-B supplements on plant performance.
Treatment:
supplement as
% increase of
ambient UV-BBE Leaf size, UV-B-
(% ozone depletion Biomass Total leaf leaflbranch absorbing
Author Species simulation) total Height area production compounds Photosynfhesis Reproduction
Caldwell Glycine + 100% ambient NS NS Increased NS (chi fl)
et al. max UV-BBE
1994 (36% ozone
depletion)
Sullivan Glycine +60% ambient NS NS NS Increased (Oz NS (seed
et aI. max UV-BBE evolution) production
1994 (25% ozone or seed mass
depletion) per plant)
Day Pisum +65% ambient NS NS NS NS Increased
et al. sativum UV-BBE % in
1996 (24% ozone adaxial
depletion) epidermis
Kim Oryza + 130% ambient NS NS, but NS NS, but tiller NS NS (13C/IZC) NS (panicle
et aI. sativa UV-BBE tended to production production
1996a (38% ozone be reduced tended to be or seed mass
depletion) early in reduced early per plant)
season in season
Mepsted Pisum +23% ambient Reduced Reduced NS NS (Pn, chi fl) Reduced total pod
et aI. sativum UV-B BE total stem number of and seed mass
1996 (4 cvs) (11% ozone 9% stems, 5% and number
depletion) per plant by
10%-12%
Newsham Quercus + 30% ambient NS Leaves
et al. robur UV-BBE thinner,
1996 (18% ozone NS shoot
depletion) length
Ryan Petunia +25% ambient Reduced Reduced Reduced Tended to NS (chi fl) Delayed
et al. spp UV-BBE leaf increase flowering
1998 (3 lines) width (some
dates)
Allen Pisum + 30% ambient NS NS Increased NS (Po, chi fl)
et al. sativum UV-BBE
1999 (18% ozone
depletion)
Stephen Hordeum +48% ambient NS NS in chi fl NS (grain yield)
et al. vulgaris UV-BBE Hordeum, sometimes
1999 (4 cvs), (15% ozone increased reduced
Pisum depletion) in Pisum in Pisum
sativum
(2 cvs)
NS, difference not significant (p > 0.05); Po, net CO 2 uptake, chI fl, chlorophyll fluorescence; CV, cultivar.
Response refers to plants under the higher UV-B level.
In studies in which more than two UV-B levels were examined, the results summarized are based on a comparison of the two most extreme UV-B levels.
UV-BBE refers to biologically effective UV-B based on the generalized plant damage action spectrum normalized to 300 nm (Caldwell 1971), where available.
00
v:>
90 Thomas A. Day
tion is that plants are more responsive to increases in UV-B when added to rel-
atively low, subambient levels of UV-B (exclusion studies) than when added
to relatively high, ambient levels of UV-B (supplementation studies). On aver-
age, filters in the exclusion studies reduced UV-BBE levels to 21 % of ambient
UV-BBE levels. Target compounds and mechanisms may become saturated at
ambient levels of UV-B, and at higher supplements further responses may be in-
significant or difficult to detect.
General Plant Responses

Increases in UV-B-Absorbing Compounds
The most consistent response observed in the studies in Tables 4.1 and 4.2, col-
lectively, was an increase in leaf concentrations of soluble UV -B-absorbing com-
pounds. Similarly, Searles, Flint and Caldwell (manuscript) surveyed 103 papers
that examined the influence of outdoor UV -B supplements (both squarewave and
modulated) and found that of the 10 response variables they assessed, the most
common treatment effect was as an increase in leaf UV -B-absorbing compounds.
Reproduction
Up to this point UV-B effects on reproductive output have not been addressed
because reproduction responses may require special considerations compared to
vegetative growth or total biomass production. Obviously, an assessment of UV-
B effects on plant performance should also consider reproductive output, which
can be particularly relevant in terms of the future success of wild populations or
the economic yield of many crops. Among the exclusion studies, three of six
studies detected an apparent improvement in reproductive output whereas the
other three studies found some evidence for a reduction in reproductive success.
Among the modulated supplement studies, two studies detected a reduction in
reproductive output while four studies found no effects on reproduction .. These
differences suggest that reproductive responses are species- and system specific.
Some of these differences may also result in part from the many different indices
used to assess reproductive output. Further complications arise because UV-B
may alter plant phenology and seed development such that the harvest dates
and environmental conditions during an experiment have a critical bearing on
the conclusions one makes regarding reproductive success. In summary, while
UV-B levels sometimes influence reproductive output, any generalizations seem
premature because of the variability in findings and complex nature of this
response.
Reduced Leaf Area

Detrimental responses observed in the exclusion studies were reductions in leaf
elongation, along with branching or tillering. Although far fewer responses were
observed in the modulated supplemental UV -B studies, branching or tillering was
reduced in two of four studies examining this parameter. Taken collectively, re-
sults from these studies suggest that reductions in leaf size and branching are the
most consistently observed responses associated with impaired plant perfor-
mance. The evidence also suggests that these reductions in leaf elongation or leaf
size are not compensated for by increases in leaf production and appear to trans-
late into reductions in whole-plant leaf area, whole-canopy assimilation, total bio-
mass, and hence impaired performance. Several mechanisms have been proposed
that might explain reductions in leaf size and area, including those associated
with (1) induction of wall-bound UV-B-absorbing compounds, (2) oxidative dam-
age, (3) DNA damage, and (4) reductions in net photosynthesis per unit leaf area.
What follows is a discussion of these various responses and mechanisms, aimed
primarily toward their possible role in UV-B-induced reductions in leaf size.
Response Mechanisms
UV-B-Absorbing Compounds
As mentioned, the most consistent overall response to higher UV-B levels
recorded in Tables 4.1 and 4.2 was an increase in leaf concentrations of soluble
UV-B-absorbing compounds. These compounds have received much attention,
in part because of their strong UV absorbance and their presumed protective
screening function. These compounds may also serve other protective functions
as antioxidants, chemical defenses against herbivores and pathogens, molecular
signals involved in the induction of nitrogen-fixing bacterial nodulation (Gyor-
gypal et al. 1991), and vesicular-arbuscular mycorrhizal fungi establishment
(Rhlid et al. 1993), and may also act as allelopathic compounds (Klein and Blum
1990).
The number of UV-B-absorbing compounds is vast, and although they have
received considerable attention, many specifics regarding their modes of induc-
tion, location, and their significance in UV-B protection are not completely un-
derstood. The predominant UV-B-absorbing compounds in higher plants are
thought to be phenylpropanoids produced by the shikimate pathway, often in
combination with the acetate-malonate pathway. UV-B, as well as UV-A and
visible light, can induce the expression of key enzymes such as PAL (phenyl-
alanine ammonia-lyase) and CHS (chalcone synthase) in these pathways (Chap-
pell and Hahlbrock 1984; Beggs and Wellmann 1994). These pathways are re-
sponsible for the synthesis of several classes of phenolic compounds including
hydroxycinnamic acids, flavonoids, lignins, and tannins. Among the most com-
mon phenolics in higher plant leaves, and those that have received the most at-
tention with respect to UV-B because of their strong attentuation of UV-B and
putative protective screening function, are the flavonoids and the hydroxycin-
namic acids, some of which serve as flavonoid precursors. Among the most wide-
spread of the hydroxycinnamic acids are p-coumaric, caffeic, ferolic, and sinapic
acid (Ibrahim and Barron 1989). These acids usually occur in conjugated forms,
often as esters.
92 Thomas A. Day
Regarding the flavonoids, there are several subclasses, but the three most wide-
spread and abundant are probably the anthocyanins, flavonols, and flavones. An-
thocyanins typically absorb much more strongly in the blue than in the UV-B
and are typically not nearly as effective UV-B screeners as most flavonols and
flavones, which typically absorb strongly in the UV-B and lower UV-A and are
quite transparent across the visible waveband (Beggs and Wellman 1994). Some
covalently modified anthocyanins, such as those esterified (Tevini, Braun and
Fieser 1991) or acylated (Woodall and Stewart 1998) with cinnamic acids, do
absorb more effectively in the UV-B. However, anthocyanins typically occur in
much lower leaf concentrations than other UV -B-absorbing compounds, and they
represent products of flavonal precursors (Brandt, Giannini and Lercari 1995).
Hence, the importance of anthocyanins as UV-B-screening compounds in most
leaves remains questionable (Beggs and Wellman 1994; Brandt, Giannini and
Lercari 1995; Chalker-Scott 1999). They might serve in other UV-B protection
roles such as antioxidants, although evidence to date for this role does not ap-
pear very conclusive (Chalker-Scott 1999). The flavonols and flavones often oc-
cur in conjugated forms produced by various substitutions, particularly as O-gly-
cosides, leading to more than 1600 variants of their basic 15-C skeleton (Markham
1982; Harborne 1989; Stafford 1990). Many flavonols and flavones tend to ac-
cumulate and occur in high concentrations in the epidermal layer ofleaves, mak-
ing them well suited to screen UV-B and reduce doses in the leaf mesophyll.
However, whether the increases in their concentrations observed under higher
UV-B levels in the field lead to improved leaf UV-B screening that mitigates
damage seems open to debate.
Do Increases in UV-B-Absorbing Compounds Improve

Leaf UV-B Screening and Mitigate Damage?
Most field studies that have assessed the concentration of UV -B-absorbing com-
pounds used whole-leaf extraction in an acidified solvent. The UV-B absorbance
(typically at 300 nm) of this extract is taken as an estimate of the concentration
ofUV-B-absorbing compounds. It is often inferred that greater UV-B absorbance
of these extracts translates into shallower penetration of UV-B into the leaf and
lower epidermal UV-B transmittance. Hence, greater UV-B absorbance of these
extracts in response to higher UV-B level is often interpreted as a protective
mechanism by way of reducing UV -B fluxes reaching sensitive targets inside
the leaf.
There is some evidence that increases in these compounds improves leaf UV
screening. On UV-B exposure of plants in growth chambers, increases in solu-
ble extract absorbance have been correlated with reductions in epidermal UV-B
transmittance in leaves of Brassica nap us (Cen and Bornman 1993; Alenius, Vo-
gelmann and Bornman 1995) and Hordeum vulgare (Reuber, Bornman and Weis-
senbock 1996). Some evidence for the protective function of these compounds
comes from another growth chamber study (Tevini, Braun and Feiser 1991) in
which increases in these compounds brought about by preexposure to UV-B ap-
peared to reduce the severity of photosynthetic inhibition when plants were sub-
sequently challenged with UV-B. Although UV-B exposure in the former stud-
ies resulted in relatively large increases in absorbing compound concentrations,
the ensuing reductions in epidermal transmittance were rather small. Whether the
more subtle increases in UV-B-absorbing compound concentrations typically
found in response to UV -B in field studies also correlates to reductions in epi-
dermal transmittance is unclear. For example, Sullivan et al. (1996) found little
correlation between UV-B-absorbing concentrations and epidermal transmittance
in Pinus taeda and Liquidambar styraciflua seedlings grown under different
UV -B levels in the greenhouse and field. Pinus taeda was more sensitive to en-
hanced UV -B, but its epidermal transmittance was much lower ( < 1%) than that
of Liquidambar styraciflua (10%-20%).
In a survey of several species growing outdoors under ambient solar regimens,
species with greater soluble extract absorbance tended to have lower epidermal
UV-B transmittance (Day 1993; Day, Howells and Rice 1994). However, the
variability in this relationship was quite large. Indirect evidence for their role in
protection via screening UV-B comes from studies that have found that mutants
deficient in some aspects of phenylpropanoid metabolism are more sensitive to
UV-B (Li et al. 1993; Harlow et al. 1994; Lois and Buchanan 1994; Landry,
Chapple and Last 1995; Orrnrod, Landry and Conklin 1995; Rao and Ormrod
1995; Sheahan 1996; Reuber, Bornman and Weissenbock 1996). However, there
is little evidence directly linking the greater sensitivity of these mutants to poorer
UV -B screening. In some cases the greater sensitivity of these mutants appears
to involve deficiencies in more than simply flavonoid production and improved
screening, which is not surprising given the diverse types of compounds syn-
thesized from phenolics and their suspected functions (Harborne 1989; Stafford
1990; Waterman and Mole 1994). Hence, in some cases the evidence from these
mutants for the critical role of flavonoids in UV-B screening and protection has
been questioned (Sheahan 1996; Fiscus et al. 1999).
The idea that increases in UV-B-absorbing compounds in response to higher
UV-B in the field is a protective response that improves UV-B screening and re-
duces damage may be overstated. Although many of these compounds strongly
absorb UV-B, this does not necessarily mean that increases (particularly in bulk-
leaf soluble extracts) provide significantly more effective UV -B screening of tar-
gets in the leaf. One problem with this assumption is that the targets of UV-B
damage are poorly understood, particularly under realistic outdoor UV-B levels,
which makes an assessment of protection or damage difficult. For example, if
significant targets are located near the leaf surface in the epidermis, an increase
in vacuole or mesophyll screening compounds may do little to protect these
targets.
The assumption that bulk-leaf soluble extract absorbance is positively corre-
lated with in vivo leaf UV-screening effectiveness is also oversimplistic for sev-
eral reasons. The nonlinear nature of the idealized relationship between ab-
sorbance and transmittance, along with the optical complexity of leaves, makes
it difficult to predict in vivo radiation levels and gradients (Vogelmann 1994).
94 Thomas A. Day
Their in vivo absorption spectra may also vary considerably from their in vitro
absorption spectra because of differences in pH and polarity of solvents (Shaath
1990). UV-B-absorbing compounds are not distributed homogeneously within
the leaf, either with depth or laterally along a leaf, and typically are differentially
compartmentalized within leaves. Thus, a comparison of UV-B absorbance of
soluble whole-leaf extracts with in vivo epidermal leaf transmittance of several
species has shown that leaves of different species having nearly identical ab-
sorbance values can vary by more than 40% in their UV-B epidermal transmit-
tance (Day 1993). Additionally, in some cases the relationship between soluble
extract absorbance and epidermal transmittance spectra within an individual leaf
is counterintuitive, in that high soluble extract absorbance at a given UV wave-
length may not necessarily correspond to low transmittance (Day, Howells and
Rice 1994).
Another reason for the discrepancies between leaf screening effectiveness and
extract absorbance stems from the fact that some UV-B-absorbing phenyl-
propanoids occur bound to cell walls, and these insoluble compounds are not ex-
tracted in the standard acidified solvent protocol. For example, ferulic and cin-
namic acid occur not only in soluble form in the vacuole but also esterified to
the cell wall in some species. Accumulation of these acids, as well as other phe-
nolics, in cell walls appears to be particularly common in some monocots (es-
pecially grasses), in conifers, and among some dicots in the Caryphyllales (Har-
ris and Hartley 1976, 1980; Hartley and Harris 1981; Strack et al. 1988, 1989;
Schnitzler et al. 1996; Harris et al. 1997; Litchenthaler and Schweiger 1998;
Hoque and Remus 1999; Fishbach et al. 1999). Conceivably, other wall-bound
phenylpropanoids derivatives such as lignin may also be effective UV screeners.
In species that contain small amounts of wall-bound UV-B-absorbing compounds,
UV-B penetration through the anticlinal wall is probably the dominant pathway
allowing UV-B past the epidermis into the mesophyll (Day, Martin and Vogel-
mann 1993). Thus, small increases in these wall-bound compounds could lead
to disproportionately large reductions in epidermal UV-B transmittance that
would go undetected in standard extraction protocols.
Conversely, because of the disproportionally large amounts of UV -B that may
pass through the anticlinal walls in these species, large changes in the soluble
pool of UV-B-absorbing compounds (using the standard protocol) might have
relatively little effect on epidermal UV-B transmittance. For example, a
flavonoid-deficient mutant of Hordeum vulgare that was only capable of pro-
ducing 7% of the total soluble UV-B-absorbing compounds of its mother line
was still quite effective at attenuating UV -B in its leaf epidermis, possibly the
result of screening by insoluble wall-bound phenylpropanoids (Reuber, Bornman
and WeissenbOck 1996). These complexities would explain why researchers have
been unable to correlate the field UV-B sensitivity of species or populations to
differences in concentrations of bulk soluble UV-B-absorbing compounds
(Barnes, Flint and Caldwell 1987; Musil 1995; Sullivan et al. 1996). In summary,
increases in soluble UV-B-absorbing compounds observed in many species un-
der higher UV -B levels suggest a widespread response. In the case of plants that
are not acclimated to outdoor spectral regimens, such as those growing indoors
or young seedlings growing outdoors, these increases could improve UV -B
screening and protection. For acclimated plants outdoors, however, whether these
increases translate into appreciable reductions in UV -B levels at target sites within
foliage is unclear.
Increases in Wall-Bound UV-B-Absorbing Compounds

May Constrain Leaf Expansion
The induction of these absorbing compounds probably elicits several other pro-
cesses, some of which may be interpreted as protective, and others of which might
even be responsible for reductions in leaf elongation and growth. Before con-
sidering other protective roles that phenylpropanoids may play in reducing UV-
B damage, one mechanism that might explain reductions in leaf elongation in-
volves UV-B induction of wall-bound phenylpropanoids. Some wall-bound
phenylpropanoids such as ferulic acid can increase in some species in response
to UV-B and may ultimately be responsible for constraining cell elongation and
growth (Liu and McClure 1995; Liu, Gitz and McClure 1995). Fry (1986) sug-
gested that ferulic acid in cell walls can be oxidized by peroxidases to produce
dehydrodiferulic acids, such as diferulic acid, which form side chains on wall
polysaccharides. These side chains or cross-links in the cell-wall matrix poly-
saccharides can decrease cell-wall extensibility, constraining cell expansion and
ultimately limiting leaf elongation and growth. For example, increases in wall-
bound ferulic acid were correlated with reduced growth rates and declines in cell-
wall extensibility in oat (Avena sativa) coleoptiles (Kamisaka et al. 1990), and
these were also correlated with greater PAL activity in wheat (Triticum aestivum)
coleoptiles (Wakabayashi, Hoson and Kamisaka 1997). Ferulic acid polysaccha-
ride cross-linking has also been observed in the cell walls of wheat internodes
(Lam, Iiyama and Stone 1994), which could explain reductions in plant height.
It is currently unclear how effective realistic enhancements of outdoor levels
of UV-B are in eliciting increases in wall-bound pools of ferulic acid or other
phenylpropanoids. However, in a series of growth chamber and greenhouse ex-
periments with barley, Liu and McClure (1995) and Liu, Gitz and McClure (1995)
found that enhanced UV-B increased PAL activity as well as wall-bound ferulic
acid esters in the leaf epidermis. Fischbach et al. (1999) examined concentrations
of phenylpropanoids in Norway spruce (Picea abies) growing outdoors, and while
they found that wall-bound concentrations of p-coumaric acid and kaempferol
3-0-glucoside were higher in needles under ambient UV-B than under UV-B-
absorbing filters, no such effect was apparent in wall-bound concentrations of
ferulic acid. Sullivan et al. (1996) suggested that this mechanism might explain
observations that enhanced UV-B leads to shorter needles and a thicker epider-
mis in Pinus taeda, which would explain why these changes are observed in spite
of the fact that nearly all the incident UV-B is absorbed by the epidermis and
little reaches the mesophyll in these needles.
96 Thomas A. Day
Reductions in leaf area induced by UV-B often involve reductions in epider-

mal cell size (Ballare, Barnes and Kendrick 1991; Ballare, Barnes and Flint 1995;
Ballare et al. 1995; Liu, Gitz and McClure 1995; Nogues et al. 1998), as well as
cell number (Tevini and Iwanzik 1986; Staxen, Bergounious and Bornman 1993;
Logemann et al. 1995; Nogues et al. 1998). Reductions in cell size would cer-
tainly fit with the previous hypotheses ascribing UV -B-induced reductions in leaf
size to reduced cell-wall extensibility via more hydroxycinnamic acid cross-links.
However, reductions in cell number or division, at least in the absence of re-
ductions in cell size, seem hard to ascribe to this mechanism. Nogues et al. (1998)
attributed UV-B-induced reductions in pea leaf size to reductions in cell number
more so than cell size because of the larger effect on the former. Possible mech-
anisms responsible for reduced cell division include oxidation of tubulin, which
could delay microtubule formation (Staxen, Bergounious and Bornman 1993), or
transcriptional repression of histone synthesis (Logemann et al. 1995). In the case
of seedling elongation, another mechanism appears involved in some UV-B-
induced reductions in elongation rates. Seedling exposure to UV-B indoors can
cause rapid, reversible reductions in hypocotyl elongation, which appears to in-
volve signals from an unidentified photoreceptor in the cotyledons (Ballare,
Barnes and Flint 1995; Ballare et al. 1995; Barnes, Ballare and Caldwell 1996).
This response precedes any accumulation of soluble UV -B-absorbing compounds
and could serve to minimize seedling damage from UV -B until these compounds
have accumulated.
Oxidative Damage
An area that has received increasing attention is the role of oxidative damage in
plant UV-Bproteins responses, as well as the role of phenylpropanoids as an-
tioxidants. Several laboratory studies have shown that UV-B exposure can lead
to increases in reactive oxygen species, and these may in tum react with and
damage membrane lipids, pigments, proteins, and nucleic acids (Kramer et al.
1991; Malanga and Puntarulo 1995; Landry, Chapple and Last 1995; Takeuchi
et al. 1995; Hideg and Vass 1996; Conklin, Williams and Last 1996; Dai et al.
1997; Hideg et al. 1997; Mackerness et al. 1998). Further evidence for UV-B-
induced free-radical production comes from increased ultraweak light emission,
which is indicative of oxidative damage (Cen and Bjorn 1994; Levall and Born-
man 1993). Several different enzymatic and nonenzymatic oxidative stress de-
fense systems operate in plants, and UV-B exposure in the laboratory can in-
crease the activity of several of these systems (Willekens et al. 1994; Landry,
Chapple and Last 1995; Malanga and Puntarulo 1995; Kim et al. 1996b; Rao,
Paliyath and Ormrod 1996; Takeuchi et al. 1996; Hideg and Vass 1996; Dai et
al. 1997; Mackerness et al. 1998). Although the activity of some of these sys-
tems can increase, the activity of others declines, and it is not clear which are
most important with respect to UV-B exposure.
Although these laboratory studies have clearly shown that UV-B has the po-
tential to cause oxidative stress, the significance of UV -B-induced oxidative dam-

age and antioxidant activity under field conditions is less clear. Kim et a1. (1996b)
found increases in antioxidant enzyme levels in rice in laboratory experiments,
but they were unable to detect this increase under UV-B supplements in the field
(Kim et a1. 1996c). In a field exclusion study with barley, Mazza et al. (1999a)
found that plants under ambient UV-B had higher activities of the H202-
scavenging enzymes catalase and ascorbate peroxidase but not superoxide dis-
mutase. In contrast, Taulavuori et a1. (1998) sampled Vaccinium myrtillus dur-
ing its seventh growing season of supplemental UV -B exposure and did not de-
tect any effects on concentrations of ascorbate or glutathione or on activities of
ascorbate peroxidase or glutathione reductase.
Phenylpropanoids as Antioxidants
Several in vitro studies have shown that phenylpropanoids such as hydroxycin-
namic acid derivatives and flavonoids can act as antioxidants (Torrell, Cillard
and Cillard 1986; Husain, Cillard and Cillard 1987; Rice-Evans 1995; Bors et
a1. 1990; Bors, Michel and Schikora 1995; Castelluccio et a1. 1995; Yamasaki,
Uefuji and Sakihama 1996). In support of their antioxidant role in vivo, Ya-
masaki, Sakihama and Ikehara (1997) found that flavonols isolated from field-
grown plants could act as H20 2 scavengers, particularly in conjunction with per-
oxidase. Recent studies have also shown that in addition to a general increase in
phenylpropanoid concentrations, UV -B exposure changes the relative amounts
of flavonoids, favoring flavonols or flavones with additional hydroxyl groups
that may be more effective free radical scavengers. Increases in the relative
amounts of flavonols and flavones with additional hydroxyl groups under en-
hanced UV-B have been detected in Brassica nap us (Bornman et a1. 1997), bar-
ley (Liu, Gitz and McClure 1995; Reuber, Bornman and WeissenbOck 1996),
birch (Lavola 1997), rice (Markham et al. 1998a), a liverwort (Markham et al.
1998b), and petunia (Ryan et a1. 1998).
Although these flavonoids typically are no more effective at absorbing UV-B
than their less hydroxylated counterparts (Mabry, Markham and Thomas 1970),
they may be more effective free-radical scavengers by means of differences in
the number and location of their hydroxyl groups (Husain, Cillard and Cillard
1987; Montesinos et a1. 1995; Yamasaki, Sakihama and Ikehara 1997). It has
also been speculated that they might be more effective at safely dissipating UV
energy (Ryan et a1. 1998). While the role of flavonoids as antioxidants seems
reasonable, it should be noted that this depends on the redox potentials of the
participating compounds (Bors, Michel and Schikora 1995). Thus, although many
flavonoids may be effective free-radical scavengers, others have relatively high
redox potentials and could conceivably act as oxidants rather than reductants in
vivo (Bornman et a1. 1997). Further research is needed to assess the role of ox-
idative damage in field responses to UV-B as well as the importance offlavonoids
in mitigating this damage in vivo.
98 Thomas A. Day
DNA Damage
Several indoor studies have shown that UV-B can damage DNA and that these
lesions appear predominantly in the form of cyclobutane pyrimidine dimers
(CPDs) and pyrimidine-pyrimidinone (6,4) dimers (6,4-photoproducts) (Britt
1995, 1996; Sutherland et al. 1996; Taylor et al. 1996; Kang, Hidema and Ku-
magai 1998). It is unclear whether one of these dimers is more important or sig-
nificant than the other regarding plant responses to UV-B; mutants deficient in
CPD repair (Hidema et al. 1997) or in 6,4-photoproduct repair (Britt et al. 1993)
are both sensitive to UV-B. Repair of CPDs and 6,4 photoproducts can be ac-
complished by both photoreactivation ("light" repair) and excision or "dark" re-
pair (Pang and Hays 1991; Chen, Mitchell and Britt 1994; Britt 1995, 1996).
Photoreactivation requires photolyase enzymes that are activated by UV-A or
blue light (350-450 nm), and possibly UV-B (Pang and Hays 1991). Photoreac-
tivation is considered less costly than excision repair because photoreactivation
relies on a single enzyme (photolyase), whereas excision repair relies on multi-
ple enzymes for incision, excision, resynthesis, and ligation, and photoreactiva-
tion uses UV-A or visible radiation as an energy source for catalysis (Sutherland
et al. 1996). Photoreactivation also reverses DNA damage in an error-free man-
ner. The kinetics of photoreactivation are faster than those of excision repair, and
photoreactiviation is considered to be the main pathway for CPD repair in most
plant species examined to date (Pang and Hays 1991; Quaite et al. 1994; Can-
non, Hedrick and Heinhorst 1995; Taylor et al. 1996; Hidema et al. 1997; Sta-
pleton, Thornber and Walbot 1997; Hada et al. 1999). In contrast, 6,4 photo-
products tend to be repaired more efficiently than CPDs by excision repair (Britt
1995).
The role of nonspecific DNA damage in explaining plant responses to UV-B
is unclear. Nonspecific damage in the form of these dimers sometimes accom-
panies reductions in gene expression of photosynthetic proteins (Jordan 1996;
Taylor et al. 1996; Mackerness et al. 1998). However, recent evidence suggests
that signal transduction in these cases may be mediated by active oxygen species
rather than nonspecific DNA damage (Mackerness et al. 1997, 1998). Further-
more, UV-B-induced reductions in photosynthesis are rarely observed under re-
alistic field doses. UV-B-induced upregulation of PAL and CHS (Frohnmeyer,
Bowler and Schafer 1997) can also occur independently of nonspecific DNA
damage.
Regarding the prevalence and significance ofUV-B-induced DNA damage and
repair under field conditions, Stapleton, Thornber and Walbot (1997) found de-
tectable CPD levels in maize (Zea mays) growing under natural sunlight and also
noted a slight increase in CPD levels over the course of the day. They also found
that CPD levels did not accumulate over the growing season, which they attrib-
uted to very efficient photoreactivation repair. Enhanced UV-B levels may not
lead to accumulation of damage products through the growing season but could
conceivably lead to greater reliance on more costly excision repair because pho-
toreactivation, which is limited to diurnal periods, may not be able to completely
repair greater amounts of damage. In two outdoor exclusion studies in Argentina,

BalIan! and coworkers demonstrated that CPD levels can increase in response to
ambient UV-B levels. Daturaferox (a summer annual) and barley grown under
near-ambient UV-B had higher levels of CPDs than plants growing under UV-
B-absorbing filters (Ballare et al. 1996; Mazza et al. 1999a). Ballare et al. (1996)
also excluded different amounts of ambient UV -B, approximating 0%, 25%, 75%,
and 100% of ambient levels, and found that CPD burden in Datura ferox in-
creased with increasing UV-B level, although CPD levels tended to level off
or saturate as UV-B levels approached ambient. In both these studies, ambient
UV-B levels caused reductions in plant growth (see Table 4.1) in conjunction
with greater CPD burdens. Although these results provide correlative evidence
that nonspecific DNA damage may be partly responsible for UV-B-induced
growth reductions, the physiological consequences of DNA damage or the costs
of repair, in terms of plant performance, have yet to be established.
Reductions in Photosynthesis
There is ample evidence from indoor studies that UV-B can impair all the main
processes of photosynthesis, including stomatal diffusion of CO 2 into the leaf,
CO 2 fixation and associated Calvin cycle reactions, and phosphorylation and as-
sociated photochemistry in the thylakoid membranes (see Bornman 1989; Tevini
1993; Teramura and Sullivan 1994; Jordan 1996). PhotosYJtem II (PSII) has of-
ten been demonstrated to be the most sensitive component in thylakoid mem-
branes, leading to suggestions that PSII dysfunction is the main mechanism re-
sponsible for UV-B-induced reductions in photosynthetic rate (Bornman 1989;
Melis, Nemson and Harrison 1992; Tevini 1993; Teramura and Sullivan 1994;
Jansen et al. 1996; Spetea, Hideg and Vass 1996; Vass et al. 1996; Babu et al.
1999). However, the idea that PSII sensitivity explains UV-B induced reductions
in photosynthetic rates has been questioned (Bjorn 1996; Allen et al. 1997; Allen,
Nogues and Baker 1998; Baker, Nogues and Allen 1997). The majority of evi-
dence for high PSII sensitivity comes from indoor studies employing low levels
of PAR, which can greatly exaggerate photosynthetic sensitivity (Adamse and
Britz 1992; Mackerness et al. 1996; Jordan 1996). Many studies have also found
simultaneous impairments in several other photosynthetic processes, in addition
to PSII activity (Strid, Chow and Anderson 1990; Huang et al. 1993; He et al.
1993, 1994; Day and Vogelmann 1995; Allen et al. 1997), and reductions in CO 2
assimilation rates can precede or occur in the absence of damage to PSII (Mid-
dleton and Teramura 1993; Nogues and Baker 1995; Baker, Nogues and Allen
1997). In contrast to the idea that PSII is the primary UV-B target, results from
some recent studies that systematically examined various potential limitations to
photosynthesis suggest that in vivo reductions in photosynthesis more likely in-
volve impairment of the Calvin cycle, leading to reductions in rubisco activity,
as well as increases in stomatal limitations (Nogues and Baker 1995; Allen et al.
1997; Baker, Nogues and Allen 1997).
The identity of the primary target for UV -B damage to photosynthesis may
100 Thomas A. Day
very well be a moot point because evidence is accumulating that photosynthesis

is quite insensitive to UV-B when realistic doses are applied under field condi-
tions. Reductions in leaf CO2 assimilation rates attributable to UV-B are very
uncommon under more realistic outdoor spectral regimens. Fiscus and Booker
(1995) and Allen, Nogues and Baker (1998) concluded that photosynthesis in ac-
climated plants growing outdoors does not appear to be at risk from current or
future levels of UV-B. Results from the studies in Tables 4.1 and 4.2 support
this contention. Of the seven exclusion studies and five modulated supplement
studies that examined photosynthetic parameters, reductions in photosynthetic
parameters under higher UV-B were only detected in one exclusion study (Schu-
maker et al. 1997) and one modulated supplement study (Stephen et al. 1999).
Schumaker et al. (1997) found lower CO 2 assimilation rates but no affects on
PSII activity, while Stephen et al. (1999) found lower PSII activity, but only on
occasional sampling dates. In neither case did these translate into reductions in
leaf area or biomass production. When reductions in biomass, growth, or leaf
size were detected under higher levels of UV -B in the exclusion studies in Table
4.1, they occurred in the absence of any detectable reductions in photosynthetic
parameters. This result reiterates the idea that changes in morphology, growth,
or biomass in response to UV-B typically occur in the absence of changes in
photosynthetic rates per unit leaf area (Beyschlag et al. 1988; Barnes, Flint and
Caldwell 1990; Adamse and Britz 1992; Searles, Caldwell and Winter 1995; Bal-
lare et al. 1996; Gonzalez et al. 1996, 1998; Allen, Nogues and Baker 1998; Hunt
and McNeil 1998).
What Traits Might Confer Tolerance

or Sensitivity to UV-B?
Species as well genotypes within species can differ substantially in their response
to UV-B, as illustrated in several of the studies in Tables 4.1 and 4.2. However,
explanations as to why certain species or genotypes are more responsive or sen-
sitive to UV-B have been elusive. In other studies, attempts to relate respon-
siveness to soluble leafUV-B-absorbing compound concentrations (Barnes, Flint
and Caldwell 1987; Musil 1995; Sullivan et al. 1996) or epidermal UV-B trans-
mittance (Caldwell, Robberecht and Nowak 1982; Sullivan et al. 1996) have
found little evidence for the idea that higher absorbing compound concentrations
or more effective epidermal screening confer less responsiveness or sensitivity
to UV -B. Generalizations about the sensitivity of different plant growth forms
have also proved elusive. Barnes, Flint and Caldwell (1990) found monocots
tended to be more responsive to enhanced UV-B than dicots, whereas Musil
(1995) found the opposite trend. Although the epidermis of mature evergreen fo-
liage, particularly conifer needles, appears to be very effective at attenuating
nearly all incident UV-B (Day, Vogelmann and DeLucia 1992; Day 1993), ever-
greens generally appear no less responsive or sensitive to UV-B and in some
cases they appear more responsive (Johanson et al. 1995a,b; Sullivan et al. 1996;
Bjorn et al. 1998). For example, Sullivan et al. (1996) found that the conifer Pi-
nus taeda was more sensitive to enhanced UV-B than the deciduous tree Liq-
uidambar styraciflua, even though epidermal transmittance was much lower in
the conifer « 1%) than in the deciduous species (20%). Hence, the relative sen-
sitivity of plants to UV-B may depend in part on their UV-B-screening effec-
tiveness, but additional factors, possibly involving the effectiveness of antioxi-
dant and DNA damage repair systems, must also playa role.
Interactions with Other Trophic Levels

Litter Decomposition
The possible influence of enhanced UV-B on biogeochemical cycles has been
reviewed by Zepp, Callaghan and Erickson (1998). Few studies have directly ex-
amined this issue, and most of these have addressed this in the context of litter
decomposition. Gehrke et al. (1995) examined the indirect effect of plant UV-B
exposure on subsequent leaf litter decomposition. They found that the decom-
position rate (mass loss) of Vaccinium leaves that had developed under enhanced
UV-B was slower and was correlated with lower concentrations of cellulose and
higher concentrations of tannins. This apparent reduction in litter quality might
explain the lower microbial respiration rates they observed. Newsham et al.
(1999) examined the indirect effects of UV-B exposure on Quercus robur litter
decomposition by growing saplings under enhanced UV -Band monitoring the
subsequent decomposition of these leaves in a forest floor. In contrast to Gehrke
et al. (1995), they found that decomposition rate (mass loss) of litter from en-
hanced UV -B plants was accelerated and had greater basidiomycete fungi colo-
nization, which may have been associated with lower lignin:N ratios in these
leaves.
Moody, Coop and Paul (1997) found no differences in the decomposition rates
or in the initial concentrations of water-soluble phenolics and in N or C:N ratios
in leaves collected from Rubus chamaemorus grown under different UV-B lev-
els. Cybulski, Peterjohn and Sullivan (in manuscript) examined decomposition
of Pinus taeda from different seed sources growing under different UV-B lev-
els. They found that the decomposition rate (C02 evolution) of needles from one
of the seed sources was accelerated when grown under enhanced UV-B com-
pared to needles grown under ambient UV-B as well as under a higher enhanced
UV-B level. Rozema et al. (1997c) examined the indirect effects of different lev-
els of UV-B exposure on Calamagrostis epigeios leaves, and suggested that de-
composition rate (mass loss) of litter from leaves that had developed under en-
hanced UV-B was slower, possibly because of a higher concentrations oflignin.
They did not find any effects on a-cellulose, hemicellulose, or tannin concen-
trations. Yue, Li and Wang (1998) examined the indirect effect of UV-B expo-
sure of spring wheat on subsequent leaf decomposition and found that decom-
position rates (% organic C loss) were accelerated in leaves that had developed
102 Thomas A. Day
under higher UV-B levels; rates were positively correlated with initial leaf con-
centrations of holocellulose and soluble proteins and negatively correlated with
concentrations of soluble carbohydrates.
Concerning the effects of direct UV-B exposure during litter decomposition,
Gehrke et al. (1995) found that exposure to enhanced UV-B led to reductions in
lignin, possibly caused by photodegradation. UV-B exposure also reduced mi-
crobial respiration rates and altered the species composition of the fungal de-
composers, suggesting that some microbes were sensitive to UV-B. Newsham et
al. (1997) examined the effect of direct UV-B exposure on decomposition of
Quercus robur litter and found that higher UV-B levels lead to slower litter de-
composition rates (mass loss), lower C loss rates, and less fungal colonization.
Newsham et al. (1999) went on to suggest that because relatively little UV-B
reaches litter in the forest floor for much of the year, slower decomposition
brought about by direct exposure of litter to UV-B would be overshadowed by
the indirect effect of accelerated decomposition of Quercus robur leaves that had
developed under enhanced UV-B. Rozema et al. (1997c) found that direct ex-
posure of Calamagrostis epigeios litter to enhanced UV -B accelerated decom-
position rates, which they attributed to photodegradation of lignin.
In summary, the handful of studies to date show that enhanced UV-B expo-
sure during plant growth and direct exposure of this litter to enhanced UV -B may
either slow, accelerate, or have no effect on the rate of litter decomposition. The
reasons for these differences are unclear, but it appears that UV-B can alter lit-
ter decomposition through a suite of factors. Changes in litter inputs and de-
composition rates could have far-reaching implications for plant growth and
ecosystem function, and it has been suggested that limitations imposed by lower
litter quality caused by UV-B exposure may ultimately be more important that
any direct impacts of enhanced UV-B on plant growth (Bjorn et al. 1996). How-
ever, the effects of enhanced UV-B on litter decomposition appear to be species-
and system specific, and generalizations will likely be difficult.
Insect Herbivory
Plant responses to UV-B are quite variable, but results emerging from the stud-
ies examining how plant exposure influences insect herbivory suggest a relatively
consistent negative correlation between plant UV-B exposure and levels of in-
sect herbivory, abundance, and performance (Hatcher and Paul 1994; McCloud
and Berenbaum 1994; Ballare et al. 1996; Grant-Petersson and Renwick 1996;
Rousseaux et al. 1998; Salt et al. 1998; Mazza et al. 1999b). However, even
among the handful of studies examining this relationship, it is apparent the these
responses can vary depending on species of host plant (Gwynn-Jones, Lee and
Callaghan 1997) as well as insect (Grant-Peters son and Renwick 1996).
Regarding evidence that plant UV-B exposure can reduce insect herbivory un-
der field conditions, Ballare et al. (1996) found that the proportion of Datura
ferox plants attacked by leaf beetles declined as the percentage of UV-B reach-
ing the plants was increased from 0% (full filter exclusion) to 100% of ambient
UV-B. Plant exposure to ambient UV-B appeared responsible for a 50% reduc-
tion in the likelihood of leaf beetle attack. In another field exclusion study,
Rousseaux et al. (1998) found fewer moth caterpillar leaf lesions on Gunnera
magellanica plants growing under ambient UV-B than on plants growing under
UV-B filters. Mazza et al. (l999b) found that thrip densities were three to five
times lower on plants growing under ambient UV-B than under UV-B filters.
Salt et al. (1998) found that a modulated UV-B supplement reduced populations
of a sap-sucking psyllid on Calluna vulgaris in the field. In constrast to these
findings, Gwynn-Jones, Lee and Callaghan (1997) examined the influence of en-
hanced UV-B on three Vaccinium species and found less insect herbivory (leaf
area loss) on one species, more on another, and no effect on the third species.
The mechanisms responsible for reductions in insect abundance, feeding, and
performance on plants under higher UV-B levels are not clear. It has been sus-
pected that UV-B induces changes in leaf chemical and physical properties that
make plants less palatable to insects, but what these changes might be is unclear.
Changes in specific leaf mass, water content, and concentrations of bulk UV-B-
absorbing compounds, hemicellulose, and C, which are considered to be general
antiherbivory responses, were typically not affected by UV-B level in these ex-
periments. Slightly higher leaf N concentrations were detected in some of these
studies under higher UV-B, and higher N diets could reduce food consumption
per individual insects (Hatcher and Paul 1994; Rousseaux et al. 1998). Whether
this would in tum correspond to less total plant consumption in the field is un-
clear. In contrast, Salt et al. (1998) did not detect any UV-B effects on leaf to-
tal N concentrations, but found lower concentrations of the amino acid isoleucine
and a tendency for lower concentrations of total free amino acid under enhanced
UV-B. The lower food quality of leaves under enhanced UV-B may have less-
ened insect feeding preference for these plants. An additional suggestion as to
why leaves growing under higher UV -B are less palatable to insects may involve
UV-B induction of specific phenylpropanoids. McCloud and Berenbaum (1994)
found that Citrus jambhiri foliage grown under enhanced UV -B had higher con-
centrations of furanocoumarins than when grown without UV-B. These phenyl-
propanoid derivatives are phototoxic to many insects and appeared to slow the
development of caterpillars reared on this foliage. Grant-Petersson and Renwick
(1996) found that cabbageworm larvae consumed less foliage from Arabidopsis
leaves grown under high UV-B levels, and this result appeared correlated with
increases in kaempferol-based flavonoids in leaves.
An additional explanation for reductions in insect herbivory on plants under
higher UV-B levels is that insects may avoid high levels of UV-B. Most of the
foregoing studies focused on examining the indirect influence of UV-B on in-
sects in that they primarily assessed how host plant exposure to UV -B influenced
herbivory. An exception is the series offield and laboratory experiments of Mazza
et al. (1999b) addressing thrips and soybeans. They presented strong evidence
that thrips perceive and avoid exposure to solar UV-B. Thrips avoided UV-B,
and this effect was detectable in response to small supplements of UV -B added
to a background of outdoor solar radiation, suggesting that insects can be quite
104 Thomas A. Day
sensitive to subtle changes in outdoor UV-B levels. Should these direct and in-
direct effects of UV-B be commonplace in other plant-insect systems, it would
suggest that any direct detrimental effects of enhanced UV-B on plant growth
might be partly offset by lower levels of insect herbivory. This finding also pre-
sents the interesting possibility that, in some cases, failure to detect reductions
in plant growth under enhanced UV-B might be partly attributable to the greater
antiherbivore protection that higher UV-B exposure might afford plants.
Conclusion
The results from a survey of some recent outdoor exclusion experiments in which
UV-B was filtered from sunlight over plants illustrate that some plants are in-
deed not only responsive to ambient levels of UV-B but that their performance
is impaired. One-half of the studies that examined whole-leaf soluble UV-B-
absorbing compounds detected higher concentrations in plants under ambient
UV-B in at least one of the species they examined. Furthermore, at least one-
half of the studies that examined total biomass production and leaf or hypocotyl
length also found that plants produced less biomass or had shorter leaves or
hypocotyls under ambient UV-B compared to reduced UV-B. Whether plants are
responsive to enhanced UV-B levels associated with ozone depletion remains a
more difficult question to answer.
A survey of recent outdoor experiments that have added modulated supple-
ments to ambient UV-B finds that plant responses are less frequently detected
and more subtle. The most consistent plant response to modulated supplements
was an increase in leaf concentrations of UV-B-absorbing compounds, which
was detected in more than one-half of these studies. In no case did supplemen-
tal UV-B reduce total biomass production, and there is little evidence to suggest
that enhanced UV-B levels impair overall plant performance. The greater re-
sponsiveness of plants to higher UV-B levels in the exclusion studies compared
with the modulated supplement studies suggests that the mechanisms involved
in plant responses to UV-B may be close to saturation at ambient UV-B levels.
Adjusting the levels of UV-B supplements through the course of experiments,
based on seasonal trends in ozone concentrations, would further improve the re-
alism of field experiments.
Although the most consistent response to higher UV-B in these field experi-
ments was an increase in concentrations of whole-leaf soluble UV-B-absorbing
compounds, whether these increases translate into improved UV -B screening and
whether this mitigates damage remains unclear. There is little evidence support-
ing the idea that increases in concentrations of whole-leaf soluble UV-B-
absorbing compounds observed under field conditions lead to significant reduc-
tions in leaf epidermal transmittance. Furthermore, the identity and location of
the major UV-B targets in leaves are generally unknown, which makes it diffi-
cult to assess how much protection is afforded by increases in concentrations of
these compounds. More research is needed on the identity and locations of these
absorbing compounds and their significance in controlling UV-B fluxes within

the leaf, as well as the identity and location of target compounds responsible for
plant responses.
The target compounds and mechanisms responsible for reductions in leaf elon-
gation in response to ambient UV-B levels are unknown, but they do not appear
related to reductions in photosynthetic rates per unit leaf area. Possible mecha-
nisms include (1) an increase in wall-bound (insoluble) UV-B-absorbing com-
pounds, (2) oxidative damage, or (3) DNA damage. Exposure to UV-B can lead
to increases in UV-B-inducible phenolics such as ferulic acid, and this may form
cross-links in the cell-wall matrix that could reduce extensibility and constrain
cell expansion. However, there is as yet little evidence suggesting that this mech-
anism explains reductions in leaf elongation under field conditions. Antioxidant
activity in plants can increase upon exposure to UV-B, but whether this occurs
consistently under field conditions and its significance in terms of reduced leaf
elongation are unclear. From a limited number of field studies it appears that
DNA damage products often increase in response to ambient UV-B levels. How-
ever, the physiological consequences of this in terms of leaf growth and overall
plant performance are also unclear. Results from the handful of studies examin-
ing the influence of UV -Bon litter decomposition are variable: enhanced UV -B
exposure of foliage and the subsequent exposure of litter during decomposition
may either slow or accelerate decomposition rates through a suite of factors.
Results emerging from the studies examining how plant UV-B exposure in-
fluences insect herbivory show that in many cases plant exposure reduces levels
of insect herbivory, abundance, and performance, although even among the lim-
ited number of studies to date it is apparent this depends on the species of host
plant and insect. The mechanisms responsible for reductions in insect abundance
and feeding on plants under higher UV-B are not clear, although such may in-
volve not only UV -B-inducible changes in plants that deter insects but avoidance
of UV-B by insects as well.
Acknowledgments. Financial support for some of the work and ideas presented
here was provided by the National Science Foundation (grant OPP-9615268) and
the U.S. Department of Agriculture (grant NRI 97-35100-4214).
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Zepp, R.O., Callaghan, T.V., and Erickson, DJ. 1998. Effects of enhanced solar ultravi-
olet radiation on biogeochemical cycles. J. Photochem. Photobiol. B Bioi. 46:69-82.
5
Ultraviolet Radiation and
Coral Communities
DANIEL F. GLEASON
Coral reefs are considered to be the most diverse marine ecosystem on Earth and
are thought to rival tropical rain forests in terms of their biological complexity
and productivity (Connell 1978; Jackson 1991). The primary constructs of trop-
ical reef systems are reef-building corals, which produce a continuously grow-
ing skeleton via biosynthesis and deposition of calcium carbonate. Growth and
death of corals provide habitat structure and topographic complexity that can be
exploited by the myriad of algae, invertebrates, and vertebrates that reside in
these ecosystems (Hoegh-Guldberg 1999).
The high productivity of coral reef systems and, in particular, reef-building
corals posed a paradox for early investigators bcause the waters surrounding coral
reefs are characteristically nutrient poor (Darwin 1842; Odum and Odum 1955;
Kohn and Helfrich 1957). Researchers later showed that the immense success of
corals can be attributed largely to a mutualistic association between the coral an-
imal and intracellular photosynthetic dinoflagellates known as zooxanthellae
(Muscatine and Porter 1977). Translocation of photosynthetic products such as
amino acids, sugars, complex carbohydrates, and small peptides from zooxan-
thellae to their coral host provides most, if not all, of the carbon needed for an-
imal respiration as well as several essential nutrients (Muscatine 1973; Trench
1979; Falkowski et al. 1984). In return the coral animal, through by-products of
cell metabolism, provides zooxanthellae with nutrients, such as nitrogen and
phosphorus, that are often in limited supply in tropical oligotrophic waters. The
result is an organism in which limited, essential nutrients can be tightly recycled
between partners, reducing the need for outside nutritional resources.
Nutritional reliance on zooxanthellae necessitates that, on average, hermatypic
corals inhabit open reef areas where visible light intensity maintains positive net
primary production of the coral-algal symbiosis (Huston 1985a). Occupying open
reef areas also exposes symbiotic corals to ultraviolet-A (UV-A, 320-400 nm)
and ultraviolet-B (UV-B, 280-320 nm) radiation, and this poses another para-
dox. Reef-building corals require visible light for growth and survival but must
somehow counteract the negative biological effects of ultraviolet radiation
(UV-R). Extensive research into the role of UV-R on coral reefs was spurred in
the 1980s to mid-1990s by issues related to ozone depletion and the fear that in-
118
5. Ultraviolet Radiation and Coral Communities 119
creases in UV-B in tropical regions may lead to reef degradation (Siebeck 1988;
Kinzie 1993; Shick et al. 1995; Lesser and Lewis 1996; Shick, Lesser and Jok-
iel 1996; and many others). Although we now know that ozone depletion will
result in little, if any, increase in UV-R levels in tropical regions (Stolarski et al.
1992; Madronich et al. 1995), it is hypothesized that UV-R has been a selective
force in the 200 million or so years that modem-day corals have been in exis-
tence. As a result, while ozone depletion was the impetus for many initial stud-
ies, recent attention has turned to the ecological and evolutionary significance of
UV-R (both UV-A and UV-B) in coral reef ecosystems.
This switch in research emphasis from UV-B only to the entire UV-R spec-
trum is especially appropriate for coral reef studies because changes in water col-
umn conditions alone can result in abrupt and large increases in UV-R reaching
to depths on coral reefs (Gleason and Wellington 1993). In fact, these changes
can be of greater magnitude than those occurring in the Antarctic in the absence
and presence of the ozone hole. Thus, it is likely that UV-R will continue to be
an important abiotic stressor in coral reef systems.
This chapter reviews what is known about the penetration of UV-R on coral
reefs, relates how UV -R affects the physiology of reef organisms, discusses the
mechanisms tropical marine species use to counter or repair UV-R damage, and
speculates on whether UV-R controls the distribution and abundance of reef
species. As might be surmised from their prominence in this ecosystem, much
of our knowledge about UV-R effects on coral reefs applies specifically to reef-
building corals. Therefore, it is inevitable that this review is biased toward the
biological impacts of UV -Ron reef-building corals. This bias is not unwarranted
because, as already noted, reef-building corals provide the underlying structure
upon which most other reef inhabitants depend (Hoegh-Guldberg 1999).
Measurement and Penetration of UV-R in Reef Waters

Worldwide, coral reefs occur generally in shallow «50-m depth), tropical seas
in a band from 25° N to 25° S latitude (Veron 1986). The upper geographic
boundaries of coral reef development are set primarily by latitudinal variation in
mean annual temperature because corals are able to thrive only at seawater tem-
peratures between 18° and 30°C. In contrast, the maximum depth limit is set
principally by the dependence of the coral-algal symbiosis on light for photo-
synthesis; thus, reef-building corals are restricted to habitats at or above the com-
pensation depth (i.e., the depth at which only 1% of the surface irradiance
occurs).
Intensities of UV-A (320-400 nm) and UV-B (280-320 nm) reaching the
Earth's surface in tropical regions are the highest found worldwide because of
the relative thinness of the ozone layer near the equator and the low zenith
angle of the sun (Baker, Smith and Green 1980). Further penetration of short-
wavelength light to depths below the ocean surface at all latitudes is controlled
by absorption by water and scattering by suspended particles (Jerlov 1968). Rel-
120 Daniel F. Gleason
atively small amounts of phytoplankton and suspended matter are present in most
tropical seas, including those surrounding many coral reefs; thus, biologically
damaging wavelengths ofUV-R can potentially penetrate to considerable depths
(Jerlov 1968; Smith and Baker 1979; Fleischmann 1989; Gleason and Welling-
ton 1993, 1995; Lesser 1995). Exceptions to this generally accepted paradigm
do occur, especially on inshore reefs and mainland reefs exposed to terrigenous
input (Gulko 1995; Dunne and Brown 1996).
A number of instruments and techniques, including chemical actinometers, bi-
ological dosimeters, narrow-band spectroradiometers, and broad-band radiome-
ters, have been used to characterize the UV-R environment on coral reefs. There
have been two excellent reviews on the role of UV -R in coral reef systems (Shick,
Lesser and Jokie11996; Dunlap and Shick 1998), but neither outlined completely,
nor discussed, the methods used for monitoring UV-R. I review these briefly
here, especially pointing out the suitability of each method for use in coral reef
systems.
Actinometers
Fleischmann (1989) provided the first systematic measures of UV-R on coral
reefs by incorporating a chemical actinometer consisting of o-nitrobenzaldehyde
film. This compound absorbs between 300 and 410 nm with heavier weighting
for wavelengths below 350 nm. As o-nitrobenzaldehyde absorbs UV -R, it is con-
verted to o-nitrosobenzoic acid. This conversion is linear so long as the film is
not used beyond 50% exposure and can be quantified on an infrared spec-
trophotometer as a decrease in peak height at a wave number of 1530 cm- l .
In Discovery Bay, Jamaica, Fleischmann (1989) used this technique and found
that UV -R penetrated as deep as 25 m. This depth of penetration is in good agree-
ment with those predicted by Jerlov (1950) and Smith and Calkins (1976) for
clear oceanic waters. The inherent advantages of using a chemical actinometer
such as o-nitrobenzaldehyde film are that it is inexpensive, simple to deploy, and
can be easily calibrated using an infrared spectrophotometer. The downside of
using this system to quantify UV -R effects on living organisms is that attenua-
tion of individual UV-R wavebands cannot be determined and, although it inte-
grates over the entire UV -R spectrum, it has a wavelength-specific response curve
that may not mimic that in biological compounds and tissues (e.g., absorption
curve in Fleischmann 1989). Furthermore, results using o-nitrobenzaldehyde
should be viewed with caution (Morales, Jara and Cabera 1993). A chemical
actinometer may be ideal for investigators on a limited budget desiring to make
relative comparisons among sites.
Biological Dosimeters
Akin to chemical actinometers are biological dosimeters. These systems have in-
cluded such biological targets as repair-deficient strains of bacteria, naked DNA,
or formation of bacteriophage plaques (Karentz and Lutze 1990; Regan et al.
1992; Kirk et al. 1994). For any of these methods, it is assumed the dosimeter
measures accumulation of chemical alterations in DNA that are directly attrib-

utable to UV-R exposure. The demonstration by Smith and Baker (1979) that the
maximum biological effectiveness, in terms of DNA, occurs around 305 nm in-
dicates that these dosimeters most closely measure effects of UV-B exposure.
Naked DNA and bacteriophages are the only biological dosimeters that have
been used in tropical waters surrounding coral reefs and only in one study. Re-
gan et al. (1992) used DNA labeled with l4C-thymidine that was extracted and
isolated from cell cultures of skin fibroplasts. They sealed this DNA into quartz
tubes containing an appropriate buffer and deployed these tubes at the surface
and at 0.5-, 1-, 2-, and 3-m depths in waters adjacent to Lee Stocking Island, Ba-
hamas. Quantification of cyclobutane pyrimidine dimer formation at 1, 2, and 5
days after deployment showed a linear progression of dimer formation with time
at all depths and a linear decrease in dimer formation with increased depth. Dimer
formation rates ranged from 0.24% day-l at 0.5-m depth to 0.08% day-l at
3-m depth (Regan et al. 1992). Extrapolation of these results to deeper water in-
dicated that 94% of the DNA-damaging UV-B is filtered out by 5-m depth. Sur-
face samples deviated from the linear pattern observed along the depth gradient
(0.46% day-l dimer formation), indicating that organisms in the upper few cen-
timeters of the water column, such as phytoplankton and dispersing larvae, may
be exposed to very high levels ofUV-B. Results obtained with naked DNA were
supported through quantification of plaque formation by bacteriophages previ-
ously exposed to ambient UV-B at the same locations and depths. Specifically,
after 1 day of exposure at the surface plaque formation was reduced by 96%,
whereas at 3-m depth there was no significant effect.
Biological dosimeters using unprotected DNA in many ways provide a worst
case scenario. These dosimeters measure negative UV-B effects in the absence
of shielding compounds or DNA photorepair systems so direct extrapolation to
organismal damage is probably not feasible. It should be pointed out, however,
that they probably underestimate the maximum amount of DNA damage that is
possible at a particular UV -B exposure. All biological dosimeters require the tar-
get organsim or molecule be enclosed in a holding chamber (Karentz and Lutze
1990; Regan et al. 1992). None of the materials used currently in this applica-
tion is 100% transparent to UV-B, and so they provide the organisms or target
molecule with some protection. Even quartz and silica glass, which are probably
the best UV-R-transmitting materials on the market, can absorb 6%-10% of the
UV-R passing through it (Gleason and Wellington 1995).
The advantages of employing biological dosimeters are threefold. First, use of
naked DNA or repair-deficient strains of bacteria provides a directly interpretable
biological assay. If the dosimeter is deployed and receives damage, then it is
clear that negative effects on organisms are possible at that location and water
depth. Second, biological dosimeters integrate UV-B-induced damage over sev-
eral days and so are not sensitive to minor meteorological variation, such as pass-
ing clouds, that may affect physical radiometers taking instantaneous readings.
Third, biological dosimeters are relatively inexpensive compared to electronic
spectroradiometers.
Although biological dosimeters are excellent for measuring UV-B-induced

DNA damage, it is unclear how results of these assays might be applied to other
impacts, such as inhibition of photosynthesis or production of oxygen radicals.
Many of these effects are sublethal but can directly impact organismal fitness.
Furthermore, UV-A, although known to be important in photorepair, can debil-
itate cells through photochemical interactions with other biological molecules or
through generation of free radicals (Kirk et al. 1994; Garcia-Pichel 1998). If we
are interested in the differential effects of UV-A and UV-B, then employing ra-
diometers and spectroradiometers may be our best option.
Radiometers and Spectroradiometers

In coral reef systems, two classes of electronic instruments have been employed:
radiometers that measure light at fixed bandwidths, and spectroradiometers that
can scan across a series of wavelengths at a specified bandwidth (Lesser 1995).
The commercially available radiometers that have been used in coral reef sys-
tems include the International Light, Inc. (Newbury Port, MA, USA) broad band
UV-A (peak detection at 365 nm with 50% detection range of 330-375 nm) and
UV-B (peak detection at 285 nm with 50% detection range of 265-310 nm) sen-
sors, and the Biospherical Instruments, Inc. (San Diego, CA, USA) narrow-band
model with fixed wavelength maxima of 305, 320, 340, and 380 nm (50% de-
tection range :510 nm at each wavelength maxima). In terms of spectrora-
diometers, the only two models that have been incorporated are the LiCor, Inc.
(Lincoln, NE, USA) model LI-1800UW and the Macam Photometrics Ltd. (Liv-
ingston, Scotland) model SR991O. The reader is referred to Kirk et al. (1994) for
further details on the specifications for the International Light, Biospherical In-
struments, and LiCor systems and to Dunne and Brown (1996) for the Macam
Photometrics system.
Studies incorporating spectroradiometers have found that both UV-A and
UV-B can penetrate to considerable depths. For example, on reefs on the outer
islands of the Bahamas and the barrier reef of Belize, Central America, detectable
levels of UV-B and UV-A occur at depths in excess of 24 m (Gleason and
Wellington 1993; Shick, Lesser and Jokiel 1996). Variation in UV-R both tem-
porally and on fairly small spatial scales, however, is significant. As might be
expected, on average intensities are greatest during the summer when the solar
zenith angle of the sun is at a minimum. For example, in the Florida Keys,
UV-B and UV-A intensities can differ by as much as 23.3% and 7.6%, respec-
tively, between April and July (Figure 5.1). Likewise, there is a tendency for
UV-R to penetrate more deeply in open ocean sites than coastal or lagoonal 10-
cations (Lesser 1995; Dunne and Brown 1996). The predictability of both these
patterns can be disrupted, however, if decreased or increased rainfall, shifts in
prevailing winds, or changes in other climatic patterns occur, ultimately leading
to a change in water column characteristics. On reefs adjacent to San Salvador
Island, Bahamas, Gleason and Wellington (1993) found UV-A and UV-B inten-
sities at 24-m depth can potentially double if the water column changes from its
-
,....
I
E
0.15
- - Apri l
UV-8
c June/July
N
•
E
-
~
(1)
u
c
0.10
1.41 ~ .
.~
'1J
nJ
a-
a-
0.05
-
m
...
en
u
CI)
c.
0.00
300 305 310 315 320
Wavelength (nm)
-
,....
I
E
c
0.8 UV-A
N
0.7
I
- - April
E 0.6
-
June/July
~
CI) 0.5
u
c
.~ 0.4
'1J
nJ
...... 0.3
-
en
nJ
a-
u
CI)
c.
0.2
0.1
320 330 340 350 360 370 380 390 400
Wavelength (nm)
FIGURE 5.1. Mean spectral irradiance for UV-B (300-320 nm) and UV-A (320-400 nm)
at 3-m depth on Conch Reef (24 57' N, SO° 27' W) in the Florida Keys, FL, USA. Each
0
curve is based on measurements taken with a LiCor LI-1S00UW spectroradiometer be-

tween 1100 and 1400 (DST) on five consecutive cloudless days during April 17-21 and
June 29-July 3, 1993. Values, with their corresponding arrows, represent the integrated
irradiance under each curve.
TABLE 5.1. Integrated UV-A and UV-B intensities between 1100 and 1400 (DST) at
24-m depth in waters adjacent to San Salvador Island, Bahamas.
Ultraviolet intensity (W m- 2)
UV-B (300-320 nm) UV-A (320--400 nm)
Mean (±SE) 0.10 (.01) 11.44 (1.25)
Maximum 0.19 18.17
Theoretical maximum 0.24 22.16
The mean UV-R intensity is based on measurements taken over 11 days during July and August 1991
with a LiCor LI-1800UW spectroradiometer. The maximum represents the single highest UV-R in-
tensity observed during this same time period. Theoretical maxima at 24-m depth were calculated
based on attenuation efficients for the clearest oceanic waters (Smith and Baker 1981) and the high-
est UV-R intensities observed at I-m depth. These theoretical maxima are hypothesized to represent
the highest intensities possible at 24-m depth at this site.
Data adapted from Gleason and Wellington (1993).
average state of turbidity to one of exceptional calm and clarity (Table 5.1). What
this means is that coral reef organisms are exposed to a dynamic UV -R envi-
ronment that mayor may not be predictable over evolutionary time.
It should be pointed out that none of the UV-R monitoring methods reviewed
here is perfect. Actinometers and biological dosimeters are the most economical
means currently available but lack the sensitivity and flexibility of scanning spec-
troradiometers. Scanning instruments, on the other hand, may suffer from stray
light intrusion at lower wavelengths or be submersible only to shallow depths
(Kirk et al. 1994; Dunne and Brown 1996). If we are to truly identify the role
of UV-R in the ecology of coral reefs, we must develop a reliable and cost-
effective means of standardizing UV-R measurements. In general, the ideal in-
strument would be small, self-contained, submersible to at least 50 m, able to
scan to at least 300 nm, and be within the budget of most reasearch labs
«$10,000). Also, as pointed out by Kirk et al. (1994), irradiance values must
be converted for the immersion effect and the sensor must have a true cosine re-
sponse underwater. Finally, for most applications a scanning instrument is prob-
ably more useful than one with fixed narrow or broad bandwidths because of
wavelength-dependent responses in organisms (Lesser and Lewis 1996).
Physiological Effects of UV-R on Coral Reef Organisms

Regardless of the monitoring method, it is clear that on all types of coral reefs
UV-R penetrates to depths inhabited by a wide range of vertebrate and inverte-
brate species. To understand how UV-R affects the broader ecology of reef sys-
tems, it is important to ascertain the physiological consequences for individual
species. Effects of UV-R on the physiology of corals and coral reef organisms
have been thoroughly reviewed by Shick, Lesser and Jokiel (1996) and are only
summarized briefly here. I then discuss the potential for negative UV-R effects
to be accentuated through interactions with other environmental parameters such

as temperature perturbations, especially as relates to coral bleaching. I complete
this section by alluding to some potential positive physiological outcomes of
UV-R exposure.
Overview of Physiological Effects

The first experimental evidence that UV-R may negatively impact reef-building
corals was provided by Catala-Stucki (1959), who noted that corals degrade when
exposed to artificial illumination at 254 and 360 nm. These results were later
confirmed using natural sunlight when it was noticed that reef-building corals
moved from deeper sites to shallower sites or to outdoor aquaria die if not shielded
from UV-R (Vareschi and Fricke 1986; Scelfo 1986). Since the observations by
Catala-Stucki (1959), a whole host of sublethal UV-R effects on reef-building
corals have been reported: these include depression of calcification and skeletal
growth (Jokiel and York 1982; Gleason 1993a); suppression of photosynthesis
(Masuda et al. 1993; Shick et al. 1995); production of cytotoxic reactive oxygen
species such as singlet oxygen, hydrogen peroxide, and other oxygen-centered
radicals (reviewed in Dunlap and Shick 1998); and inhibition of zooxanthella
growth in culture (Jokiel and York 1982, 1984; Lesser and Shick 1989; Lesser
1996) and in hospite (Gleason 1993a).
The impacts of UV-R exposure on other coral reef organisms have not been
well studied in most cases. In the only investigation of cryptic sessile epifauna,
Jokiel (1980) showed that these organisms are killed by acute exposure to
UV-R (see "UV-R and Distributional Patterns of Coral Reef Species," follow-
ing). Studies investigating UV-R effects on benthic algae occupying coral reef
systems are also not plentiful even though these organisms contribute substan-
tially to the high primary productivity of the reef (Odum and Odum 1955). In-
vestigations with the alga Eucheumia striatum, which occupies un shaded habi-
tats in shallow reef flat communities in Hawaii, did show reductions in both
chlorophyll a and carotenoid concentrations in the presence of natural UV-R
(Wood 1989). These results as well as those conducted on phytoplankton, ben-
thic macroalgae, and seagrasses from temperate regions (Larkum and Wood 1993)
suggest that high levels of UV -R may inhibit photosynthesis of algae in tropical
waters.
UV-R and Coral Bleaching

What is the role of UV-R in coral stress responses? Addressing this question is
becoming more and more critical as the frequency of coral stress events, espe-
cially coral bleaching, rises. Over the past several decades there has been an in-
crease in the frequency and severity of coral bleaching events worldwide (Glynn
1991, 1993; Brown 1997; Hoegh-Guldberg 1999). Coral bleaching results when
endosymbiotic algae dissociate from host coral tissues, or photosynthetic pig-
ments per algal cell decrease, or both occur simultaneously. Bleaching can re-
sult in depressions in coral primary productivity, reduced reproductive output,

decreased tissue biomass, and, in extreme cases, colony death (Porter et al. 1989;
Glynn and D'Croz 1990; Szmant and Gassman 1990; Fitt et al. 1993; Gleason
1993b; Lesser 1997). Many factors including sedimentation, salinity fluctuations,
bacterial infestation, and increased UV-R have been implicated in coral bleach-
ing (reviewed in Glynn 1993; Hoegh-Guldberg 1999), but the primary culprit is
thought to be water temperatures that exceed the average annual maximum by
1°C or more (Brown 1997; Hoegh-Guldberg 1999). Although this has been true
for many of the bleaching events that occurred in recent years, complications
arise because of a lack of correspondence between bleaching and high water tem-
perature in some instances (Atwood, Hendee and Mendez 1992) and the fact that
high water temperatures and high UV-R intensities sometimes covary (Drollet et
al. 1994; Drollet, Faucon and Martin 1995).
Investigation into the role of UV-R in coral bleaching was stimulated by two
observations. First, bleaching events often occur during periods when environ-
mental conditions favor penetration of UV -R through the water column (i.e., low
wind velocity, clear skies, calm seas, low turbidity) (Glynn 1993). Second, corals
often bleach most severely on their upper, most sunlit surfaces (Hoegh-Gu1dberg
1999). Hypothesizing a UV-R role in coral bleaching is reasonable because of
the biological effectiveness of this light and, as indicated previously, UV-R in-
tensities underwater can as much as double if the water column changes from its
normal state to one of exceptional calm and clarity (Gleason and Wellington
1993). Although field and laboratory experiments indicate that UV-R can con-
tribute to coral bleaching (Lesser et al. 1990; Glynn et al. 1992; Gleason and
Wellington 1993; Reaka-Kudla et al. 1993; Shick et al. 1999), current evidence
suggests it is unlikely to be the primary cause. UV-R probably exacerbates the
bleaching process in the presence of high water temperature (usually >30°C)
and visible light.
Identifying the physiological alterations leading to coral bleaching is an active
area of study, and a recent physiological model by Jones et al. (1998) that was
reviewed by Hoegh-Guldberg (1999) appears to be most consistent with previ-
ous work. This model suggests that increased temperatures are a prerequisite for
coral bleaching but that the effect of temperature can be exacerbated by sun en-
ergy. In this model (see Hoegh-Guldberg 1999 for details), heat stress during the
process of zooxanthellae photosynthesis prevents the flow of energy to the dark
reactions where CO 2 would be fixed to organic carbon by the enzyme rubisco.
As a result, light energy that would normally be passed to the dark reactions is
absorbed by oxygen, creating reactive oxygen species. If these oxygen radicals
are not purged from the system, then cellular damage and expulsion of photo-
synthetic endosymbionts ensues (Lesser 1997). Although this model suggests the
role of UV -R in coral bleaching is secondary to that of photosynthetically active
radiation (PAR, 400-700 nm), any factor that blocks the dark reactions or causes
overenergization of the light reactions, such as UV-R, may contribute to this
process.
Interestingly, coral bleaching studies have placed greatest emphasis on nega-

tive impacts imposed upon zooxanthellae. This emphasis has occurred even
though detachment of whole host animal cells containing zooxanthellae has been
proposed as one cellular mechanism leading to coral bleaching (Gates, Bagh-
darian and Muscatine 1992). Increased UV-R exposure, such as occurs during
calm and clear water conditions, may lead to damage of critical animal cellular
components including DNA and the cytoskeleton. As hypothesized by Shick et
al. (1999), cytoskeletal damage could lead to the process of host cell detachment
through inhibition of cytokinesis and alterations in cytoskeletal interactions with
cell-surface integrins. Studies investigating how host damage may contribute to
coral bleaching events are definitely needed to provide us with a complete un-
derstanding of the factors leading to bleaching.
Positive Outcomes of UV-R Exposure

Although UV-R is primarily considered a negative abiotic stressor, it should be
pointed out that there may be positive aspects induced by this radiation, partic-
ularly in photosynthetic organisms such as corals. Because UV -R, especially
UV-A, can penetrate to considerable depths on many coral reefs, the ability to
use this portion of the light spectrum for physiological functions such as photo-
synthesis may benefit a species and allow it to extend its maximal depth range.
An example of this phenomenon is provided by the coral Leptoseris fragilis, the
only zooxanthellate coral species found at depths in excess of 100 m in the Red
Sea (Fricke and Schuhmacher 1983).
The highest densities of L. fragilis occur between 110- and 120-m depth. The
ability of this species to occupy depths that at noon receive only 0.15%-1.7%
(0.5-10 /LE m- 2 S-l) of surface irradiance in the photosynthetically active por-
tion of the spectrum (i.e., 400-700 nm) results from autofluorescence of pigment
granules located below the zooxanthellae in the oral gastroderm of the host
(Schlicter, Fricke and Weber 1986; Schlicter and Fricke 1990, 1991). These chro-
matophores absorb UV-A in the range from 380 to 400 nm and reemit it at wave-
lengths between 420 and 450 nm. This emission spectrum fits nearly perfectly
with the absorbance maxima of the algal pigments and makes existence possible
in a habitat that otherwise receives photosynthetically active photon flux densi-
ties below those necessary for photosynthesis of the symbiotic algae (Schlicter
and Fricke 1990).
In L. fragilis, the evolution of a complex and potentially costly (i.e., biosyn-
thesis of chromatophores and pigments) host mechanism to promote photosyn-
thesis of the symbiotic algae underscores the importance of this mutualism to the
success of extant coral reef ecosystems. To my knowledge, however, the studies
just cited are the only ones that have investigated positive contributions of
UV -R to coral reef organisms; this is surprising considering that the prevalence
of UV -R-fluorescent pigments in reef organisms, especially reef-building corals,
has been recognized for many years (Kawaguti 1944; Logan, Ha1crow and
Tomascik 1990). Further, UV-A exposure has been implicated in photorepair

processes that may enhance the UV-R resistance of reef-building corals (Siebeck
1981, 1988). Investigations into the positive biological aspects of UV-R are def-
initely underrepresented in the literature but are needed in both photosynthetic
and heterotrophic coral reef species.
UV -R Protective Mechanisms in Coral Reef Organisms

Given the potential for UV-R to cause biological damage in reef-building corals
and other reef organisms, it is not surprising that tropical marine species have
evolved several means of mitigating its effects. Physiological mechanisms used
by reef organisms to resist UV-R, as with most other species, are primarily of
two types: those that prevent biologically damaging UV-R from reaching criti-
cal cellular targets and those that counter the negative effects of UV-R once they
have resulted. UV-R sunscreens represent the first line of defense and in reef or-
ganisms include a group of compounds known as mycosporine-like amino acids.
Processes that correct problems once they arise include quenching of reactive
oxygen species and other detrimental ions and photorepair of DNA.
UV-R-Absorbing Compounds
By far the most investigated UV-R protective mechanism in reef organisms is
that of UV-R-absorbing compounds. Shibata (1969) was the first to discover
UV-R protective compounds in coral reef organisms when he extracted a water-
soluble, 320-nm-absorbing substance from corals and cynaobacteria on the Great
Barrier Reef. He dubbed this substance "S-320" to coincide with its absorbance
maximum. The material Shibata (1969) extracted has since been identified as a
class of compounds known as mycosporine-like amino acids (MAAs). All MAAs
are free amino acids having a cyclohexenone or cyclohexenimine chromophore
conjugated with the nitrogen substituent of an amino acid (Dunlap and Shick
1998). There are 19 structurally distinct MAAs identified to date that have peak
absorbances between 309 and 360 nm (structures in Dunlap and Shick 1998;
Cockell and Knowland 1999). These sunscreens are not only present in many
coral reef organisms but have also been detected in bacteria, algae, invertebrates,
and vertebrates throughout the world's oceans (reviewed in Shick, Lesser and
Jokiel 1996; Dunlap and Shick 1998; Cockell and Knowland 1999).
In coral reef systems, the role of MAAs as sunscreens has been inferred from
four aspects of their biology. First, MAAs have a high molar extinction coeffi-
cient (E == 28,000 to 50,000) in the range of environmentally relevant UV-R. Sec-
ond, concentrations of MAAs in coral tissues are generally higher in shallow wa-
ters where UV-R intensities are higher and decrease with depth in accordance
with the gradient in UV-R (Maragos 1972; Dunlap, Chalker and Oliver 1986;
Gleason and Wellington 1993, 1995; Banaszak et al. 1998). Third, in many cases
concentrations of MAAs in animal or algal tissues increase when UV -R intensi-
ties are enhanced experimentally (Lesser et al. 1990; Gleason 1993; Shick, Lesser
and Stochaj 1991; Shick et al. 1999). Finally, individuals containing higher con-
centrations of MAAs show better performance under a similar UV-R regimen
than conspecifics with lower levels (Gleason 1993; Shick et al. 1995). Further
details on the sunscreening role of MAAs in coral reef organisms can be found
in two excellent recent reviews by Dunlap and Shick (1998) and Cockell and
Knowland (1999) and are not reiterated here. Instead, I discuss our current knowl-
edge regarding the synthesis and distribution of MAAs within the coral-algal
symbiosis and how this may relate to UV -R protection. I then explore the ques-
tion of whether there is a biological cost to producing and maintaining MAAs.
It has been assumed that MAAs in corals are biosynthesized by zooxanthellae
via the shikimate pathway (Shick et al. 1999). This assumption is reasonable be-
cause animals lack the requisite pathway to produce aromatic amino acids (Bent-
ley 1990). Whether the shikimate pathway within zooxanthellae is the source of
MAAs in cnidarian-algal symbioses was tested for the first time recently in the
coral Stylophora pistillata. Glyphosphate, an inhibitor of several enzymes in the
shikimate pathway, when added to the surrounding seawater was shown to re-
press production of MAAs in corals exposed to increased intenisties of UV-R
(Shick et al. 1999). This result confirms that MAAs can be derived via this path-
way in reef-building corals.
Two lines of evidence, however, place doubt on the assumption that the shiki-
mate pathway is the sole source of MAAs in reef-building corals. First, many
species of marine animals lacking intracellular photosynthetic endosymbionts,
including sponges, echinoderms, crustaceans, and fishes, possess MAAs (re-
viewed in Dunlap and Shick 1998). These organisms are thought to acquire these
compounds from the diet. Likewise, the ability of reef-building corals to feed on
zooplankton, as well as to carry out photosynthesis, may provide an alternative
source of MAAs that can subsequently be sequestered. Second, intracellular di-
noflagellates do not appear to be the source of MAAs in all algal-cnidarian sym-
bioses. For example, Banaszak and Trench (1995) showed that MAAs are not
present in freshly isolated Symbiodinium californium extracted from the host
anemone Anthopleura elegantissima, even though this anemone possessed six
MAAs. Furthermore, aposymbiotic A. elegantissima exposed to UV -R had higher
concentrations of MAAs than those not exposed, suggesting that these anemones
are obtaining MAAs from some exogenous source. At present, the contribution
that endogenous and exogenous sources make to the MAA pool in reef-building
corals is unclear, and it may vary from species to species just as nutritional de-
pendence on heterotrophic sources is thought to vary.
MAAs are considered to be an important UV-R protective mechanism in reef
building corals, but we do not know exactly where these compounds occur within
the tissues of the symbiosis. Shick et al. (1995) separated zooxanthellae from the
animal and found 95% of the total MAA pool in the animal tissues. They also
demonstrated that photosynthesis in zooxanthellae isolated from shallow-water
colonies is inhibited by UV -R, indicating that host tissues protect the zooxan-
thellae. They did not, however, determine the exact positioning of MAAs within
the symbiosis. Identifying the location of these compounds could be vital for de-
termining their role in preventing both UV -R-induced photosynthetic inhibition
and animal cellular damage. Zooxanthellae are located in the innermost gastro-
dermal tissue. If MAAs are present in high concentrations in ectodermal cells,
or throughout the ectoderm and gastroderm, then they may provide protection
for both animal cellular targets and the photosynthetic apparatus. In contrast, if
these compounds occur primarily in gastrodermal cells, then it is likely that they
only provide protection for the photosynthetic system. The study that has come
closest to determining the location of MAAs within coral tissues analyzed the
top and bottom halves of plugs from the Hawaiian coral Montipora verrucosa
(Kinzie 1993). Greater concentrations of MAAs were located in the upper half,
but it is unclear which cell layers were included in each plug half. Obviously,
this question is still open for investigation.
Recently, it has been suggested that coral mucus may reduce the amount of
UV-R reaching tissue surfaces because MAAs have been detected in the mucous
layer (Drollet, Glaziou and Martin 1993; Drollet et al. 1997; Teai et al. 1998).
Based on an average optical density of 0.3 for samples from six scleractinian
species in Tahiti, Teai et al. (1998) concluded that mucus blocks approximately
7% of the total UV-R impinging on the coral surface. Furthermore, recent stud-
ies have shown that bacteria present in the mucus-laden coral surface microlayer
suffer less DNA damage than those present in the adjacent water column (Lyons
et al. 1998). Although demonstration of its UV-R-absorbing properties adds to
the myriad of functions including sediment removal, feeding, and prevention of
desiccation (Meikle, Richards and Yellowlees 1988; Coffroth 1990) that are al-
ready ascribed to coral mucus, it is unclear whether corals secrete more of this
substance in response to UV-R exposure.
One of the major questions in terms of lifetime fitness of reef organisms is
whether there is a cost to producing MAAs. The answer to this question is cur-
rently unclear, and differences of opinion exist (Shick et al. 1995; Norris 1999).
Interestingly, the same question has long been asked by plant ecologists in ref-
erence to antiherbivore compounds, and it may be worthwhile to follow their
lead in approaching this issue. The resource availability hypothesis was devised
to explain allocation of resources in plants to antiherbivore compounds when re-
sources are in limited supply (Coley, Bryant and Chapin 1985). According to this
hypothesis, the amount of resource allocated to defense should depend on the ex-
tent of exposure to the damaging force and the ability of the plant to replace crit-
ical tissues. Slower-growing species should allocate more resources to defensive
compounds because they are less able to replace tissues that are critical for en-
hancing fitness.
If producing MAAs truly has a cost in terms of organismal fitness, and the re-
source availability hypothesis applies, then we can make four general predic-
tions: (1) MAA concentrations are positively correlated with variation in UV-R
intensities; (2) MAAs occur in greater concentrations in parts of the organism
exposed to higher intensities of UV-R; (3) slower-growing species maintain
higher static concentrations of MAAs than faster-growing species in the same

habitat because faster-growing species can more easily replace damaged tissues;
and (4) MAAs cannot be maintained at levels sufficient to prevent UV-R dam-
age if the organism is severely stressed by other abiotic factors. I next investi-
gate whether these predictions are supported by the current literature.
Prediction 1: Positive Correlation Between UV-R Intensities and

MAA Concentrations
If MAAs are costly to produce, than resources should be allocated to producing
them only if, and when, they are needed. As pointed out previously, a positive
relationship between UV -R intensities and MAA concentrations is one of the ma-
jor pieces of evidence implicating these compounds as UV-R protectants. In fact,
for the 16 reef species so far sampled along a wide depth gradient, only 2, Diplo-
ria strigosa from the Caribbean and Clavularia sp. from the Great Barrier Reef,
have failed to show any statistically significant pattern of decreased MAAs with
increased depth (Table 5.2). It should also be pointed out that for D. strigosa,
Montipora verrucosa from Moku Manu, and cases in which two studies sam-
TABLE 5.2. Studies quantifying mycosporine-like amino acid (MAA) concentrations in

coral reef organisms along a depth gradient.
Decrease
Species Location with depth Reference
Agaricia agaricites Key Largo, FL Yes Gleason et aI. (in preparation)
A. tenuifolia Carrie Bow Cay, Belize Yes Banaszak et al. (1998)
Acropora formosa Davies Reef, GBR Yes Dunlap et al. (1986)
A. microphthalma Bowl Reef, GBR Yes Shick et aI. (1995)
Clavularia sp. Grub Reef, GBR No Shick et aI. (1991)
Diploria strigosa Carrie Bow Cay, Belize No Banaszak et al. (1998)
Fungia fungites Tahiti Yes Drollet et al. (1993)
Montastraea annularis Carrie Bow Cay, Belize Yes Banaszak et al. (1998)
M. annularis San Salvador, Bahamas Yes Gleason and Wellington (1993)
M. cavernosa Carrie Bow Cay, Belize Yes Banaszak et aI. (1998)
Montipora patula Moku Manu, Hawaii Yes Banaszak et al. (1998)
M. verrucosa Kaneohe Bay, Hawaii Yes Banaszak et al. (1998)
M. verrucosa Moku Manu, Hawaii No Banaszak et aI. (1998)
Pocillopora damicornis Kaneohe Bay, Hawaii Yes Jokiel et al. (1997)
P. damicornis Kaneohe Bay, Hawaii No Banaszak et al. (1998)
P. meandrina Moku Manu, Hawaii Yes Banaszak et aI. (1998)
Porites astreoides St. Croix, USVI Yes Gleason (l993a)
P. compressa Kaneohe Bay, Hawaii No Banaszak et al. (1998)
P. compressa Kaneohe Bay, Hawaii Yes Kuffner et al. (1995)
P. porites Carrie Bow Cay, Belize Yes Banaszak et al. (1998)
US VI, U.S. Virgin Islands

A "Yes" in the third column indicates a significant decrease in MAA concentrations with increased
depth. All species listed are in the order Scleractinia except Clavularia sp., which belongs to the sub-
class Octocorallia, order Stolonifera.
pIing the same species at the same site differed in their result (i.e., Pocillopora
damicornis and Porites compressa), a trend for decreasing MAA concentrations
with increasing depth is evident but detection of a statistically significant pattern
is probably hampered by inadequate sample sizes (Banaszak et al. 1998).
A positive relationship between MAAs and UV-R is bolstered by studies that
have either enhanced or reduced UV-R intensities and found a requisite increase
or decrease in MAA concentrations. A total of 12 different coral reef species
have been investigated in this manner (Table 5.3). Of these, 8 (67%) exhibited
a response consistent with prediction 1. It should be noted that with 2 of the
species, Pocillopora damicornis and Stylophora pistillata, multiple studies ob-
tained disparate results (Table 5.3). When combined, data from the studies cited
earlier indicate that current evidence supports prediction 1 of the fitness cost
hypothesis.
Prediction 2: MAAs Occur in Greater Concentrations in Portions of the

Organism Exposed to Higher Intensities of UV-R
Studies investigating distributions of MAAs within individuals of coral reef
species are numerically scarce but taxonomically diverse, encompassing 1
Caribbean (Muszynski et al. 1998) and 1 Pacific (Jokiel, Lesser and Ondrusek
TABLE 5.3. Studies quantifying MAA concentrations in coral reef organisms after
manipulation of UV -R levels.
Field! UV-R MAA
Species lab source concentration Reference
Acropora valida Lab Sun No difference Glynn et al. (1992)
Cassiopeia xamachana Lab Lamps UVR higher Banaszak and Trench (1995)
Clavularia sp. Lab Sun UVR higher Shick et al. (1991)
Eucheuma striatum Lab Sun UVR higher Wood (1989)
Montastrea annularis Field Sun No difference Gleason and Wellington (1993)
Montipora verrucosa Lab Sun UVR higher Scelfo (1986)
M. verrucosa Field Sun UVR higher Kinzie (1993)
Palythoa caribaeorum Lab Sun UVR higher Lesser et al. (1990)
Phyllodiscus semoni Lab Sun No difference Shick et al. (1991)
Pocillopora damicomis Lab Sun No difference Glynn et al. (1992)
P. damicomis Lab Sun UVR higher Jokiel and York (1982)
P. damicomis Lab Sun UVR higher Jokiel et al. (1997)
Porites astreoides Field Sun UVR higher Gleason (1993a)
Stylophora pistillata Field Sun No difference Gattuso (1987)
S. pistillata Lab Lamps UVR higher Shick et al. (1999)
Zoanthus padfus Lab Sun No difference Scelfo (1985)
Whether each study was conducted in the field or laboratory is noted along with the UV -R source.
Changes in MAA concentrations occurring after the manipulations are noted in the "MAA Concen-
tration" column.
"No difference" indicates either that individuals exposed and shielded from UV-R showed similar
MAA concentrations or that enhancing UV -R levels resulted in no increase in MAAs. In contrast, a
response of "UV-R higher" indicates greater concentrations of MAAs in individuals exposed to more
intense UV-R.
1997) coral species, 12 species of holothuroid echinoderms (Shick et aI. 1992),

the giant clam Tridacna crocea (Ishikura, Kato and Maruyama 1997), and the
red alga Eucheuma striatum (Wood 1989). In all cases, MAAs were found in
higher concentrations in polyps, tissues, or structures exposed to more direct sun-
light. For example, in the Caribbean coral Montastrea annularis, MAA concen-
trations on the top of the colony (parallel with the ocean surface) were more than
twice those found on the east- or west-facing sides (perpendicular to the ocean
surface) (Muszynski et aI. 1998). Likewise, MAAs in coral reefholothuroids oc-
cur predominately in epidermal tissues as opposed to the inner body wall and
longitudinal muscles (Shick et aI. 1992). Thus, while studies are not plentiful,
those that have been conducted to date clearly support prediction 2.
Prediction 3: Slower-Growing Species Maintain Higher Static

Concentrations of MAAs than Faster-Growing Species
This prediction has not been explicitly tested, but we can conduct a tentative
analysis of the relationship between MAA concentrations and growth rates us-
ing published data. In investigating this relationship I accumulated information
for all species for which both MAA concentrations and growth rates have been
determined. To avoid confounding the results with depth-related variation, my
search was limited to those species that have been sampled in shallow water be-
tween 1 and 3 m of depth. Furthermore, to minimize artifacts resulting from dif-
fering data collection methods, I included only studies that standardized MAA
concentrations to milligrams of soluble protein.
A total of 10 species met the foregoing criteria: 5 from the Caribbean (Glea-
son 1993a; Banaszak et aI. 1998; Muszynski et aI. 1998; Gleason et aI., in prepa-
ration), 3 from Hawaii (Banazsak et aI. 1998), and 2 from the Australian Great
Barrier Reef (Dunlap and Chalker 1986; Shick et al. 1995). If multiple studies
used similar techniques to quantify MAA concentrations, I averaged across all
studies. Growth rates for all species were from the review by Huston (1985b),
except for Porites astreoides, which was measured by Gleason (1993a). Results
indicated a negative trend between MAA concentrations and growth rates (Fig-
ure 5.2). These results should be viewed with caution, however, because of the
low number of species analyzed and the fact that sample sites likely differ widely
in terms of their UV-R environment. Nevertheless, these crude results are con-
sistent with prediction 3 and suggest that studies explicitly testing this negative
relationship are warranted.
There are two other inferences that can be made regarding the negative rela-
tionship between coral growth rate and the concentration of UV-R-absorbing
compounds. The first is that producing large quantities of MAAs exacts a cost
in terms of resources allocated to growth. The second is that faster-growing
species generally exhibit higher photosynthetic rates and so can respond more
rapidly to changes in UV -R intensity through enhanced production of MAAs by
symbiotic algae. Neither of these questions has been tested experimentally.
375:h
374
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t::
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600
0
c..
-
CI 500
E
I /) 400
<C
<C
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"0
CP
200 •
E
t:: •
100 •
0 •
0 10 20 30 40
Growth Rate (em year- 1)
FIGURE 5.2. The relationship between coral growth rate and concentrations of UV-R-
absorbing mycospore-like amino acids (MAAs) within the tissues. Although not signifi-
cant (p = 0.17), these data are best explained by an inverse second-order polynomial where
y = (-94.9/x2) + (941.9/x) + 104.5 and ,-2 = 0.39. Details on how these data were ac-
cumulated are provided in the text.
Prediction 4: MAAs Cannot Be Maintained at Levels Sufficient to Prevent

UV -R Damage if the Organism is Severely Stressed by Other Abiotic Factors
The only tests of the fourth prediction are from studies investigating interactive
effects of temperature and UV-R in coral bleaching. To date there have been two
such studies conducted in the laboratory, encompassing three species. Lesser et
al. (1990) showed that concentrations of MAAs in the Caribbean zoanthid Pa-
lythoa caribaeorum decrease when exposed to an average temperature of 31°C
for 2 days. This temperature certainly exerts stress on many symbiotic antho-
zoans because it is generally believed that temperatures in excess of 30°C lead
to coral bleaching. Likewise, Glynn et al. (1992) observed a significant decline
in MAA concentrations in the Pacific coral, Acropora valida, under a similar
temperature regime. In contrast, no effect of temperature on MAA concentra-
tions was observed in the Pacific coral Pociliopora damicornis even though it
was exposed to conditions nearly identical to that of A. valida. I conclude from
these studies that the relationship between MAA production and abiotic stressors
is still open to question and is in need of further investigation.
Overall, the foregoing analysis suggests that there is substantial evidence sup-
porting the concept that MAAs are costly to produce. In symbiotic anthozoans
existing under adequate light conditions, zooxanthellae can provide more than
100% of the carbon needed for host animal growth and respiration. Given this,
it is unlikely that carbon is the limiting element for MAA production. I would
suggest instead that nitrogen may be the component in short supply. Nitrogen is
one of the major limiting nutrients in marine ecosystems (D'Elia and Wiebe 1990)
and is an integral component of MAAs. Before this question can be laid to rest,
however, experiments testing the cost of producing MAAs, in terms of trade-offs
with life history parameters such as growth and reproductive output, need to be
completed. Unfortunately studies of this type are often confounded by the fact
that production of the protective compounds can only be induced if the animal
is exposed to the stress that induces it. Obviously this relationship makes it dif-
ficult to partition negative responses resulting from allocation of resources to
MAA production from those attributable to UV-R exposure.
Carotenoids
Although much knowledge has been acquired about the existence and function
of MAAs in coral reef organisms, it is unclear how significant these compounds
are relative to the entire arsenal of UV-R protective mechanisms. Furthermore,
when it comes to the ability of coral reef organisms to resist UV-R, virtually
nothing is known about carotenoid-like compounds. These compounds do not
absorb in the UV-R region of the light spectrum so it is unlikely that they pre-
vent this radiation from reaching critical tissues. Rather, as pointed out previ-
ously, one of the consequences of UV-R exposure, especially in photosynthetic
organisms, is production of cytotoxic reactive oxygen species such as singlet oxy-
gen, hydrogen peroxide, and other oxygen-centered radicals that can damage cel-
lular components, especially lipids (reviewed in Dunlap and Shick 1998).
Some MAAs, especially mycosporine glycine, have been shown to function
as mild antioxidants (Dunlap and Yamamoto 1995; Dunlap and Shick 1998), but
their ability to quench reactive oxygen species from biological systems appears
to be nowhere near the capacity of carotenoids (Shick, Lesser and Jokiel 1996).
Carotenoids function as photoprotectants by quenching energy from the excited
state of chlorophyll and deactivating singlet-state oxygen. In both cases,
carotenoids exert their photoprotective action by accepting energy and dissipat-
ing it in the form of heat as they return chemically unchanged to their ground
state (Porra, Pfundel and Engel 1997).
Progress has recently been made in understanding the role of carotenoids in
protecting the photosynthetic apparatus of zooxanthellae from chronic (i.e., irre-
versible) light-induced photoinhibition (Brown et a1. 1999). The primary carot-
enoids identified in reef-building corals include peridinin, diadinoxanthin, dia-
toxanthin, and ~-carotene (Ambarsari et a1. 1997). In the intertidal coral
Goniastrea aspera, two of these compounds, diadinoxanthin and diatoxanthin,
show diurnal fluctuations with diatoxanthin concentrations increasing in direct
relation to solar irradiance (Brown et a1. 1999). Conversion from diadinoxanthin
to diatoxanthin with increasing light intensity may allow dissipation of excess
absorbed light energy as heat and is analogous to the violaxanthin-zeaxanthin cy-

cle of higher plants (Porra, Pfunde1 and Engel 1997).
At present, the role UV -R plays in this cycle is unclear because the experi-
ments by Brown et al. (1999) did not partition effects of photosynthetically ac-
tive radiation (PAR, 400-700 nm) from UV-R. It is likely, however, that any
light energy that sends chlorophyll into an excited state and produces singlet oxy-
gen would stimulate this cycle, resulting in a photoprotective response. Investi-
gations along these lines are warranted, especially because corals exposed to high
temperatures and UV-A exhibit the largest decrease in photosynthetic efficiency
(Fitt and Warner 1995).
Other Antioxidant Compounds

In addition to carotenoids, the primary antioxidants in reef organisms are super-
oxide dismutase (SOD), ascorbate-specific peroxidases, and catalase. In cnidar-
ians possessing zooxanthellae, a protective role for these compounds against ox-
idative damage to chlorophyll has often been inferred by measuring increases in
their activity under enhanced levels of irradiance or UV-R in isolated zooxan-
thellae or the intact symbiosis (Lesser 1989, 1996; Lesser and Shick 1989; Shick,
Lesser and Stochaj 1991; Shick et al. 1995). Furthermore, spiking the surround-
ing water with antioxidant compounds improves photosynthetic performance. For
example, in cultured Symbiodinium bermudense isolated from the tropical
anemone Aiptasia pallida, the photosynthetic capacity of algae exposed to 31°C
and UV-R from fluorescent lamps was enhanced by 37% when ascorbate and
catalase were added to the surrounding medium (Lesser 1996).
Negative correlations between light intensity and activity of antioxidant en-
zymes is also consistent with a photoprotective role for these compounds. In the
reef-building coral Acropora microphthalma, a decline in activity of antioxidant
enzymes with increased depth in both zooxanthellae and animal tissues is thought
to parallel photodynamic production of reactive oxygen species resulting from
the visible light and UV -R gradient. This pattern does not occur in all cases.
Shick, Lesser and Stochaj (1991) found no difference in antioxidant activity be-
tween 4- and 17-m depth in the octocoral Clavularia sp. They explained this re-
sult as reflecting compensatory responses in zooxanthellae to maintain high pho-
tosynthetic rates. Specifically, higher chlorophyll concentrations in zooxanthellae
from Clavularia sp. at 17-m depth compensate for the reduced light intensity and
ultimately raise total photosynthetic rates. As a consequence, net oxygen flux in
host tissues from 4- and 17-m depth may be similar and require comparable anti-
oxidant enzyme activity.
The studies just cited provide strong indirect evidence that UV-R exposure re-
sults in accumulation of reactive oxygen species in tropical symbiotic cnidari-
ans, but direct measurements of oxygen radicals have only been carried out with
the temperate anemone Anthopleura elegantissima. Dykens et al. (1992) used
electron paramagnetic resonance spin trapping to show that hydroxyl radicals
start accumulating immediately on exposure of this anemone to visible light sup-
plemented with UV-R. Interestingly, radicals were also detected in apozooxan-

thellate anemones, indicating that this process is not dependent on photosyn-
thetically induced hyperoxia. This result should not be surprising considering that
free radicals and other active oxygen species are natural by-products of biolog-
ical redox reactions. However, it suggests that studies investigating UV-R effects
on coral reef organisms should be expanded to include nonphotosynthetic species,
such as some species of sponges and tunicates, that occupy sunlit reef habitats
and are inevitably exposed to high intensities of UV-R.
Photo repair
In general, the process of photoreactivation involves a single enzyme that rec-
ognizes and monomerizes cis-syn cyclobutane dimers in DNA (reviewed in Kar-
entz 1994). This enzyme system requires exposure to long-wave UV-R (mainly
UV-A) or short-wave visible light (400-480 nm) for activation. In reef-building
corals from the Great Barrier Reef, Siebeck (1981, 1988) found that exposing
these animals to UV-R and then irradiating them with white light increased
UV-R tolerance sixfold. As expected, the wavelengths most effective in this pro-
cess were those in the blue-violet region of the spectrum.
Beyond Siebeck's initial studies, there has been virtually no progress in elu-
cidating the role of DNA photorepair in the UV-R tolerance of coral reef or-
ganisms. This research gap may have arisen from our intense focus on cnidari-
ans possessing photosynthetic endosymbionts. With all the fears regarding coral
bleaching and coral declines, the major research focus has been on identifying
underlying factors that destabilize coral-algal symbioses. As can be seen from
many of the studies cited previously, this emphasis has led to a host of investi-
gations using photosynthetic rates, rather than DNA damage and subsequent pho-
toreactivation, as the baseline. Integrating the latter into coral reef research pro-
grams may prove useful in gaining a fuller understanding of how UV-R impacts
symbiotic as well as nonsymbiotic reef organisms.
UV-R and Distributional Patterns of Coral Reef Species

It should be apparent from the previous sections that UV-R penetrates to con-
siderable depths on many coral reefs and that reef organisms allocate substantial
resources to preventing and repairing UV-R damage. Given this background, it
is logical to consider impacts of UV-R at the population and community levels.
Coral reefs have historically been viewed as space-limited systems where either
disturbance from abiotic factors, mainly the frequency and severity of storms, or
biotic interactions, mainly predation and competition, have determined commu-
nity structure and species diversity (Glynn 1976; Connell 1978; Huston 1985a).
In contrast, the role chronic disturbances, such as UV-R, play in determining
population- or community-level patterns has received less attention. We can ad-
dress the notion of whether UV-R sets limits on the distributions of coral reef
species by categorizing these organisms into the following groups: (1) het-
erotrophic, sessile species that are more cryptic and occupy areas protected from
direct sunlight; (2) sessile species inhabiting areas exposed to direct sunlight; and
(3) mobile animals having the capabilities to behaviorally avoid UV-R. In the
following sections, I concentrate on the first two groups because these may be
the species most vulnerable to UV -R damage.
Cryptic Heterotrophic, Sessile Species

This group includes many species of sponges (especially boring sponges), tuni-
cates, bryozoans, polychaetes, bivalves, and nematodes, as well as many other
invertebrate taxa. As pointed out by Jokiel (1980), shallow reef zones are often
depauperate in epifauna except in shaded locations. This observation suggests
that UV-R may have an impact on the distributions of organisms in shallow reef
zones. In fact, for many of these species, including encrusting and branching
sponges and tunicates, Jokiel (1980) clearly showed that residing in cracks and
crevices or on the lower sides of substrates is negatively correlated with UV-R
resistance.
In a now-classic set of simple but elegant experiments, Jokiel incorporated
acrylic UV-R cutoff filters to either expose or protect sessile benthic epifauna
from UV-R. All the species he tested showed negative effects within 4 days of
UV -R exposure and all, except one species of bryozoan, died within 2 weeks. It
is apparent from his studies that these species lack the UV-R protective mecha-
nisms to tolerate the high intensities of UV-R that penetrate clear tropical
waters. The evolutionary question that arises with these species is whether it is
UV -R intolerance or avoidance of predation and competition that originally drove
these species into shaded, cryptic habitats.
Sessile Species Exposed to Direct Sunlight

Organisms in this category include all photosynthetic species, including corals
and benthic algae, and many nonphotosynthetic species, such as many sponges
and tunicates, that live in open reef habitats. For most of these organisms, the
impact of UV-R on their distributions has not been extensively investigated. As
with much other research concerning UV-R effects on coral reefs, the best stud-
ies to date at the population level have been completed on reef-building corals.
Colonies of the ubiquitous Caribbean coral, Poritis astreoides, occur as either
yellow/green or brown morphs (Gleason I993a). In previous studies I have found
that UV-R has effects that are consistent with the distributions of these color
morphs in shallow water (Gleason I993a). Specifically, transplant experiments
showed that yellow/green morphs of this species moved from 6- to I-m depth
and exposed to UV-R show no differences in growth rates, zooxanthellae densi-
ties, or algal division rates compared to yellow/green morphs protected from
UV -R. In contrast, brown morphs show significant reductions in colony and al-
gal growth rates when exposed to high intensities of UV-R. These results are
concordant with the concentrations of MAAs found within these two morphs:
green morphs contain significantly higher concentrations of MAAs, especially
the compound asterina-330. In addition, green morphs are usually much more
common in shallow reef zones (::52-m depth) where UV-R intensities are high.
Further investigation into the ecology of P. astreoides provides an intriguing
example of how UV-R may interact with other abiotic parameters to control
species distributions. Inorganic sediments suspended in the water column and
settling onto reef surfaces can exert control on the distributions and abundances
of coral species through both lethal and sublethal effects (reviewed in Gleason
1998). Examination of morph-specific distributions of P. astreoides at several
sites on St. Croix, U.S. Virgin Islands, suggested that at depths greater than 2 m
brown colonies may be favored in areas exposed to greater sediment stress. These
observations were confirmed by correlating sedimentation rates with color morph
abundance patterns and conducting sediment shedding experiments with both
colony types in the laboratory (Gleason 1998).
Simultaneous consideration of the effects of UV -R and sedimentation rates on
the distributional patterns of yellow/green and brown P. astreoides leads to the
following three predictions: (1) if UV-R intensities are high and sedimentation
rates are low, yellow/green colonies will be in greater relative abundance; (2)
under conditions of low UV-R intensities and high sedimentation rates, brown
colonies will be relatively more abundant; and (3) if both UV-R intensities and
sedimentation rates are low then the color morphs co-occur in approximately
equal numbers (Figure 5.3). These results discussed in this chapter provide sup-
port for the contention that the wide array of morphology observed within species
of reef-building corals is maintained by disruptive selection differentially favor-
ing phenotypes across a range of habitats. More specifically, it shows that
UV-R may be one of the factors selecting for phenotypic variation across envi-
ronments.
The foregoing observations explain the distributional patterns seen in P. as-
treoides but provide no insight about the stage of the life cycle at which UV-R
has its greatest impacts. Elimination of brown P. astreoides from high-UV-R en-
vironments could arise through detection and avoidance of UV-R during the lar-
val stage or UV-R-induced mortality following settlement. Many sessile marine
species, including P. astreoides, have a pelagic larval stage that results from
spawning of eggs and sperm into the water column or the release of brooded lar-
vae. The role that UV-R plays during larval dispersal and settlement, although
critical to understanding the ecological significance of this radiation in coral reef
ecosystems, has not been extensively investigated.
In one of the few studies investigating UV -R effects on coral larvae, we found
that larvae from species occupying a broad depth range may not be created equal
when it comes to UV-R resistance (Gleason and Wellington 1995). The brood-
ing Caribbean coral, Agaricia agaricites, occurs at depths ranging from less than
3 to more than 30 m. Concentrations of MAAs in planula larvae of this species
are inversely correlated with depth: larvae from adults at 3-m depth contain sig-
nificantly higher concentrations of MAAs than those spawned at 24-m depth
UVR Intensity
~
o
[
~
Yellow/Green Yellow/Green and Brown [
(Aster!na-330) g
1
Sedimentation
Brown Yellow/Green and Brown

(Sediment Shedding)
High UV, LowUV,

! LowUV,
1
Low Sediment High Sediment Low Sediment
FIGURE 5.3. Summary of how UV-R and sedimentation rates interact to shape the distributions of yellow/green and brown color morphs of the coral
Porites astreoides. Throughout the flow chart, the color morph predicted to be most abundant under a particular set of abiotic conditions is indi-
cated. In situations where both yellow/green and brown colonies are present, abundances are expected to be approximately equal. Where appro-
priate, the feature allowing the color morph to respond to a particular abiotic factor is given in parentheses. At the base of the flow chart are the
combined factors for which yellow/green and brown morphs are predicted to be well adapted.
(Gleason and Wellington 1995). Furthermore, when larvae from both depths are
exposed to natural levels of PAR and UV-R at 3-m depth, larvae from deeper
water suffer significantly higher mortality. These results indicate that larvae
spawned from deeper-water corals may be relegated to settling in deeper water
or in shallow water only in shaded locations.
Given the results found with both P. astreoides and A. agaricites, two keys to
successful recruitment of coral larvae may be the capacity to detect and avoid
habitats with high levels of UV-R and the ability to quickly enhance MAA con-
centrations, if needed, after settlement. Preliminary experiments I have conducted
with the brown morph of P. astreoides suggested these larvae have UV-R re-
ceptors and can potentially avoid high intensities of this radiation while dispers-
ing in the water column or at the time of settlement (Figure 5.4). In contrast, a
time-course experiment investigating changes in MAA composition under
UV-R exposure in newly settled coral recruits has never been completed but is
needed if we are to fully understand the constraints this physical parameter places
on larval recruitment.
The studies cited here provide examples of how UV-R may contribute to
population-level patterns on coral reefs. Unfortunately, studies of UV-R effects
_ UV Present
40 c=:J UV Absent
*~
*, - **, -
*r- **r-
35 n.s. *
,- r-
30
III
..!!! 25 n.s.
::::I -r-
c
1"11
ii 20
=11=
15
10
5 - '-'-- '-'-- '-'-- '-'-- - -

10:30 11:00 11:30 12:00 12:30 13:00 13:30 14:00
Time of Day
FIGURE 5.4. Distribution of Porites astreoides larvae at 30-min intervals in petri dishes in
which one-half of the dish was exposed to UV-R (black bars) and the other half was
shielded (white bars) with UV-R-absorbing acrylic. A total of 10 dishes contained five to
seven larvae (planulae) each, and all dishes were placed in full sunlight. Deviations from
random larval dispersion were tested for at each time interval using the chi-square test.
Note that the observation at 1400 was made after all dishes had been completely covered
with UV-R-absorbing acrylic for 30 min. Asterisks indicate significance levels as follows:
*, p < 0.05; **, p < 0.01
on benthic macroorganisms go to no higher levels of ecological complexity. In

contrast, recent studies on benthic tropical diatom assemblages show negative,
but temporary, impacts at the community level. Santas et al. (1998) allowed al-
gae to settle on substrate in situ and monitored accumulation of diatom assem-
blages over a period of 6 weeks. Substrates were exposed either to UV-B,
UV-A, and PAR or to UV-A and PAR only using acrylic filters. Results showed
reduced productivity on substrates exposed to UV-B for the first 4 weeks but
equal productivity during weeks 5 and 6. These results suggest that tropical ben-
thic diatoms are most susceptible to UV-B during the spore establishment and
vegetation stages and that long-term effects of UV-B on primary productivity do
not occur. In contrast to results for productivity, high species diversity was main-
tained throughout the experiment, and UV-R exposure may actually keep diver-
sity high by restricting abundances of competitively dominant species. Whether
these results can be extrapolated to sessile macrofloral and macrofaunal com-
munities is still open to question.
Conclusions and Recommendations

A wealth of information on the relationship between UV-R and coral reef or-
ganisms has been accumulated, especially during the past 20 years. This data-
base, much of it initially spawned by fears over the consequences of ozone de-
pletion, has provided insight into the penetration of UV-R in coral reef waters,
the effects of UV-R on the physiology of reef organisms, especially corals, and
adaptations used by reef organisms to counter UV-R-induced stresses. It is now
time, however, to consolidate our efforts and fill in the gaps. In this regard, I
would recommend that we place significant efforts and resources into three
areas.
First, we should standardize UV-R instrumentation. Using a myriad of detec-
tion devices, investigators have confirmed that UV-R penetrates to considerable
depths on many coral reefs. Unfortunately, using different devices also prevents
comparisons from reef to reef and region to region. Given the current concerns
regarding coral reef declines, developing an instrument that is reliable, afford-
able, and can be used worldwide would do much to advance our understanding
of the significance of UV -R in reef systems.
Second, we should identify the role of carotenoids and photoreactivation in re-
sistance of reef organisms to UV-R. Currently, we do not know which UV-R pro-
tective mechanism is most common or furnishes the greatest resistance because
most research has concentrated on MAAs and antioxidant compounds such as su-
peroxide dismutase and peroxidases. These studies should continue, but we should
also expand our investigations to include other UV -R protective mechanisms. With
the advent of molecular techniques, we should be especially poised to move into
the area of DNA photorepair. Along these lines, we also should attempt to iden-
tify the costs to organisms, in terms of energy and other resources, to prevent UV-
R-induced biological damage. Doing so will provide an understanding of how
UV-R has played into the life history evolution of reef organisms.
Finally, we should view the effects of UV-R within the context of other abi-
otic stressors on coral reefs and attempt to conduct studies that allow extrapola-
tion to the population and community level. At this point we only have a cur-
sory understanding of how UV-R may interact with other physical factors, such
as temperature, to cause physiological stress. Furthermore, it may be worthwhile
to remind ourselves that coral reefs contain numerous other and widely diverse
species besides corals. Understanding the role ofUV-R in coral communities will
only come by greatly expanding our studies outside the realm of reef-building
corals to other animal and algal taxa.
Acknowledgments. This chapter represents a compilation of many years of re-

search, countless discussions with colleagues at scientific meetings, and fruitful
collaborations in the field. At the risk of leaving many names out, I would like
to thank the following for their substantial and varied contributions: Britt An-
derson, Ron Burton, Blaine Cole, Walter Dunlap, Peter Edmunds, Elizabeth Glad-
felter, Ruth Gates, Debbie Gleason, Malcolm Hill, Jeff Miller, Steven Miller,
Kenyon Mobley, John Ogden, Lock Rogers, Otto Rutten, Malcolm Shick,
Stephanie Schopmeyer, John Schmerfeld, David Ward, Gerard Wellington, Di-
ane Wiernasz, and Tom Wilcox. Much of my UV-R work has been funded, and
continues to be funded, by grants from the National Undersea Research Program
at the University of North Carolina at Wilmington. Without their financial and
logistical support, much of this work would have been impossible. Financial sup-
port has also been provided by Sigma Xi, Houston Underwater Club Seaspace
Scholarships, University of Houston Department of Biology Research Fellow-
ships, University of Houston Coastal Center, Georgia Southern University Fac-
ulty Research Fund, as well as a National Science Foundation Grant to G.M.
Wellington for some of the earlier studies related to coral bleaching.
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6
Ultraviolet Radiation and Aquatic
Microbial Ecosystems
DONAT-P. HADER
Solar ultraviolet radiation is easily blocked by high concentrations of dissolved

and particulate organic matter, but it has been found to penetrate to ecologically
significant depths in clear freshwater and marine ecosystems (USEPA 1987;
Smith et al. 1992; Scully and Lean 1994; Hader 1995a; Booth et al. 1997; Coohill,
Hader and Mitchell 1996). The Antarctic ozone hole has continued to grow in
size and depth, and measurements during the past few years have shown dra-
matic stratospheric ozone depletion also over the North Pole. At high and mid-
latitudes, moderate decreases in total ozone column have been found with re-
sulting increases in erythemally weighted surface UV radiation of about 7% over
the midlatitudes of the Northern Hemisphere in winter and spring and about 4%
in summer and fall as compared with the values of 1970. For the Southern Hemi-
sphere midlatitudes, an erythemally weighted increase in surface solar UV of
about 6% has been determined on a year-round basis (Madronich et al. 1998).
Although current stratosphere ozone levels are expected to be near their low-
est level and thus solar UV-B at its peak, the maximum may be shifted well into
the current century because of noncompliance of several countries with the Mon-
treal protocol and its amendments (London, Vienna, and Copenhagen) as well as
illegal production, trafficking, and emission of chlorofluorcarbons. Consequently,
increasing amounts of solar UV-B are expected to penetrate into the euphotic
zone where phytoplankton productivity is highest. Furthermore, altered ratios of
UV-B:UV-A:PAR radiation (PAR, photosynthetic available radiation) may af-
fect the fine-tuned, light-controlled responses of aquatic microorganisms, such
as photosynthesis, photoorientation, photoinhibition, and photoprotection (Smith
et al. 1992; Hader et al. 1995; Gerber, Biggs and Hader 1996; Jimenez et al.
1996; Hader 1997a,b). Aquatic ecosystems may experience significant stress as
the result of a changed spectral distribution in the underwater light climate (lASC
1995). UV-B and UV-A control growth, productivity, and development by af-
fecting a number of different molecular targets in the irradiated cells that may
experience an overload of their protective and repair mechanisms.
Substantial increases in solar UV may result in decreased biomass productiv-
ity in aquatic ecosystems. Reduced primary productivity would be relayed
through all levels of the intricate food web, including crustaceans, fish, mollusks,
150
6. Ultraviolet Radiation and Aquatic Microbial Ecosystems 151
birds, and mammals, and result in decreased food production for humans (Hader
et al. 1995; Hader 1997d; Hader and Worrest 1997). Because aquatic ecosystems
match terrestrial ecosystems in taking up atmospheric carbon dioxide, reduced
sink capacity may occur (Ducklow et al. 1995; Takahashi, Takahashi and Suther-
land 1995; Takahashi et al. 1997). The role of oceanic carbon dioxide uptake in
global warming is well recognized (Sarmiento and Le Quere 1996; Thomson
1997), but the quantification of the possible impact of ozone depletion on car-
bon dioxide uptake is still uncertain, and a better understanding is badly needed.
Another area of concern is changes in species composition and ecosystem in-
tegrity. Earlier studies have shown that organisms have different UV sensitivi-
ties, so that under increased UV stress some species are more prone than others
to be affected. There is a clear correlation between cell size and stress; smaller
organisms are more impaired than larger ones.
Numerous investigations on UV-B-related damage of aquatic ecosystems have
been published in the past few years (Nolan and Amanatidis 1995). Reviews on
several aspects of UV effects on aquatic ecosystems include aquatic ecosystems
in general (Hader 1997c; Hader and Worrest 1997; Hader et al. 1998), the role
of MAAs in marine organisms (Dunlap and Shick 1998), phytoplankton (Cullen
and Neale 1997a,b,c; Hader 1997a), macroalgae (Franklin and Foster 1997; Hader
and Figueroa 1997), coral bleaching (Shick, Lesser and Jokiel 1996; Lesser 1996),
and lake acidification and UV penetration (Williamson 1995, 1996).
Measurement of UV Radiation in the Water Column

The penetration of UV and PAR into the water column needs to be measured to
determine the effects of solar radiation on aquatic ecosystems (Montecino and
Pizarro 1995; Bjorn et al. 1996). The water column shows large temporal and
spatial differences and variations in the concentrations of dissolved and particu-
late absorbing substances. Jerlov (1968) has classified marine waters into nine
types of coastal and five types of open ocean waters depending on their trans-
mission. The ratio between the 0.1% depths for UV-B and PAR can be used to
calculate the effects on organisms in the euphotic zone (Piazena and Hader 1997).
Recent developments allow accurate measurements of the underwater light field
(Morrow and Booth 1997). Dissolved organic matter as well as organic and in-
organic particulate material mainly attenuate the ultraviolet radiation in the wa-
ter column, but reports on the underwater light field in coastal habitats are scarce,
particularly in the UV-B range. In addition, algal canopies modify the spectral
composition by absorption and scattering of the incident light. Figure 6.1 shows
the spectral distribution of solar radiation in the water column of the Baltic Sea
at different depths.
Recently, a network of three-channel (UV-B, UV-A, PAR), broad-band filter
dosimeters (ELDONET [European Light Dosimeter Network]) has been installed
in Europe from Abisko (Northern Sweden) to Gran Canaria (Santas, Koussoulaki
and Hader 1997; Hader et aI., 1999). Two of the instruments are located at high
152 Donat-P. Hader
E
c::
Q) depth:
C,.)
c:: 1: 0.3m
.~ 2: 1.0m
"C
~
3: 2.0m
10....
4: 3.0m
5: 4.0m
6: 5.0m
7: 7.0m
8: 10.0m
300 350 400 450 500 550 600 650 700 750 800
Wavelength [nm]
FIGURE 6.1. Spectral distribution of scalar solar irradiance at different depths at Gull-
marsfjordeniKattegat measured during local noon under cloudless sky on May 27, 1994.
altitudes and seven are located under water where they operate in conjunction
with a terrestrial counterpart. In addition to Europe, instruments have been
installed in Egypt, India, Japan, New Zealand, and Argentina (Figure 6.2). The
data are transmitted to a server in Pisa and are available on the Internet (http://
power.ib.pi.cnr.it:80/eldoneti and http://www.biologie.uni-edangen.de/botanikll
htmlleldonet.htm). Other networks have been installed, e.g., the U.S. National
Science Foundation UV Spectroradiometer Monitoring Network (http://www.
biospherical.com), including stations in San Diego (California), Ushuaia (Ar-
gentina), Barrow (Alaska), and Antarctica (South Pole, Palmer, and McMurdo).
The optical characteristics of the water column can be obtained from satellite
data (e.g., CZCS (Coastal Zone Color Scanner) and SeaWiFS (Sea-viewing Wide
Field-of-view Sensor). The instruments cover only the visible range, but attempts
have been made to extrapolate into the UV range. Great efforts have been made
to develop techniques for measuring algal biomass by using remote sensors, e.g.,
by quantifying chlorophyll in surface oceanic waters (Brown, Esaias and Thomp-
son 1995). One major obstacle for remote monitoring is the fact that mainly the
surface signal is determined whereas deeper layers do not contribute significantly
to the signal (Piazena and Hader 1997). A profound knowledge of the vertical
distribution of phytoplankton as well as the composition of the phytoplankton
may help to derive a quantitative analysis of biomass productivity (Piazena and
Hader 1997).
FIGURE 6.2. Map with the installed instruments of the ELDONET (European Light Dosime-
ter Network) network. Circles, terrestrial stations; triangles, underwater instruments;
squares, high-altitude stations.
Behrenfeld and Falkowski (l997a,b) have developed models to estimate pho-

tosynthetic activity derived from satellite-based chlorophyll concentration. If
equivalent parameterizations are used for satellite-derived chlorophyll and the
maximum chlorophyll-specific carbon fixation rate, estimates of global annual
primary production were found to be fairly accurate.
Effects of Solar UV Radiation on Dissolved

Organic Material
Dissolved organic carbon (DOC) is a major component that decreases the pene-
tration of solar radiation into the water column by absorption and scattering. Most
of the DOC is of terrestrial origin and therefore mainly found in freshwater and
coastal marine ecosystems. This group of substances is relatively resistant to
chemical degradation and other external forces (Naganuma et al. 1996); how-
154 Donat-P. Hader
ever, humic substances and other components of DOC are photolytically degraded
by solar UV radiation and break down into such components as formaldehyde,
acetaldehyde, glyoxylak, and pyruvate. These breakdown components are read-
ily taken up by bacterioplankton and heterotrophic nanoflagellate communities
(Wetzel, Hatcher and Bianchi 1995; Wangberg et al. 1996).
As a consequence of this process, increased breakdown of DOC and subse-
quent consumption of the small molecular fragments by bacteria increases the
UV-B penetration into the water column. However, the sequence of events is
more complex: close to the surface, solar UV radiation photolyzes DOC. Si-
multaneously, it affects bacterioplankton and impairs bacterial ectoenzyme ac-
tivity, important for the uptake of the fragments (Herndl 1997). Only when both
bacteria and the photolyzed DOC are circulated to deeper layers does the uptake
rate increase. During photolysis of DOC, photosensitizers are generated from the
chromophoric groups of colored dissolved organic matter (cDOM). Absorption
of UV radiation causes the production of reactive oxygen species or free radi-
cals. Other important factors that affect solar penetration into the water column
include acidification and eutrophication, both of which have synergistic and an-
tagonistic effects (see Chapter 2, this volume).
The problem is more complicated because UV-B has been found to be more
damaging for small phytoplankton organisms (Karentz et al. 1994) and bacteri-
oplankton (Herndl 1997). However, a recent study of plankton in a lake indi-
cated that cells larger than 2 /Lm were twice as sensitive to solar UV -B as smaller
ones (Milot-Roy and Vincent 1994).
Bacterioplankton and Picoplankton

Bacterioplankton is no longer regarded solely as a final decomposer of organic
material. Its productivity is much greater than previously thought because of high
division and turnover rates (Fuhrman and Noble 1995) and is comparable to, or
exceeds, phytoplankton primary productivity (Herndl 1997). In the "microbial
loop hypothesis," bacterioplankton is seen in the center of a food web (Pomeroy
and Wiebe 1988). Bacterioplankton is a key player in the global carbon cycle
taking up dissolved organic carbon (DOC) and remineralizing the carbon. As in
all other aquatic organisms, the effect of solar UV on bacterioplankton depends
on the attenuation in the water column and the depth. Bacterioplankton are pas-
sively moved around in the mixing layer, and the time at the surface or at depth
defines the exposure hazard. Bacterioplankton lack UV screening pigments (see
following); such pigments are probably useless because of their small size (Kar-
entz et al. 1994; Garcia-Pichel 1994). Therefore, bacterioplankton are more af-
fected by UV-B stress than larger (eukaryotic) organisms.
A case study in the Gulf of Mexico has shown that UV exposure produces
about double the amount of cyclobutane dimers in phytoplankton (Jeffrey et al.
1996a,b). This damage is partially repaired by photoreactivation (Nicholson
1995), provided that the cells are allowed sufficient time at greater depth where
the UV -Alblue radiation (360-430 nm) activates the photolyase enzyme. Also,
the ectoenzymes excreted by the bacteria for the cleavage of external organic
matter are impaired by solar UV-B (Miiller-Niklas et al. 1995). Bacterioplank-
ton serves as food for heterotrophic flagellate picoplankton, forming the next step
in the food web. The ecological consequences of solar UV are even more com-
plicated because the flagellate picoplankton and viruses that prey on the bacte-
ria likewise show a high sensitivity to solar short-wavelength radiation (Som-
maruga, Oberleiter and Psenner 1996).
Cyanobacteria
Despite being prokaryotes, cyanobacteria possess an oxygenic photosynthesis
similar to that of higher plants. In contrast to eukaryotes, several of these or-
ganisms are capable of fixing atmospheric nitrogen, which thus becomes avail-
able to terrestrial and aquatic phytoplankton and higher plants (Kashyap, Pandey
and Gupta 1991; Sinha and Hader 1997). The role of cyanobacteria as a biolog-
ical fertilizer for wet soils such as in rice paddies has been recognized (Baner-
jee and Hader 1996). Cyanobacteria are cosmopolitan and possess a high capa-
bility of adaptation to UV-B stress, which is known to affect growth, survival,
pigmentation, and motility as well as the enzymes of nitrogen metabolism and
CO 2 fixation (Donkor and Hader 1996, 1997).
There are several specific targets for UV-B radiation in the cell. DNA is specif-
ically damaged; the most common effect is the formation of thymine dimers.
Within the photosynthetic apparatus, the pigments are affected; especially, the
phycobiliproteins are readily bleached and broken into their subunits (Sinha et
al. 1995, 1996; Araoz and Hader 1997). Before this happens the energy transfer
to chlorophyll a, the reaction center of photosystem II, is impaired, which is seen
in an increased fluorescence (Sinha et al. 1996). Slightly delayed, an increase in
phycobiliprotein synthesis has been observed under mild UV -B stress (Figure
6.3). These pigments strongly absorb in the UV-B and are located in the cell pe-
riphery so that they function as an effective screen (Araoz and Hader 1997). They
intercept more than 99% of UV-B radiation before it penetrates to the centrally
located DNA. In addition to the bleaching of the photosynthetic pigments, ru-
bisco (ribulose-1,5-bis-phosphate carboxylase/oxygenase) activity is severely af-
fected by UV-B treatment (Sinha et al. 1996). The nitrogen-fixing enzyme ni-
trogenase is inhibited by UV-B even after short exposure times of the order of
minutes, depending on the species (Kumar, Sinha and Hader 1996). It is inter-
esting to note that a stimulation of nitrate reductase by UV-B was found in all
nitrogen-fixing cyanobacterial strains studied so far (Sinha et al. 1995) whereas
the ammonia-assimilating enzyme glutamine synthetase (GS) is inhibited.
Cyanobacteria often dominate ecosystems that form mats on rocks and soil.
The organisms in these mats have developed a number of adaptive strategies to
reduce the detrimental effects of solar UVR. Vertical migration is utilized
to avoid excessive radiation. Many organisms have been found to synthesize
156 Donat-P. Hader
a b c d e f
FIGURE 6.3a,b. Phycobiliprotein induction by solar UV-B. (a) Zinc staining of samples
exposed to solar radiation, total protein samples (20 j.Lg protein); (b) immunodetection of
PE with the monoclonal antibody anti-PE (Sigma, USA) from cells exposed to solar ra-
diation. Lanes a, cells exposed for 2 hat 5-cm water depth in a pond to PAR + UV-A;
lanes b, cells exposed for 4 h at 5-cm depth to PAR + UV-A; lanes c, cells exposed for
4 h at 65-cm depth to PAR + UV-A; lanes d, cells exposed for 2 h at 5-cm depth to
PAR + UV-A + UV-B; lanes e, cells exposed for 4 hat 5-cm depth to PAR + UV-A +
UV-B; lanesf, cells exposed for 4 h at 65-cm depth to total solar radiation (UV-B was
not detected at this depth). PAR, photosynthetic available radiation
1
0.06 PAR + UV 0.02 PAR
0.05
0.01 • n
.~ 0.04 0.00 ~ =r==;=;
-j:==;=:y:::=::;:L;=;=,
o
~ 0.03
e
co
o
0.02
o
~ 0.01
«
0.00 i==r==r==r=:;==;L';:=:;=;=;=;=;=;=;=;==r=;r=;r=;r=;r==;
10
Retention time [mini
FIGURE 6.4. Induction of mycospore-like amino acids (MAAs) by exposure to UV radia-

tion in the cyanobacterium Anabaena sp.
chemical scavengers that detoxify the highly reactive oxidants produced photo-
chemically (Vincent and Roy 1993). UV-screening pigments include scytonemin
and mycosporine-like amino acids (MAAs), as well as a number of spectro-
scopically characterized, but chemically unidentified, water-soluble pigments
(Kumar et al. 1996; Donkor and Hader 1995). MAAs can be induced by expo-
sure to UV radiation (Figure 6.4). The screening pigment from Scytonema hof-
mannii shows an absorption maximum at 314 nm and is released into the medium
during the late stationary phase of growth (Sinha et al. 1995). Other Scytonema
species that do not produce this pigment are unable to survive 2 h of UV-B
(2.5 W m- 2). Screening pigments such as scytonemins, carotenoids, and my-
cosporine-like amino acids are incorporated into the cytoplasm or the outer slime
sheath, efficiently protecting the organisms from solar short-wavelength radia-
tion (Karsten and Garcia-Piche1 1996).
Phytoplankton
On a global scale, phytoplankton is the most important biomass producer in
aquatic ecosystems. Recent research covering a wide range of aquatic ecosys-
tems has confirmed that environmental UV-B is an important ecological stress
factor that influences growth, survival, and distribution of phytoplankton. The
organisms populate the euphotic zone of the oceans and freshwater habitats to
receive sufficient solar radiation (photosynthetic available radiation, PAR) for
photosynthesis. In this zone, the organisms are simultaneously exposed to solar
UV radiation.
To evaluate if phytoplankton are affected by increased solar UV-B, a number
of questions need to be answered:
158 Donat-P. Hader
What is the spectral distribution of solar radiation penetrating to depth?

What is the biological weighting function (BFW) of the biological effect?
What is the sensitivity of the organisms?
What is the efficiency of mitigating and repair strategies?
Full quantitative understanding has not been reached in any of these topics, but
advances have been made, as covered by recent reviews (Hader 1997c; Cullen
and Neale 1997a,b,c; Vemet and Smith 1997; Hader et al. 1998).
As described, DOC influences the penetration of UV-B. In tum, DOC is bro-
ken down by UV-B with consequent increased penetration to depth. This factor
may be especially important in assessing the influence of increased UV-B on
freshwater ecosystems.
Biologically weighting functions have recently been determined for phyto-
plankton photosynthesis (Cullen and Neale 1996; Boucher and Prezelin 1996;
Neale, Cullen and Davis 1998). It is interesting to note that biological weighting
is highest in the UV-B but also contains a significant UV-A component (Figure
6.5). However, biological weighting functions have been shown to vary by
species, region, and other environmental variability. Therefore, it is now recog-
nized that a single BWF may be inadequate for a complete description of a com-
plete ecosystem. Biological weighting functions also show large experimental
variability (Neale, Cullen and Davis 1998), likely a result of the balance between
damage and repair.
Solar UV affects growth and reproduction as well as photosynthesis (Herrmann
et al. 1996; Herrmann, Hader and Ghetti 1997; Giacometti et al. 1996; Figueroa
et al. 1997; Gieskes and Burna 1997); it affects cellular proteins and photosyn-
2.0 -r--------------------,
'"E 1.5
-,
=.
>-
'-'
C
·u 1.0
<D
:i:
<D
E
::::>
1: 0.5
'"
::::>
0
250 275 300 325 350 375 400
Wavelength [nm]
FIGURE 6.5. Action spectrum for photosynthesis in Nodularia.

thetic pigments (Gerber and Hader 1995a,b; Burna et al. 1996a; Peletier, Gieskes
and Burna 1996; Hader 1997a). The uptake of ammonium and nitrate is impaired
by solar radiation (Behrenfeld 1995; Dohler 1996, 1997; Dohler and Hagmeier
1997). Also, in phytoplankton, one of the major targets is DNA, which strongly
absorbs in the short-wavelength range of solar radiation (Scheuerlein et al. 1995;
Burna, Engelen and Gieskes 1997; Burna et al. 1995, 1996b). UV-B effects have
also been studied at the ecosystem level (Santas, Hader and Lianou 1996; Wang-
berg and Selmer 1997).
Models have been developed (Arrigo 1994; Cullen and Neale 1994; Boucher
and Prezelin 1996; Cullen and Neale 1996; Neale, Cullen and Davis 1998) to es-
timate the impact of enhanced solar radiation. These models have provided im-
portant advances to quantify possible impacts, identifying the most affected pro-
cesses, and to evaluate uncertainties. One inherent problem is the difficulty of
using short-term observations to estimate longer-term ecological responses
(Smith et al. 1992; Vincent and Roy 1993; Bothwell, Sherbot and Pollock 1994;
Cullen and Neale 1994; Holm-Hanson 1997; Neale, Cullen and Davis 1998).
Phytoplankton are motile in the water column (Hader et al. 1995), but most
macroalgae are sessile and thus restricted to their growth site (Liining 1990). Dif-
ferent algal species occupy different depth niches and are adapted to different
solar exposure (Hader and Figueroa 1997). The range in light exposure can be
substantial, from more than 1000 W m- 2 (total solar radiation) at the surface to
less than 0.01 % of that which reaches the understory of kelp forests (Markager
and Sand-Jensen 1994). Macroalgae are subject to UV damage similar as to that
affecting phytoplankton and have developed similar mechanisms to protect them-
selves from excessive radiation, but different species differ in their ability to cope
with enhanced UV radiation (Franklin and Forster 1997). A broad survey was
carried out to understand photosynthesis in aquatic ecosystems and the different
adaptation strategies to solar radiation of ecologically important species of green,
red, and brown algae from polar to tropical oceans (Markager and Sand-Jensen
1994; Wiencke et al. 1994; Figueroa et al. 1996; Beach and Smith 1996a,b; Kirst
and Wiencke 1996; Hader and Figueroa 1997; Porst et al. 1997). This research
indicated that solar UV-B is a stress factor for macroalgae and seagrasses even
at current levels; therefore, further increases in UV-B may reduce biomass pro-
duction and changes in species composition in macroalgae ecosystems.
Freshwater Ecosystems
Freshwater ecosystems have a high turnover. The development of the commu-
nity structure follows defined routes, but the fate of an individual species is dif-
ficult to predict (Biggs 1996). Even though absorption of solar UV-B is consid-
erably higher than in oceanic waters, solar UV-B may be an additional stress
factor that affects species composition and biomass productivity (Williamson
1995, 1996; Hader and Hader 1997; Piazena and Hader 1997). Often UV-B in-
teracts with other stress factors such as heavy metal pollution, which results in
160 Donat-P. Hader
synergistic inhibition of nutrient uptake, enzyme activity, carbon fixation, ATP

synthesis, and oxygen evolution (Rai, Tyagi and Mallick 1996; Rai and Rai 1997).
Sixty-seven freshwater species of algae (Chlorophyta and Chromophyta) were
screened to determine their UV-B sensitivity (Xiong et al. 1996). The algae were
selected to represent different ecosystems ranging from high-altitude lakes to
thermal springs. The sensitive species lost 30%-50% of their oxygen-evolving
capacity during a 2-h UV-B exposure (2 W m- 2). Most of the UV-B-resistant
species have solid cell walls encrusted with sporopollenin and often originated
from high mountain locations. In another experiment in a high-altitude mountain
lake, no significant differences were found between the control (full sunlight)
and a UV-B-depleted population (Halac et al. 1997). UV-A may also impair
growth and photosynthesis (Kim and Watanabe 1994); in other organisms, how-
ever, UV-A was found to have a beneficial effect, partially counteracting UV-B
inhibition (Quesada 1995). In addition to the primary producers, the role of het-
erotrophic picoplankton needs to be taken into account in freshwater ecosystems
(Sommaruga and Robarts 1997).
Predictions of responses by ecosystems to elevated UV -B exposure should not
be based solely on single-species assessments. The results of an experiment by
Bothwell, Sherbot and Pollock (1994) showed that greater algal growth occurred
in an artificial stream under UV-B exposure than in the control. The explanation
of this at first puzzling finding was that the grazers, larval chironomids, were
more sensitive to UV-B radiation than their food, the algae.
The Antarctic Aquatic Ecosystem

Productivity in the Southern Ocean is governed by large-scale spatial and tem-
poral variability (Sullivan et al. 1993; Arrigo 1994; Smith et al. 1998). There-
fore, it is difficult to determine UV-B-specific effects on the background of other
variable environmental factors (Neale, Cullen and Davis 1998; Karentz and Spero
1995; Davidson, Marchant and de la Mare 1996). At high latitudes, variability
in solar elevation, cloud cover, deep vertical mixing, and the cover of ice and
snow have a significant impact on UV -B effects on phytoplankton in the field
and the interpretation of these results. Recent estimates of the effect of a 50%
ozone reduction on total water column productivity were 0.7%-8.5% (depend-
ing on BWF, assumed mixing regime and cloudiness) (Boucher and Prezelin
1996; Smith et al. 1992; Neale, Davis and Cullen 1998).
Although there is convincing evidence of UV -B damage to phytoplankton in
the Antarctic ecosystem, long-term acclimation and adaptation phenomena need
to be assessed (Villafaiie et al. 1995; Lesser 1996; Helbling et al. 1996), as well
as other factors (Neale, Cullen and Davis 1998). Several models have been de-
veloped to estimate UV-related losses in ecosystem productivity based on short-
term observations (Arrigo 1994; Behrenfeld, Lee and Small 1994; Broucher and
Prezelin 1996; Neale, Cullen and Davis 1998). Vertical mixing is a major com-
plication in quantifying UV-B effects on phytoplankton; this is taken into ac-
count in a recent model of UV effects on photosynthesis of Antarctic phyto-

plankton (Neale, Cullen and Davis 1998). Photosynthesis of Antarctic phyto-
plankton is inhibited by ambient UV during incubation in fixed containers (Smith
et al. 1992; Helbling, Villafane and Holm-Hansen 1994; Vemet et al. 1994; Neale,
Davis and Cullen 1998), but this may be different in the natural water column.
Neale, Cullen and Davis (1998) have shown in a model study that near-surface
UV strongly inhibits photosynthesis under all conditions; however, inhibition of
photosynthesis can be modified by vertical mixing, depending on the depth of
the mixed layer. A sudden 50% reduction in stratospheric ozone could lower
daily integrated water column photosynthesis by as much as 8.5%. Thus, UV is
a significant environmental stress factor, and its effects are enhanced by ozone
depletion, but natural variability in exposures of phytoplankton to UV, associ-
ated with vertical mixing and cloud cover, has a major role in either enhancing
or diminishing the impact on water column photosynthesis (Neale, Davis and
Cullen 1998).
The Arctic Aquatic Ecosystem
The Arctic Ocean is a nearly closed water mass characterized by limited water
exchange with the Atlantic and Pacific Oceans (Wlingberg et al. 1996). It is one
of the most productive ecosystems on earth and a source of fish and crustaceans
for human consumption. The Arctic ocean encompasses 25% of the global con-
tinental shelf areas and receives about 10% of the world's river discharge. This
substantial freshwater inflow causes pronounced stratification in the water col-
umn and is responsible for high concentrations of particulate and dissolved or-
ganic carbon (POC and DOC) (Burenkov 1993). Macroalgae are of greater im-
portance in the Arctic than in the Antarctic.
Productivity in the Arctic ocean is higher and more heterogeneous than in the
Antarctic Ocean (Springer and McRoy 1993). In the Bering Sea, the sea-edge
communities contribute about 40%-50% of the total productivity. Due to the
shallow water and the pronounced stratification of the water, the phytoplankton
is exposed to relatively high levels of solar UV-B. Many economically impor-
tant fish spawn in shallow waters, and many of the eggs and early larval stages
are found at or near the surface. Reduced productivity of fish and other marine
crops could affect not only humans in the region but also natural predators. Fur-
ther analysis is necessary to quantify UV-B-related phytoplankton inhibition and
possible effects to higher trophic levels.
The Arctic Ocean is often nutrient limited, especially with respect to inorganic
nutrients such as nitrogen and phosphorus. The nitrogen cycle controls the pri-
mary productivity of the marine ecosystems, as is also found in oligotrophic lakes
and streams. The uptake of nitrogen is sensitive to UV-B (Dohler 1992). Low
doses of UV-B increase the uptake of phosphate, which is probably used for
DNA repair, whereas at higher doses it impairs the uptake.
162 Donat-P. Hader
Conclusions and Consequences

Loss of biomass productivity is still discussed as a potential consequence of en-
hanced levels of exposure to UV -B radiation that can reduce food sources for
humans, but the effects are no longer considered to be as dramatic as a few years
ago. The most significant consequences may be changes in species composition.
A third concern is the reduced uptake capacity for atmospheric carbon dioxide,
resulting in the potential increase of global warming. There is significant evi-
dence and common consent that increased UV-B exposure is harmful to aquatic
organisms, but the extent of damage to ecosystems is still uncertain. The impact
of enhanced levels of UV-B exposure on aquatic ecosystems is probably more
complex than previously thought.
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ters, K.J. 1992. Ozone depletion: ultraviolet radiation and phytoplankton biology in
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ity of the Palmer Long-Term Ecological Research Area and the Southern Ocean. J. Ma-
rine Systems 17:245-259.
Sommaruga, R., and Robarts, R.D. 1997. The significance of autotrophic and heterotrophic
picoplankton in hypertrophic ecosystems. FEMS Microbiol. Ecol. 24:187-200.
Sommaruga, R., Oberleiter, A., and Psenner, R. 1996. Effect of UV radiation on the bac-
terivory of a heterotrophic nanoflagellate. Appl. Environ. Microbiol. 62:4395-4400.
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Sullivan, C.W., Arrigo, K.R, McClain, C.R., Comiso, J.c., and Firestone, J. 1993. Dis-
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7
Ultraviolet Radiation and the Antarctic
Coastal Marine Ecosystem
MARIA VERNET AND WENDY KOZLOWSKI
The Antarctic marine ecosystem is one of the largest ecosystems on the planet.
It is bound by the Antarctic continent to the south and by the Polar Front to the
north. Physical, chemical, and biological properties are distinct to this system
both by their absolute value as well as by their scale of variability. For example,
low and relatively constant temperatures are characteristic of surface marine wa-
ters (from -1.84° and 2SC) (Hofmann et al. 1996). In contrast, solar radiation
presents a large seasonal variability that reaches an extreme of 24 h of light in
summer and 24 h of darkness in winter, south of the Antarctic polar circle
(66.5° S). Similarly, a strong seasonal variability in sea ice coverage reaches max-
imum values in winter (July and August) and minimum in the fall (March), sweep-
ing approximately half the Antarctic marine ecosystem and effectively doubling
the surface of the Antarctic continent. Atmospheric circulation, a driving force on
air temperatures and sea ice distribution, includes several cyclonic pressure sys-
tems that surround the continent, introducing winds, cloudiness, moisture, and
heat into the marine environment and coastal regions in a scale of days to weeks.
The Antarctic aquatic ecosystem has been divided into four major biogeo-
chemical regimes: polar front, permanent open oceanic waters, areas affected by
the annual advance and retreat of sea ice, and coastal waters (Trt!guer and Jacques
1992). The most productive areas are concentrated in coastal regions swept by the
seasonal ice edge, such as the continental shelf west of the Antarctic Peninsula
(Figure 7.1). This area is characterized by highly productive waters that sustain
abundant antarctic krill, Euphausia superba. Several large-scale research projects
have been carried out in this region to understand krill population dynamics and
the marine food chain that supports large secondary production, the penguins and
whales as major krill predators, and the linkages between environmental forcing
and the marine ecosystem (El Sayed 1996). In addition, major studies on the ef-
fect of ultraviolet radiation (UVR, 280-400 nm) on marine organisms have orig-
inated in Western Antarctic Peninsula (e.g., Karentz, Cleaver and Mitchell 1991;
Helbling et al. 1992; Smith et al. 1992; Malloy et al. 1997; Prezelin, Moline and
Matlick 1998; Quetin et al. 1998). This is an area of particular scientific interest
because of a 50-year warming trend, thus combining several aspects of global
change research, mainly UV radiation and surface warming.
170
7. Ultraviolet Radiation and the Antarctic Coast Marine Ecosystem 171
E 295E 300E
285£ ~_....:2~90_ _ _--'-_ _ _....I....._ _-..:3~05::E~
310£
Drake Passage -58£
Palmer LTER
Large-scale Grid
'.
.... ~......
• ".;;:::)f>
Anvers Is. .
(Palmer Station).•
Fariia~1 '.
Vernadslty * ~
•.•• ~. Q..~
Adelaide Is.'··. Weddell Sea

(Rother<1.Bas a, ..
FIGURE 7.1. Map of the Western Antarctic Peninsula with location of Palmer Station, Fara-
day, and Rothera. The points in the grid indicate the stations sampled during the yearly
January cruises from 1997 to 2000.
As an environmental factor, ultraviolet radiation (UVR) in Antarctica has a

predictable UVR to PAR (photosynthetically available radiation, 400-700 nm)
ratio as a function of latitude and time of the year. Variables that affect UVR
(i.e., clouds) can affect PAR as well (Lubin and Frederick 1991) while UVR to
PAR ratios remain unchanged. The presence of the ozone hole in Antarctica
(Farmer, Gardiner and Shanklin 1985) causes an increase in UVB only (290-
320 nm, as the ozone hole moves around the continent), independent of UV A
(320-400 nm) or PAR, resulting in higher UVB:UVA:PAR ratios (Smith et al.
1992; Booth et al. 1994). This change in UVR ratios will increase damage by
UVB as well as change the induction of repair by UV A and PAR, affecting short-
and long-term responses of organisms and communities to UVR (Vincent and
Roy 1993).
The net effect of UVR on marine organisms is a balance between photo-
chemical damage and biologically driven processes of recovery and repair (Vin-
cent and Neale 2000). When considering UVR effects on Antarctic organisms,
and systems, we need to assess how environmental conditions affect both the rate
of UVR damage (i.e., by changing exposure) and the rate of repair (i.e., by ac-
172 Maria Vernet and Wendy Kozlowski
tivating enzymatic processes). UVBis known to affect a variety of cellular pro-

cesses and molecules in the marine environment (Weiler and Penhale 1994; Hader
1997; de Mora, Demers and Vernet 2(00). UV A is damaging to certain cellular
process as well, such as photosynthesis (Helbling et al. 1992), but it is also in-
volved in repair mechanisms (Mitchell and Karentz 1993). Thus, the change in
the ratio of UVB:UVA, by both changes in stratospheric ozone and in the water
column by differential attenuation of UVB and UV A with depth (Diaz, Morrow
and Booth 20(0), is key to our understanding of UV stress on aquatic ecosystems.
In this chapter we describe the major environmental factors influencing ma-
rine Antarctic organisms as they are exposed to possible effects of UVR. We re-
view the effect of UVR on Antarctic marine organisms, in particular primary pro-
duction and the krill-centered food web in coastal areas. Although we address
what is known of UVR effects in Antarctica, we stress the Western Antarctic
Peninsula because of its interest to krill recruitment and fishery and as an area
undergoing climate warming.
The Antarctic Coastal Marine Environment

Atmospheric Processes
Average winter and summer air temperatures in the Western Antarctic Peninsula
are -5Se and 2.9°e, respectively (Smith et al. 1995). Superimposed on sea-
sonal and interannual variability, a period of rapid warming has been observed
in the Antarctic Peninsula in the last half-century. Based on records collected at
Faraday (65° 15' S, 64° 15' W; see Figure 7.1) by the British Antarctic Survey,
the average annual air temperature has increased by 2.4°e (Figure 7.2). Most of
-2
u
~
OJ
"- -4
:::::I
......
(tJ
"-
OJ
Co -6
E
~
«"- -8
-1 0
45 54 63 72 81 90 99
Year
FIGURE 7.2. Faraday annual average air temperatures from 1945 to 1999 (n = 54). Lines
indicate the least-squares regression line ::t 1 SD. (significant at the 90% confidence level).
(From Smith and Stammerjohn, in press.)
the warming is caused by an increase of about 6°C in the average monthly air
temperature in June (Smith, Starnmerjohn and Baker 1996). Spring and summer
trends are comparatively smaller. The same warming trend is observed further
south in the data collected at Rothera (67° 34' S, 68° 08' W). Enhanced merid-
ional flows from mid- to high latitudes during winter are responsible for above-
average winter temperatures observed in the past (van Loon 1967). The warm-
ing trend indicates an increase in maritime, as opposed to continental, influence
in the region (Smith and Stammerjohn, in press). Paleoecological records col-
lected from sediment and ice cores indicate that the region has experienced other
warming periods of similar magnitude in the past 7000 years (Smith et al. 1999).
Thus, the present-day warming seems to be within the boundaries of climate
change observed in the past. In addition to magnitude, climate variability is char-
acterized by the rate of change. It has not been ascertained yet if the warming
we observe now is occurring at a faster rate of change than previous events.
Sea Ice Dynamics

Sea ice formation in Antarctica is driven by the cooling of surface seawater by
air temperature in the fall and winter months. Conversely, the ocean provides the
heat to melt sea ice in the spring and summer (Figure 7.3). Sea ice extent (or
maximum area covered during the season) in the Western Antarctic Peninsula is
closely coupled with winter air temperature (Jacka and Budd 1991; Smith, Stam-
merjohn and Baker 1996). In contrast to the Southern Ocean as a whole, the
warming of winter air temperature in the Western Antarctic Peninsula has re-
sulted in decreased winter sea ice in this region, based on a 21-year record of
satellite passive microwave (Smith and Stammerjohn, in press). On average, the
sea ice in spring and fall during the 1990s was lower than in the 1980s as the
result of its slower advance and faster retreat. A consequence of this trend of
higher winter air temperatures and faster melting of sea ice is to expose plank-
ton to UVR in this region earlier in the spring season than in previous years.
Ultraviolet and Photosynthetically Active Radiation

Background information about the solar spectrum and fundamental physical con-
cepts related to UVR in the atmosphere and underwater have been summarized
recently by Diaz, Morrow and Booth (2000). On average, only 1.5% of extra-
terrestrial UVB reaches the Earth's surface. Solar elevation is the most impor-
tant factor governing surface UVR in the world, followed by total column ozone,
which absorbs UVB strongly at 280-310 nm (Lubin, Jensen and Gies 1998). In
Antarctica, irradiance is at a maximum in December and at a minimum in June
(Figure 7.4). Within Antarctica, UVR variability is also driven by cloudiness.
The ratio of UVB:UVA:PAR also changes seasonally because of changes in
ozone concentration and differential path length through the atmosphere. As UVB
is mostly absorbed in the stratosphere by ozone, the depletion of ozone (ozone
hole) occurs in late winter and spring when the Antarctic vortex closes. The chlo-
rofluorocarbons destroy the ozone on ice particle surfaces (Solomon 1988).
2.4x10 5
1990
1.6 x 10 5
8.0 x 104
o =-id::.._.-.J
2.4 x 10 5r--------,
E 1.6x 10
..::.::
~8.0X104
a:>
>
o
c..:>
FIGURE 7.3. Monthly ice coverage of the Western Antarctic Peninsula area. Dotted line
represents monthly averages based on the October 1977 to August 1998 monthly record
derived from passive microwave satellite data (Smith and Stammerjohn, in press); con-
tinuous lines represent monthly averages for that year; top line in each square is total area
covered by ice within the grid in the Western Antarctic Peninsula (see Figure 7.1); mid-
dle line represents the area of 100% ice coverage; lower line is the difference between to-
tal area and area with 100% ice coverage, or the area of open water.
Changes in total column ozone, due to decreases in stratospheric ozone, notice-

ably increase the ratio of UVB to UVA and PAR (Booth et al. 1994). Overall,
up to 60% higher UVB increases are expected in high latitudes in October due
to total column ozone variability (Sabziparvar, Forster and Shine 1998). Other
natural and anthropogenically induced factors can also change UVB reaching the
Earth's surface. Increased aerosols in the atmosphere are thought to decrease sur-
face UVB up to 2% globally. Conversely, feedback effects of enhanced green-
house gases can cool the polar stratosphere, resulting in a more stable polar vor-
tex; this will lead to enhanced ozone depletion by chemical reactions and to
reduced transport of ozone from lower latitudes (Taalas et al. 2000), resulting in
increased UVB reaching Antarctica.
UVR is further modified through the air-water interface at the sea surface and
after entering the water. Overall transmission in the water follows an exponen-
tial decrease with depth for both UVR and PAR (Holm-Hansen, Lubin and Hel-
bling 1993). UVB is differentially absorbed and can reach depths of 50 m with
an average effective irradiance of 20-30 m. Light transmission is inversely pro-
Palmer LTER Seasonal Time Line
Oaylenglh (h)
Light
Sell
1.<
~
OCI Nov
1<.0 '..
~~
Jan
Dec
<u .• '".
!ilUlI!!!!!m...
" .
Feb Mar
,<.• . .
I\j)r
,
liIl May
"
~
Jun·Aug
J, r ••
PAR
(~Wlcm ' 2 )
5392 6663 8918 8247 6679 5466 3437 879 001 3()9 2009
UVBllJVA 0.047 0.106 0.142 0.095 Q.Ooo 0,068 0,016 0,012 0,015 0,024 0,017
Climalology:
air temp
·4.4 ·3.2 0,3 2 2.9 2.4 0.6 '1.3 ·3.4 ·5.1 ·55
(mean ' C)
cloud cover
(%)
89 90 90 89 9t 88 88 85 81 83 67
Ice Cover:
low
avelll1le
high
Seasonal Thermod ine:

high
stratlrrcation
Nuirlellis (dlssolv,. morganlc):

reducec
high .'.',
Phytoplankton Pro< uCllOn:

low
medium
high
Consumers:
W aler Column Grazers:
krill
krill laMe
salps J::~
copepods
FrOUP-E 7.4. Seasonal development of physical and biological components of the coastal
Antarctic ecosystem based on what is known of the area. General physical and biologi-
cal parameters are extracted from Smith et al. (1995) and are based on known interannual
variability (see text). UV radiation is based on data from the UV network of National Sci-
ence Foundation, sea ice data from Smith and Stammerjohn (in press), and phytoplank-
ton development data from Kozlowski et al. (1995).
portional to the diffuse attenuation coefficient, which is mostly controlled by the

absorption of particles (i.e., phytoplankton), dissolved organic matter (i.e., Gel-
stoff), and water itself (Diaz, Morrow and Booth 2000).
Through the seasons, UVR starts in the Western Antarctic Peninsula in Au-
gust (Booth et al. 1994). At this time, we can expect maximum sea ice cover in
the area (see Figure 7.3) (Starnmerjohn and Smith 1996). UVR transmission
through the ice varies with physical conditions, in particular, ice thickness and
snow cover. For an average 40-cm-thick first-year ice, only 0.5%-9% of surface
UVB reaches the underside of ice, with an average of 2% (Perovich 1993). UVR
can affect photosynthesis and a variety of cellular processes in sea ice popUla-
tions (Prezelin, Moline and Matlick 1998). In ice-free areas, UVR can penetrate
the water column, affecting phytoplankton and other components of the aquatic
food chain (see Figure 7.4). It is not known, and probably it is difficult to mea-
sure, if a decrease in sea ice cover in the spring that increases UVR exposure of
plankton will result in increased net UVR damage to the system. As the ozone
176 Maria Vemet and Wendy Kozlowski
hole develops early in the season (Roscoe, Jones and Lee 1997), any biological
activity during late winter and early spring will be exposed to high UVB. Pos-
sible negative feedback mechanisms are also present. The reduced melting of sea
ice will have an opposite effect on UVR exposure as well. It is believed that the
melting of ice increases water column stratification and favors early springtime
phytoplankton development (Smith and Nelson 1986). Decreased ice melting
could delay phytoplankton development in the water column and thus reduce
phytoplankton UVR exposure in early spring.
UVR Effects on Primary Production in the Western

Antarctic Peninsula
Phytoplankton Development
In the vicinity of Palmer Station (64 0 46.7' S, 64 0 04.0' W), midway through the
Antarctic Peninsula (see Figure 7.1), phytoplankton growth starts in October and
measurable accumulation (> 1 mg chlorophyll a m- 3 ) is seen in October or No-
vember (see Figure 7.4). Phytoplankton concentration, measured as chlorophyll
a (chI a), is low through the winter (0.001-0.04 mg m- 3 ; Vernet, unpublished
data) and early spring (0.04-0.12 mg chI a m- 3 ; Kelley et al. 1999). Phyto-
plankton develops through the summer (December to February) and lasts until
March or April (Smith, Baker and Vernet 1998). The area is swept by several
biomass peaks centered at the month of January. In years of high production, chI
a can reach concentrations of 40 mg m- 3 in the mixed layer while in years of
low production the accumulation does not surpass 3--4 mg m- 3 . On the conti-
nental shelf, a large gradient is observed from high values near the shore to low
values on the continental slope, about 200 km offshore. Thus, phytoplankton can
reach high accumulations in this region through spring and summer, under high
UVR and PAR.
Large interannual variability in phytoplankton accumulations and correspond-
ing primary productivity are characteristic of this region. During the 1990s
(1991-2000), estimated annual primary production in the vicinity of Palmer Sta-
tion varied by a factor of 8 (54-380 g C m- 2 year-I). This variability is asso-
ciated also with changes in phytoplankton composition. The main microphyto-
plankton groups (>2 m) dominating in the region, in order of importance, are
diatoms, cryptomonads, and prymnesiophytes. The northern coastal areas in the
Peninsula are characterized by high diatom concentrations and sometimes cryp-
tomonads (Vernet et al. 1994; Moline and Prezelin 1996; Ross et al. 2000)
whereas further south, in the region of Marguerite Bay, summer populations are
dominated by prymnesiophytes (e.g., Phaeocystis sp.).
UVR Effect on Primary Production

The overall effect of UVR on phytoplankton is to decrease rates of primary pro-
duction (Smith 1989; Holm-Hansen, Helbling and Lubin 1993; Cullen and Neale
1994; Prezelin, Boucher and Schofield 1994; Weiler and Penhale 1994; Smith
and Cullen 1995; Cullen and Neale 1997). UVB and UVA inhibit both light-
limited and light-saturated carbon uptake (Steemann-Nielsen 1964; Maske 1984;
Cullen, Neale and Lesser 1992; Ekelund 1994; Lesser 1996). In Antarctic phy-
toplankton, UVB inhibits carbon incorporation by 25%-50% of shielded sam-
ples (Holm-Hansen, Villafane and Helbling 1997). A strong depth gradient is ob-
served in UVR inhibition from the surface to depth. Measurable UVB inhibition
of primary production is usually constrained to the upper 20--25 m of the water
column (Holm-Hansen, Mitchell and Vernet 1989; Karentz and Lutze 1990;
Smith et al. 1992), as expected from UVB transmission.
The effect of UVR on the inhibition of carbon uptake is not constant across
the spectrum (280-390 nm) (Neale 2000). In some populations, UV A can have
twice the inhibitory effect as UVB (Holm-Hansen, Villafane and Helbling 1997)
whereas other populations are more sensitive to UVB (Boucher and Prezelin
1996a). This difference is of importance to assess possible effects of decreased
stratospheric ozone, affecting only UVB. The response of phytoplankton is not
linear across UVR irradiance levels; the threshold for photosynthetic inhibition
of Antarctic coastal phytoplankton has been determined to be 0.5 W m -2 for
UVB and 10 W m- 2 for UVA (Booth et al. 1997). In contrast, an order of mag-
nitude higher sensitivity and no threshold was observed for Arctic phytoplank-
ton sampled from a deep mixed layer (Helbling et al. 1996). The variability has
been attributed to differences in phytoplankton composition and to the degree of
adaptation to in situ conditions.
Variability in UV Inhibition of Primary Production

To date, the effect of UVR on Antarctic phytoplankton has been studied in mono-
specific cultures and in a variety of field assemblages. Most of the projects have
been carried out in late winter and spring (September to December), coinciding
with the period of ozone depletion. These experiments are short term and diffi-
cult to extrapolate to other time or space scales.
To assess the effect of UVR on primary production at longer time and space
scales, recent experiments were carried out in four consecutive summers (Janu-
ary to mid-February), from 1997 to 2000, in the Western Antarctic Peninsula.
Samples were taken randomly within the grid shown in Figure 7.1, between
Palmer Station and Rothera. Each experiment was incubated for 24 h and sam-
pled every 2, 4,8, and 24 h. UVB and PAR irradiance were measured during the
incubations with a GUV-511 from Biospherical Instruments Inc. Dose was cal-
culated by integrating 305-nm irradiance (/1,1 cm- 2) over the time of the incu-
bations. Ambient temperature was maintained with running seawater from the
ship's seawater intake sampled at 3-m depth. Inhibition of primary production is
expressed as the ratio of primary production exposed to UVR and PAR to pri-
mary production when UVR was blocked (PPUVR + PARIPPPAR)'
The experiments showed inhibition of primary production by UVR, as indi-
cated by a negative ratio of PPUVR + PARIPPPAR (Figure 7.5). For any given time
of incubation, there was a negative linear correlation between inhibition and
305-nm dose, showing higher inhibition at higher dose. The inhibition decreased
1.6
1.4
•
.. •
--
1.2
.. ...
24h
•--
E2
- .-
<t:
!2=.. 1.0 -~-
--~ -. -
•
a...
a... ~
:::::. O.B
cr:
<t:
\.
4"' . .
._ - --
a... \.
+ 0.6
cr:
>
::::l
.. Bh
~ 0.4 I!J.
a...
t:.
•
0.2
0.0 •
0 500 1000 1500 2000 2500 3000 3500 4000
305nm (IlJ/cm2 )
FIGURE 7.5. Effect of UVR on primary production (PP). Experiments were carried out
with surface waters sampled from the Western Antarctic Peninsula, within the LTER grid
(see Figure 7.1), in January 1997. Incubations were done in Teflon bottles (73.2% re-
duction of incident UVR at 305 nm). Doses are 305-nm irradiances integrated over 2, 4,
8, and 24 h of on-deck incubations.
with time, as seen by a decrease in the slope at time intervals of 4, 8, and 24 h.

After 24 h, some samples showed slightly higher production under UVR + PAR
than under PAR alone.
Large variability in daily 305-nm doses was observed for all 4 years (Table
7.1). Changes in dose are related to variability in irradiance as all incubations
were integrated by the same time interval (2, 4, 8, and 24 h). For low daily
305-nm doses (::53,736 ILJ cm~2), as observed in January 1997, there was accli-
mation by phytoplankton carbon uptake to UVR. We observed a decrease in sur-
TABLE 7.1. Average UVR inhibition of primary production observed in surface waters
of the Western Antarctic Peninsula.
Incubation (h) 1997 1998 1999 2000 Average
2 0.29 ± 0.32 0.65 ± 0.33 0.80 ± 0.20 0.88 ± 0.84 0.66 ± 0.26
4 0.43 ± 0.36 0.83 ± 0.37 0.71 ± 0.27 0.74 ± 0.36 0.68 ± 0.17
8 0.59 ± 0.25 0.74 ± 0.22 0.67 ± 0.29 0.62 ± 0.24 0.65 ± 0.07
24 0.95 ± 0.23 1.05 ± 0.21 0.56 ± 0.25 0.61 ± 0.23 0.79 ± 0.24
PAR, photosynthetic active radiation.

Data are Primary productionUVR + PAR/primary productionpAR.
Phytoplankton inoculated with radioactive carbon were incubated on the ship's deck, under sunlight,
and sampled at 2, 4, 8, and 24 h. UVR was screened out with plexiglas (similar to UP3). Incuba-
tions started at mid- to late morning and were completed the next day at the same time. Average day
length at this time of year is 16-19 h, depending on latitude (64.5° S to 68° S).
face inhibition with time, with maximum inhibition of 0.27 ::!::: 0.32 after 2 h in-
cubation and a final inhibition of 0.95 ::!::: 0.23 after 24 h (Figure 7.5 and Table
7.1). With intermediate 305-nm UV doses (::;9617 pJ cm- 2 and ::;9,697 pJ cm- 2 ,
respectively) there was acclimation in 1998 and a lack of acclimation in 1999.
In 2000, with maximum 24-h 305-nm UV doses ::;27,067 pJ cm- 2 , no accli-
mation was observed. As all experiments were carried out from mid-January to
mid-February of 1997 to 2000, changes in 305-nm UV doses were not caused
by variability in sun angle or difference in total ozone column but by changes in
weather patterns affecting UVR reaching the ocean surface. The observed vari-
ability in UVR is attributed mainly to variability in cloud cover.
To understand the factors controlling inhibition of carbon uptake and the
ability of phytoplankton to acclimate, a linear least-squares regression was cal-
culated to the average inhibition of primary production (primary produc-
tionuvR+PAR)/primary productionpAR) as a function of incubation time (2, 4, 8,
and 24 h) for each of the 4 years (Table 7.2). A positive slope indicates a de-
crease in inhibition with time (see Table 7.1) whereas a negative slope indicates
higher inhibition after 24 h or an absence of acclimation. The total average
305-nm dose per year explains 79% of the variance in acclimation observed in-
terannually (Figure 7.6a) and temperature can explain 54% of the variance (Fig-
ure 7.6b).
Similar to our results in Antarctic phytoplankton, acclimation to UVR was also
observed in the cyanobacterium Phormidium murayi (Roos and Vincent 1998)
as growth increased from day 1 to day 5 in cells incubated under UVR and PAR.
Acclimation within 24 h of exposure to ambient UVR, as seen in the Western
Antarctic Peninsula in 1997, is comparable to responses by the sUbtropical di-
atom Chaetoceros gracilis Schutt (Hazzard, Lesser and Kinzie 1997). Antarctic
coastal phytoplankton from the vicinity of McMurdo Station showed a 22% de-
crease in maximum photosynthetic rate (mg C (mg chI a)-I h- I ) after 9 days of
UVR exposure (Lesser, Neale and Cullen 1996).
How representative are the experiments performed with surface phytoplank-
ton to overall primary production in the water column? As discussed earlier, UVR
and PAR decrease exponentially with depth, and UVB is differentially absorbed
with respect to UV A and PAR. We can expect UVB to decrease to 1% of sur-
TABLE 7.2. Lease-squares linear regression of the average UVR inhibition

of primary production.
Average 24-h Average
305-nm dose temperature
Year Slope Intercept r2 (m] cm- 2) (oq Acclimation
1997 0.106 0.14 0.94 2395 :±: 915 1.17 :±: 0.61 Yes
1998 0.055 0.60 0.69 5858 :±: 2776 1.62 :±: 0.56 Yes
1999 -0.038 0.83 0.97 7957 :±: 1595 0.86 :±: 0.18 No
2000 -0.047 0.90 0.90 23998 :±: 3100 0.17:±: 1.33 No
Primary productionUVR + PAR/primary productionpAR as a function of incubation time (2, 4. 8. and

24 h) in the Western Antarctic Peninsula experiment for each of the four years (data in Table 7.1).
(a)
0.15
y =-0.0694Ln(x) + 0.6355
0.1 R2 =0.7945
0.05
'"
c.
0
u; 0
-0.05
-0.1
0 5000 10000 15000 20000 25000 30000
305 nm dose (JlJ/cm 2)
(b)
0.15
•
Y =0.0895x - 0.0664
0.1 R2 =0.5413
0.05
'"
c.
0
u; 0
-0.05
-0.1
0 0.5 1.5 2
temperature (DC)
FIGURE 7.6a,b. Environmental factors controlling UVR inhibition and acclimation of pri-
mary production in four consecutive summers (1997-2000). (a) Rate of change of inhi-
bition of primary production by UVR in 24-h experiments as a function of average daily
305-nm UV doses for each year (data in Tables 7.1 and 7.2). (b) Rate of change of inhi-
bition of primary production by UVR in 24-h experiments as a function of temperature
of incubation
face irradiance at 30-m depth in low productive Antarctic waters where chI a
concentration is approximately 0.25 mg m- 3 (Holm-Hansen, Helbling and Lu-
bin 1993). The results presented in Figure 7.5 and Tables 7.1 and 7.2 would be
representative of UVB at 30% of surface irradiance or about 5-m depth and thus
representative of irradiance encountered in the mixed layer. For more produc-
tive, less clear waters, this represents shallower depth (2-3 m).
On average, daily depth-integrated primary production decreases by 6%-12%
in the presence of UVB (Holm-Hansen, Mitchell and Vernet 1989; Smith et al.
1992; Helbling et al. 1992) during springtime ozone depletion over Antarctic
coastal waters, although higher water column inhibition has been measured also
(i.e., 25%; Boucher and Prezelin 1996b). UVR inhibition of annual primary pro-
duction was calculated as 2% for the Southern Ocean (Smith et al. 1992). Hel-
bling, Villafane and Holm-Hansen (1994), on the basis of different assumptions

and methodology, calculated the decrease in primary production to be 0.15% for
the entire icefree waters south of the Polar Front. The degree of uncertainty of
these measurements increases with area- and time-integrated calculations, as they
are based on discrete hourly or daily measurements (i.e., depths) taken in a short
period of time (i.e., month-long cruise) and space (i.e., several hundred square
kilometers as opposed to the whole Southern Ocean).
Temperature
Low ambient temperatures are characteristic of the marine environment in the
Antarctic. Lowest, freezing temperature is -1.84°C. In late spring and summer,
low temperatures in the Western Antarctic Peninsula are associated with melt-
ing ice (-1.61 0c) and warmer waters are offshore, 2.5°C. For any given loca-
tion, the melting and formation of ice drive the distribution of low surface tem-
perature. Furthermore, melting of continental ice decreases temperature and
salinity in nearshore areas.
Overall response of the UVR inhibition of primary production was also influ-
enced by the ambient (incubation) temperature during the 1997-2000 experi-
ments. Average temperature for all the experiments was 1.29° ± O.72°C, vary-
ing from -IS to 2SC. The ability of the phytoplankton to acclimate carbon
uptake to ambient UVR was enhanced at higher temperatures (Figure 7.6b and
Table 7.2). The influence of temperature on acclimation could result from the in-
fluence of temperature on repair mechanisms (Vincent and Neale 2000) because
the higher temperature should promote higher enzymatic activity.
Temperature influences also the effect of UVR on primary production (as mea-
sured by carbon uptake) in polar mat-forming cyanobacteria. Cyanobacteria are
psychotrophs, growing slowly (0.23 + 0.069 day-I) at the optimum temperature
of 19.9°C (Tang, Tremblay and Vincent 1997). Experiments carried out on the
polar cyanobacterium Phormidium murayi West and West showed a synergistic
effect of temperature and UVR inhibition (Roos and Vincent 1998). Cyanobac-
teria were grown at 5°, 10°, 15°, 20°, and 25°C. Photosynthesis versus irradi-
ance (P versus I) curves showed that maximum photosynthetic rate (Pmax) was
a function of temperature (a factor of 2.7 higher at 35°C than at 5°C), but no ef-
fect of temperature was observed on the light-limited response. After several days
of acclimation under UVR, P max was reduced by 30% but there was no effect by
temperature on Pmax or lr. From Table 7.1 of Roos and Vincent, we can calcu-
late that temperature reduced P max by 78% (0.22 of optimal photosynthesis) from
20°C to 5°C for incubations under PAR only. Cultures grown at 20°C under UVR
showed decreased photosynthesis by 21 % or 0.79 of optimal. When both factors
were combined, P max was 0.146 of optimal photosynthesis or resulted in a 85%
reduction.
The combined effect of temperature and UVR inhibition can be compared to
models of multiple stressors (Folt et al. 1999). The comparative model implies
that the dominant limiting factor will be expressed when more than two stres-
sors are present. The additive model predicts that the combined effect of two
stressors will be equal to the sum of the effect of each factor separately. The mul-
tiplicative model predicts that the final result in the presence of both factors will
be equal to the multiplication of the effect of the two independent factors. Syn-
ergism occurs when the observed effect of both factors is larger than that pre-
dicted by a model, and antagonism among multiple stressors is present when the
combined effect is less than predicted by a model. In the example of the cyanobac-
teria, comparing temperature effect (from 20° to 5°C) and UVR effect at opti-
mal photosynthesis (at 20°C), the additive model predicts a 78% + 21 % = 99%
reduction in Pmax (78% + 21 % reduction). The multiplicative model predicts P max
to be 0.17 (0.22 * 0.79) of optimal values, and the comparative model predicts
that the dominant stress factor, in this case temperature, will predominate and
that the combined effect of both stressors would be 0.22 of optimal photosyn-
thesis. In the experiment, the observed P max for both factors (temperature and
UVR) combined was 0.146 of optimal photosynthesis (85% reduction), better
than the 98% reduction predicted by the additive model and worse than the 0.17
(83% reduction) predicted by the multiplicative model. Thus, for this case, there
was a multiplicative synergistic effect of both stressors. The authors interpreted
their result as a decrease in repair mechanisms at low temperatures.
Similar multiplicative effect for temperature and UVR combined was also ob-
served in Nostoc sp. (Anioz, Lebert and Hader 1998) grown at 18°C and exposed
to temperatures up to 4]oC and to UVB of 0-150 kJ m- 2. Cells could survive
high temperature (84% survival or 16% reduction at 42°C and 20% survival at
47°C) but were more sensitive to UVR at 18°C (40% survival at 50 kJ m- 2 or
60% reduction). When both factors were combined at 42°C and 50 kJ m- 2 , they
observed a 12% survival or 88% reduction. The comparative model predicts a
60% reduction in survival, the multiplicative model predicts a 67% reduction,
and the additive model predicts a 76% reduction. Thus, high temperature and
UVR have a synergistic effect on Nostoc sp., as concluded by the authors. In the
case of Nostoc sp., this is an additive synergistic effect, with a higher reduction
than for the multiplicative synergistic model.
No experiments are yet available to calculate synergism or antagonism by tem-
perature and UVR on primary production in antarctic phytoplankton. The results
presented here (Figures 7.5, 7.6 and Tables 7.1, 7.2) suggest that temperature
might have an effect on acclimation to UVR. Thus, there is a suggestion that am-
bient low temperatures decrease the rate of repair and that a similar synergistic
effect of temperature and UVR can be expected, as for polar and temperate
cyanobacteria.
Nutrient Metabolism
UVR affects nutrient uptake and nitrogen metabolism in marine phytoplankton
(see Vernet 2000). Furthermore, recent studies show that nutrient limitation might
affect UVR inhibition on population growth. In an experiment carried out with
natural phytoplankton for 7 days, onset of UVB effect on phytoplankton at 5-m
depth or greater was observed on day 3, once nitrate concentration decreased ap-
preciably (Figure 7.7) (Mostajir et al. 1999). Similar to the combined effects of
temperature and DVR, nutrient limitation and DVR might have a synergistic ef-
fect. Cullen and Lesser (1991) found that nitrate-limited Thalassiosira pseudo-
nana was 8.6 times more sensitive to UVB than nitrate-replete cells.
In contrast, other long-term exposure experiments showed mixed results. The
marine diatom Phaeodactylum tricornutum exposed to UVR showed a lack of
growth inhibition due to nitrogen limitation (Behrenfeld, Hardy and Lee 1992).
The freshwater green alga Selenastrum capricornutum grown under DVB and
phosphate limitation showed higher inhibition of photosynthesis and growth than
for short-term exposure (hours) but a relaxation in the inhibition of nutrient lim-
itation (Veen, Reuvers and Ron~ak 1997).
Community Composition
Damage to organisms exposed to DVB varies by 100 fold between species
(Ekelund 1990; Karentz, Cleaver and Mitchell 1991). The differential sensitiv-
ity to DVB suggests a change in species composition caused by long-term DVB
exposure, with species that are more DV tolerant ultimately dominating (Wor-
rest et al. 1981). In general, based on culture studies, diatoms are the most re-
sistant to UVR, followed by prymnesiophytes and other flagellates, such as cryp-
tomonads. Green algae and cyanobacteria are usually considered as resistant as
diatoms. This differential sensitivity among phyla has been established based on
FIGURE 7.7. Phytoplankton (5- to 30-p,m cells) abundance and nitrate concentration dur-
ing a 7-day experiment in a 1500-1 mesocosm with St. Lawrence River water under four
UVB treatments. (Drawn from Mostajir et al. 1999.)
several cellular processes, such as nitrogen assimilation (Dohler 1997), radio-

carbon uptake (Davidson and Marchant 1994; Helbling, Villafafie and Holm-
Hansen 1994; Vernet et al. 1994; Villafafie et al. 1995a), specific growth rate
(Karentz 1994; Davidson et al. 1994; Villafafie et al. 1995b), and cell abundance
in natural populations (Karentz and Spero 1995).
Experiments with mixed populations can be used to test predictions on phy-
toplankton succession based on differential UVR sensitivity established in the
laboratory and from short-term field experiments. Davidson, Marchant and de la
Mare (1996) found that 2-day UVB exposures of exponentially growing mixed
cultures at O°C favored Phaeocystis antarctica over diatoms. They rejected a hy-
pothesis based on previous experiments in which they found diatoms were three
to five times more resistant than P. antarctica (Davidson et al. 1994). Part of the
discrepancy can be attributed to differences in experimental design: this latter
experiment used 9150 J m- 2 erythemal UVB in a 2-day exposure whereas pre-
vious cultures had been exposed to 20%-650% of average springtime UVB ra-
diation in the area.
Cell Size
A differential effect of UVR on cell size has been observed for diatom cultures
(Karentz, Cleaver and Mitchell 1991), with greater damage being associated with
smaller cells. Small cells have a shorter light path length with reduced absorp-
tion and refraction by cytoplasmic components between the cell membrane and
nuclear DNA, which results in increased UVB reaching the DNA (Raven 1991;
Garcia-Pichel 1994; Booth et al. 1997).
Increases in cell size have been observed in cultures under UVB exposure
(Dohler 1985; Behrenfeld, Hardy and Lee 1992; Veen, Reuvers and Ronc;ak 1997)
and are a consequence of the reduction in specific growth rates. Burna, Engelen
and Gieskes (1997) attributed the increased cell size to an arrested cell cycle
caused by residual DNA damage, as measured by concentration of thymidine
dimer cellular content. The increase in cell size results from carbon uptake in the
absence of cell division. Coastal waters have, on average, a higher proportion of
larger cells than open waters (Malone 1980). For example, more than 80% of the
nearshore phytoplankton biomass was associated with cells larger than 10 f-tm in
Terre Adelie, Antarctica, during summer whereas 70 km offshore, cells larger
than 10 f-tm represented only 30% of the total biomass and 59% of the cells were
between 1 and 10 f-tm (Fiala and Delille 1992). Within Antarctic coastal waters,
high chI a accumulations are dominated by large cells (e.g., >20 f-tm) while low
chI a concentrations are dominated by smaller cells (Holm-Hansen and Mitchell
1991; Bidigare et al. 1996). Based on increased inhibition found in smaller cells,
presumably due to their smaller light path length, we might hypothesize that oce-
anic Antarctic phytoplankton may have a higher sensitivity to UVB.
The differential effects of UVR on phytoplankton populations, resulting from
their composition or size, are relevant to the spatial, seasonal, and interannual
variability in phytoplankton (Ross et al. 2000) and also result from the conse-
quences of global change that could influence a shift in coastal phytoplankton

composition. It has been suggested that increased air temperature is increasing
continental glacial melt in the region of the Western Antarctic Peninsula and, as
a consequence, decreasing surface salinity and increasing stratification. From the
dominant phytoplankton groups in the area, Cryptophyceae (also known as cryp-
tomonads) seem to favor shallow mixed layers, with lower salinity and a strati-
fied water column. These algae are unicellular, flagellate cells, 13-20 /Lm in
length. They are not selected by krill in a mixed assemblage, probably due to the
small size (Haberman 1998). In addition, they are known to be more sensitive to
UVR (Vernet et al. 1994). Such a shift in phytoplankton composition, an indi-
rect effect of climate warming, could not only affect the efficiency of the food
chain but also increase the overall inhibition of primary production in the area.
Effect of UVR on the Antarctic Food Chain in the

Western Antarctic Peninsula
The phytoplankton growth that supports krill populations in the Western Antarc-
tic Peninsula is composed of large cells (>20 /Lm) that prefer calm conditions
and shallow mixed layers. Phytoplankton under these conditions are usually less
sensitive to UVR (Karentz et al. 1991) or have a faster recovery rate (shallow
mixed layers). Once the phytoplankton accumulation reaches high particle con-
centration, there is a shielding of UVR for cells at depth due to increased UVR
absorption by surface populations. Thus, it seems phytoplankton can grow un-
der high UVR but that once the populations are established they can acclimate
to, or avoid, damaging UVR.
Before experiments in mesocosms, prediction of UVR effects on ecosystems
had assumed a linear addition of UV effects on different trophic levels. More re-
cent experiments suggest that UVE might change carbon and energy flows in an
ecosystem, thus favoring some pathways at the expense of others. For example,
differential UVR sensitivity between algae and herbivores can increase algal pop-
ulations by decreased grazing pressure (Bothwell et al. 1993). Similarly, increase
in substrate due to photooxidation of dissolved organic matter has been reported
as enhancing bacterial populations exposed to low levels of UVB (Herndl, Muller-
Niklas and Frick 1993). Thus, changing the interaction between biotic and abi-
otic components or between different components of the food web can some-
times decrease or reverse the deleterious effect of UVB on a known organism
(Vernet and Smith 1997).
Research on the effect of UVR at the ecosystem level is a demanding task.
Mostajir et al. (1999) cite five criteria necessary to extend results from labora-
tory and mesocosms into whole ecosystems. First, the experiment must have or-
ganisms representative of natural environments. Second, it is the relative sensi-
tivity of the different elements of the community that determines the net effect
of UV on the ecosystem, not the absolute response. Thus, experiments need to
be carried out with all the elements of the system under study present. Third, en-
hanced UVB irradiances and doses must be plausible, i.e., not too high, but rep-
resentative of ozone-depleted conditions at that location. Fourth, the effect of
UvB must be carried out under environmentally representative conditions, e.g.,
nutrient depletion for surface summer populations. Fifth, natural mixing rates
should be included in the experiment.
Mesoscosm experiments have not been carried out for Antarctic systems but
in temperate, subarctic, and arctic environments. Subarctic experiments lasting 7
days in St. Lawrence Estuary surface water (screened by a 240-mm mesh) main-
tained between 8.So and l1.4°C in summer (July) at four UvB treatments (no
UVB, natural UVB, low UVB, and high UVB) showed a shift from herbivory
to microbial food web. Ciliates and large (S-20 /Lm) phytoplankton were differ-
entially sensitive to UvB. Ciliates showed decreased abundance at all UVB lev-
els while large phytoplankton did not show inhibition at natural UvB but de-
creased in number at both levels of enhanced UvB (low UvB and high UVB,
which enhanced by a factor of 1.23 and 1.79, respectively, the natural UVB lev-
els). As a consequence of decreased predation, ciliate prey increased: bacteria,
heterotrophic flagellates, and small «S /Lm) phytoplankton showed higher abun-
dance under UvR. These results suggest that enhanced UVB levels at realistic
doses expected under severe ozone depletion can change the food web structure.
Ciliates are particularly sensitive to UvB. Experiments in freshwater systems
in the Arctic, at 3.8° to S.2°C, showed species-specific ciliate and rotifer inhibi-
tion of growth by UvB (Wickman and Carstens 1998). Not all species were in-
hibited; some showed no UvB effect whereas others were enhanced under UVB.
Heterotrophic flagellates and bacteria were not sensitive to UVB, similar to the
results from the St. Lawrence Estuary (see also Rae and Vincent 1998). In tem-
perate areas, experiments show either no effect of UVB (Hill et al. 1997, Lange
et al. 1999) or show that some predators or some grazers are more sensitive than
their prey to UvB exposure (Bothwell et al. 1993; Williamson et al. 1999; Za-
garese and Williamson 2000).
In the Western Antarctic Peninsula, krill, salps, and copepods are the main
components of the macrozooplankton assemblages (see Figure 7.4). Years of
abundant krill seem to alternate with years of salp dominance, and the two groups
do not overlap geographically (Ross et al. 1996). This alternation correlates with
years of higher and lower ice coverage in the previous winter, with krill domi-
nating after winters with high ice (Loeb et al. 1997). Natural UvB fluxes in ice-
free areas during springtime are high enough to cause DNA damage in krill, al-
though no quantitative relationship was found between DNA damage and UVB
flux in the field (Malloy et al. 1997). Krill and Antarctic fish that reproduce in
spring and summer showed, on average, higher rates of DNA repair than species
that reproduce in the winter.
Under experimental conditions, PAR radiation, three to five times lower than
noon surface irradiance caused captive juvenile krill to die within 1 week (New-
man et al. 1999). The addition of UvB radiation, similar to exposure at 0- to
lS-m depth, increased krill mortality and decreased overall activity. Krill exposed
to sublethal UvA doses also showed decreased activity. As these organisms had
been kept in darkness for several months before the experiments, it is not known
if they were more susceptible than wild krill to UVR. Thus, field experiments
are needed to ascertain overall UVR effect on krill. To date, indications are that
they might be highly susceptible but, as their repair rate is also high, net dam-
age is unknown.
It is not known and probably is difficult to measure if a decrease in sea ice
cover in the spring that increases UVR exposure will result in increased net UVR
damage to the coastal Antarctic food web. The obligatory association of young
krill (less than 1 year) with the under-ice surface during winter protects these lar-
vae from UVR in early spring and provides protection from exposure until the
ice retreats. As the ice melts, the young larvae are in an environment that pro-
motes phytoplankton growth and provides food for the young krill (Ross et al.
2000). It is not known if the shallow mixed layer associated with the ice edge
phytoplankton accumulation is also an environment conducive to high zoo-
plankton DNA repair rates, as in the case of phytoplankton.
Years of early ice retreat, as in 1998 (see Figure 7.3), not only decrease the
chances of developing an ice-edge phytoplankton bloom because of low PAR
but also expose young krill to high UVR:PAR during periods of low ozone. If
ice protects krill larvae feeding underneath the ice, then earlier melting increases
UVR exposure in a vulnerable time when larvae might be subject to low food
levels until the bloom develops.
Naganobu et al. (1999) showed a positive correlation between krill recruitment
and ozone depletion when years of high ozone depletion and expected higher
UVB irradiance coincided with years of lower year 1 class. Thus, directly or in-
directly, UVB may affect krill recruitment, either through decreased primary pro-
duction or by direct net damage on krill larvae. Data interpretation is further lim-
ited by the fact that years of low recruitment coincided with years of low winter
sea ice cover. These results, based on correlations between UVB variability re-
sulting from stratospheric ozone depletion and krill recruitment, do not show
causal effect by UVB. Further research on the physiological and environmental
factors influencing UVB damage in krill is needed to ascertain if UVB affects
krill recruitment.
The effect of UVR on Antarctic salps and copepods is unknown. Salps be-
come abundant in the summers following a low ice winter (Loeb et al. 1997; see
Figure 7.4). They are abundant in oceanic Antarctic waters and are associated
with small phytoplankton cells characteristic of offshore assemblages. UVR can
be more damaging to small cells (Karentz, Cleaver and Mitchell 1991; Villafane
et al. 1995a,b), thus indirectly affecting salp food source. In addition, offshore
locations have deeper mixed layers than coastal environments where phyto-
plankton and zooplankton could be more susceptible to UVR because of their
decreased ability to repair (Neale, Davis and Cullen 1998).
In summary, recent studies have shown the susceptibility of Antarctic zoo-
plankton to UVR. The knowledge of the effect of UVR on the Antarctic food
web has not yet been approached systematically nor has the experimental design
been done to detect possible changes in the energy flow within the ecosystem.
Studies on abiotic factors (Mopper and Kieber 2000), bacteria (Jeffrey, Kase and
Wilhelm 2000), phytoplankton, and krill are starting to emerge. However, we
need a more comprehensive approach such as those obtained from microcosms

experiments in other areas.
Conclusions
In conclusion, the damage caused by UVR to the marine ecosystem in coastal
environments (seasonally swept by the advance and retreat of sea ice) in Antarc-
tica is tightly coupled to the meteorology (i.e., clouds) and sea ice dynamics of
the area. Large interannual variability from January 1997 to January 2000 on the
effect of UVR on primary production is caused by a factor of 5 on UVR expo-
sure resulting from cloud cover. Because of the rapid absorption of UVB by ice,
maximum UVB exposure will occur under icefree conditions. Those conditions
will be subject to large interannual variability on total area covered by sea ice
and by the specifics of sea ice formation and retreat, which can vary as much as
several months for any given location. Melting of sea ice in spring exposes krill
larvae to higher UVB and higher predation but also provides the conditions for
phytoplankton development necessary for production of food. Higher sea ice in
winter is related to higher krill abundance in the following growth season, either
by direct effect on UVR protection or indirectly by higher food availability.
The balance between repair and damage in phytoplankton in this area is pri-
marily controlled by UVR radiation and also by water temperature. As radiation
affects damage and because temperature might be related to repair processes, we
can speculate that changes in UVR, caused either by anthropogenic ally induced
changes or by natural variability, might control net damage. Finally, although
large strides have been accomplished in Antarctica with respect to understand-
ing the overall effect of abiotic and biotic components of the ecosystem, a more
systematic approach is needed to characterize the relative effect of UVR on the
interacting elements.
Acknowledgments. We thank K. Sines, M. Crowder, M. Duffy, C. Moraes, E.

Polman, J. Walker, and K. Weinbaum for technical assistance and Antarctic Sup-
port Associates for logistic support in the Antarctic. This project was partially
funded by the U.S. National Science Foundation grant DPP-9632763 and by the
InterAmerican Institute for Global Change Research (CRN-026).
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8
Ultraviolet Radiation and Exobiology
CHARLES S. COCKELL
In comparison to the Earth, extraterrestrial environments possess quite different

UV radiation regimes, both in terms of absolute flux and in terms of spectral
quality (Homeck et al. 1984; Homeck 1993). For example, the moon has no
atmosphere and thus its UV regimen is determined solely by the extraterrestrial
spectrum. Mars, on the other hand, has an atmosphere that is one-hundredth the
total atmospheric pressure of Earth and is composed of 95% CO 2 (carbon diox-
ide). The surface UV flux is primarily determined by this atmospheric composi-
tion, and this flux is very different from that of the Earth. Planets around other
stars will also have very different surface UV regimens, determined partly by
their atmospheric composition but also by the fact that the spectral quality of
light emitted by other stars can be very different from that of our own Sun.
There are a number of reasons why we are interested in extraterrestrial UV
environments. First, we are interested in the possibility of life. The Earth has
been colonized by microbial ecosystems for at least 3.5 Ga (billion years) (Schopf
and Packer 1987) and possibly 3.8 Ga (Mojzsis et al. 1996). It is the pervasive
nature of microorganisms spatially and temporally in almost every extreme habi-
tat on Earth, as well as their appearance so soon after the formation of the Earth
about 4.5 Ga ago, that leads us to ponder the presence of life on other planetary
surfaces.
Mars is of particular interest. We do not know whether Mars ever possessed
life. Channels and valley networks on the Martian surface, formed during its ear-
liest history at least 3.5 Ga ago, provide persuasive evidence of a planet that may
have had abundant liquid water (Carr and C10w 1981; Carr 1987; Cabrol et al.
1999). Furthermore, the impact flux on the early planets was much higher than
today, and so there is a high probability that material was transferred between
the terrestrial planets (Gladman et al. 1996). Quite contrary to the excitement en-
couraged by the media for the likelihood of past life on Mars, it would actually
be a rather more extraordinary scientific discovery if it were demonstrated that
during the Archean era (3.9-2.5 Ga ago), when the Earth was covered in abun-
dant microbial life, Mars (which was wetter and warmer than today) remained a
dead planet.
Another more practical reason for our interest in the UV radiation environ-
195
ment of Mars is our interest in establishing ourselves in these environments for

either economic, social, or even tourist motives. Understanding the UV radiation
regimen is essential for the design of UV-resistant materials. We also need to
calculate what UV exposure organisms would receive if we built closed-loop
ecosystems for food manufacture that used natural sunlight to drive photosyn-
thesis (Cockell and Andrady 1999).
In this chapter, I have three principal foci. First, I wish to explore the ultravi-
olet history of Mars and its biological implications. I do not assume that there
was life on Mars. My purpose is to provide an exercise in comparative planetary
evolution. In Chapter 1, I gave a review of what we know about the photobio-
logical history of Earth. Because Mars has been subject to a quite different path
of atmospheric and surface evolution, its ultraviolet history is of considerable in-
terest as a means to gain a perspective on the unique photobiological history of
Earth. In the next part of this chapter, I describe the implications of the present-
day Martian UV climate to human exploration. How does the UV regimen im-
pact our plans to explore and possibly even to settle Mars? Finally, I describe
methods to quantify the UV radiation environments of extrasolar planets, i.e.,
planets orbiting other stars (Kasting, Whittet and Sheldon 1997; Cockell 1999).
I give some examples of the means by which we can use spectroscopic data re-
turned from large telescopes to compare these planetary environments to what
we know about Earth and its biota.
The Ultraviolet History of Mars: An Exercise in

Comparative Evolutionary Photobiology
The atmosphere of Mars is 95% CO 2 , and so the radiative transfer calculations
that we use to calculate the surface UV environment can essentially assume a
pure CO 2 atmosphere (see Cockell et aI., 2000, for details). Unlike the Earth,
Mars does not have a significant ozone column, although some ozone buildup
occurs over the poles in spring and winter (Barth et aI. 1973; Barth and Dick
1974; Lindner 1991). These levels, although about two orders of magnitude lower
than typical terrestrial column abundances, can reduce UV -C flux reaching the
ground (Kuhn and Atreya 1979; Cockell et aI., 2000). The photobiological his-
tory of the planet has been almost exclusively determined by the increase in so-
lar luminosity over time and the change in the atmospheric carbon dioxide reser-
voir. Haberle et aI. (1994) carried out a detailed modeling study of the evolution
of CO 2 on Mars over time. They investigated varying initial CO 2 inventories as
well as alterations in solar luminosity and the greenhouse effect. They ultimately
concluded that none of the outcomes is entirely satisfactory. Large initial CO 2
inventories tend to predict Martian polar caps that are too large compared to the
ones we observe today. Smaller inventories require low partial pressures of CO 2
on early Mars, which may be inconsistent with a warmer, more water rich past
(Carr 1987).
8. Ultraviolet Radiation and Exobiology 197
In view of the warmer conditions that are proposed for early Mars, Haberle et
al. proposed a scenario where the initial CO 2 inventory may have been between
0.5 and 3 bar. At the beginning of the time corresponding to the terrestrial Archean
at approximately 3.8 Ga, the CO 2 inventory may have been 0.5-1 bar. How the
CO 2 atmospheric reservoir then evolved to current conditions (the present-day
surface pressure is 6 mb) is unknown. Either the CO 2 was slowly lost to car-
bonates through weathering, or the atmosphere may have collapsed. In the latter
scenario, the buildup of the polar ice caps results in reduced temperatures and a
freeze-out of more carbon dioxide. A positive feedback process is initiated that
leads to a rapid collapse of the atmospheric CO 2 reservoir (Haberle et al. 1994).
Because of the direct coupling between the Martian polar caps and the atmo-
spheric CO 2 reservoir, the time to reach equilibrium may have been only about
200 years (Leighton and Murray 1966). If such a scenario did occur, it would
have significant consequences for the surface UV flux, as discussed in the next
section.
In Figure 8.1, the photobiological history of Mars has been presented for an
initial inventory of 2 bar, declining to 1 bar in the time corresponding to the early
terrestrial Archean (the Martian Noachian), with an arbitrary gradual decline to
present-day conditions. The rate of decline of CO 2 varies with the models used
(McKay and Davis 1991; Haberle et al. 1994). Although improved models may
increase the accuracy of the rate of change in UV flux, the qualitative evolu-
tionary conclusions are not critically altered by the assumptions.
Theoretical Effects on Life

Unlike the Earth, whose photobiological history during the Proterozoic and
Phanerozic has been dominated by an ozone column, Mars has a more simple
history and one that has been closely coupled with the changes in atmospheric
CO 2 inventory.
The rising UV flux over time, although theoretically presenting an increasing
photobiological challenge, probably does not prevent the evolution of life. The
present-day DNA-weighted irradiance on the surface of Mars is similar to the
weighted irradiance on the surface of Archean Earth, the biological significance
of which has been discussed previously (Cockell 1998). The importance of the
photobiological deterioration of Mars is that it could theoretically exacerbate the
demise of life in synergy with the deterioration in other physical factors (Cock-
ell 1998). Low temperature extremes and the possible existence of peroxides in
the Martian soil are two environmental stressors detrimental to life, but the lack
of liquid water on the surface is undoubtedly the worst (McKay and Davis 1991).
The drop in temperature of the planet as well as the reduction in CO 2 would have
reduced habitats in which water was available.
The time over which this occurred is difficult to assess, but if the Haberle mod-
els are accurate in suggesting a gradual decline in pC0 2 over time, then the
100
10
0.1
4 3 2 o
Time (Ga)
1000
Ultraviolet Crisis
N
E
tr------- __ --
~
'"'-'
t::
.~
"0
100
.~
"0
~
..c::
Cl
·CD
:;:
<l:
2:
Cl EpisodicC02 injection
10
4 3 2 o
Time (Ga)
FIGURE 8.1. The ultraviolet history of Mars (compare to Figure 1.7). The graph of bio-
logically effective irradiances also shows the theoretical photobiological consequences of
an "ultraviolet crisis" caused by an atmospheric collapse; also shown are the effects of an
episodic CO 2 injection.
increase in UV stress has been a continuing problem for Mars from 4.5 Ga un-
til the present atmospheric pressures were reached. The availability of liquid wa-
ter on the surface probably started to become a serious biological problem shortly
after approximately 3.8 Ga, when it is presumed that few new valley networks
were formed (Carr and Clow 1981). However, liquid water may have persisted
for some 700 million years after this date in ice-covered lakes (McKay and Davis
1991), which would theoretically provide ecological refugia for any potential sur-
face biota and potentially some UV protection as well. Some hydrothermal re-
gions that may have existed well after late bombardment (Gulick and Baker 1989)
could theoretically provide an extinction refugium for surface life. In deeper re-
gions of Mars, such as the Hellas Basin, it is possible that even during recent epochs
atmospheric pressures have risen above the triple point of water (~6.l mb) to
allow for the existence of moisture in the soil.
This gradualist view of the ultraviolet history of Mars may have been differ-
ent if the planet did suffer an atmospheric collapse at some point in its history
between 4.5 and 3 Ga ago (Haberle et al. 1994). A planetary atmospheric col-
lapse has the potential to trigger an ultraviolet crisis. A reduction of the Martian
atmospheric CO 2 reservoir from about 1 bar to about 6 mb would increase DNA-
weighted biologically effective irradiances by fivefold. A reduction from 0.5 bar
to about 6 mb would cause a threefold increase. What would be the effect on a
theroetical biota?
Although these relative percentage increases in DNA-weighted irradiance may
occur on present-day Earth for an ozone depletion of approximately 50%, the ab-
solute UV flux is much higher on Mars than Earth. The increase in damage on
Earth caused by ozone depletion can be compensated in some organisms by the
induction of UV-screening compounds or repair processes (see Tevini 1993 and
discussions therein). On Mars, ifthe limits of UV -screening compounds were al-
ready employed (for example, 99% screening in the subsurface photosynthetic
layers of a microbial mat) under a biologically effective irradiance some three
orders of magnitude higher than on present-day Earth, a substantial amount of
the effect of the increased UV flux would have to be handled by repair processes.
A fivefold increase in DNA-weighted irradiance over just 200 years might be
expected to present a substantial selection pressure.
Other communities affected by such UV radiation changes would be single-
celled organisms in the water column. Isolated single-celled organisms cannot
make use of the matting habit and, in the absence of substantial UV absorption
in the water column, can be profoundly affected by UV radiation (Milot-Roy and
Vincent 1994). However, organisms in ice-covered lakes might be protected by
the ice covering, which can confer substantial protection against incident UV ra-
diation (Vincent et al. 1998).
Communities unaffected by such a change would be deep-subsurface chemo-
synthetic communities (Boston, Ivanov and McKay 1992) where exposure to UV
radiation was irrelevant. Organisms living in substrates such as lithic communi-
ties associated with rock, where even a small movement into the rock may re-
duce light levels by an order of magnitude (Nienow, McKay and Friedmann
1988), might also be robust against the photobiological consequences of atmo-

spheric collapse. Organisms with well-evolved repair processes would also be
robust. For example, the extremely UV -tolerant Deinococcus radiodurans is pre-
sumed to have acquired its UV resistance as a result of desiccation selection pres-
sure (Mattimore and Battista 1996). Its repair capabilities exceed the instanta-
neous DNA-weighted irradiance on present-day Earth at a zenith angle of 0° by
approximately three orders of magnitude (Cockell, 2000) and thus possibly by
threefold the DNA-weighted irradiance on early Mars with an atmospheric CO 2
inventory of approximately 2 bar. This organism would survive the increase in
instantaneous DNA-weighted irradiance associated with the atmospheric collapse
considered here. Therefore, for some organisms a planetary ultraviolet crisis
brought on by atmospheric collapse need not necessarily precipitate a true biotic
crisis.
Finally, it should be noted that Mars may also have experienced periods of re-
duced UV radiation even since 3.5 Ga ago. Gulick et al. (1997) suggested that
episodic CO2 releases, 2 bar resulting from catastrophic floods may have resulted
in transient hydrothermalism during the past 3.5 Ga. Such episodes would have
resulted in an ultraviolet amelioration, as illustrated in Figure 8.1. The possibil-
ity of UV amelioration events concomitant with episodes of surface water avail-
ability since 3.5 Ga ago caused by transient CO 2 injections should be noted, be-
cause regardless of whether there was life on Mars they represent periods of
increased biological potential.
The foregoing exercise is an entirely theoretical one. We do not know if Mars
ever possessed life. However, it gives us rather interesting insights into how a
planet's atmospheric evolution could theoretically have profound consequences
for photobiological evolution and the challenges posed to life. It shows us that
the Earth's history is unique and that it is by no means a general template for
the ultraviolet history of other planets.
The Present Martian UV Flux: Implications for Human

Exploration and Settlement
Much of recent life on Earth, including plants and mammals, has mechanisms to
cope with UV-A (315-400 nm) and some UV-B radiation damage, such as re-
pair mechanisms and UV-screening compounds. However, these systems did not
evolve to cope with the very high radiation flux characteristic of present-day
Mars. This limitation has implications for the introduction of a present-day biota
to the Martian surface and for the types of materials that are used to protect that
biota, particularly in closed-loop ecosystems or "Mars greenhouses" (Boston
1981). Here I discuss in more detail the nature of the present-day Martian UV
regimen and the implications for the introduction of a biota, particularly in arti-
ficial ecosystems that use natural sunlight (Cockell and Andrady 1999).
The radiation flux that reaches a point on the surface of present-day Mars de-
pends on a variety of factors such as the presence of cloud cover, atmospheric
dust loading, season, and latitude (Sagan and Pollack 1974; Kuhn and Atreya
1979). As for the Earth, it can be calculated using a radiative transfer model (de-
tails are provided in Cockell et al. 2000), similar to methods used for calculat-
ing visible light on Mars (Haberle et al. 1993). Here I assume a 6 mb atmosphere
of CO 2 with no other significant gaseous constituents. During perihelion (clos-
est approach to the Sun) when the southern polar cap sublimes, the total atmo-
spheric pressure may increase to between 9 and 10mb, as was observed during
winter solstice at the two Viking landing sites (Hess et al. 1980). Thus, the as-
sumption of a 6 mb atmosphere is a typical summer value for most sites on Mars.
Neither H 20 (0.03%) nor the low levels of atmospheric O2 (0.13%) have sig-
nificant absorbance in the UV region at Martian column abundances.
The Martian polar regions do experience some production of ozone during the
winter and in early spring and fall when atmospheric temperatures drop (Barth
et al. 1973; Barth and Dick 1974; Lindner 1991). The quantity of ozone mea-
sured by Mariner 9 was equivalent to a maximum column abundance of 1.61 X
10 17 cm- 2 in the north polar region (50 0 -75°N). This quantity was measured in
winter and slowly decreased until it vanished in the summer.
Figure 8.2 shows the extraterrestrial flux for various scenarios on Mars, both
for a zenith angle of 0° at the equator and also for a more northern latitude with
lE+OO
Extraterrestrial flux inci-
dent on Mars
lE-Ol
- - ..0- - Zenith angle =0°, 1=0.5
lE-02 Zenith angle =0°, 1=2.0
'"E lE-03
~
~
u::
lE-04
lE-05
lE-06
Wavelength (nm)
FIGURE 8.2. Extraterrestrial spectrum and corresponding fluxes at the Martian surface.
Two cases are provided. First, flux received at a zenith angle of 0° (equator at vernal
equinox) with no ozone; second, flux for a solar zenith angle of 60° (solar zenith angle
at noon) at 60 N during spring (vernal equinox) with an ozone column abundance of 8.1 X
0
10 16 cm- 2 • For both cases, data are provided for a clear day with some dust loading (r =
0.5) and a medium-scale Martian dust storm (r = 2.0).
the protection of some ozone. The predominant effect of the ozone is a reduc-
tion in radiation around 250 nm, consistent with previous calculations (Kuhn and
Atreya 1979). Figure 8.3 shows how the spectrum on Mars with the sun directly
overhead compares with the same situation on Earth. The extraterrestrial spec-
trum (and thus also the flux received at the surface of the moon) is shown for
reference.
Unlike the Earth (see Xenopoulos and Schindler, Chapter 2, this volume), the
effects of altitude variations on UV flux are small on Mars. At the summit of
Mount Olympus, the largest mountain in the Solar System, which rises approx-
imately 27 km above the Martian reference datum, the atmospheric pressure may
be between 0.5 and 1 mb (Zurek 1992). The Hellas Basin is probably the low-
est point on Mars, approximately 5 km below the reference datum. Average pres-
sure here might be approximately 10 mb (Zurek 1992), although it is conceiv-
able that it would rise higher than this at perihelion as 10 mb was found at the
Viking landing site during perihelion. The total UV-B and UV-C variation be-
tween the Hellas Basin and the summit of Olympus Mons spans a range that lies
between 2% and 3% on either side of average UV values found at the reference
datum. The calculated 2% enhancement in UV flux near the summit of Olym-
pus Mons may not reflect the actual UV radiation environment experienced on
the structure. Classical observations of Olympus Mons and of other high con-
structs on Mars indicate that the volcano is the site of frequent cloud cover, most
likely CO 2 cirrus (Martin et al. 1992). The frequent presence of such clouds is
likely to be the prime controller of the local UV radiation regimen. During the
1981-1982 opposition, Akabane et al. (1987) measured the optical thickness of
an Olympus Mons cloud, attributing to it a maximum value of 0.5. To first or-
1E+01
1E+00 Extraterrestrial flux

(Near-earth and lunar)
1E-01
Martian surface flux
(zenith angle of 0°)
N 1E-02
E Surface of earth
~ 1E-03
(zenith angle of 0° )
x
"
u::
1E-04
1E·05
1E-06
200 250 300 350 400
Wavelength (nm)
FIGURE 8.3. The spectrum at the surface of Mars and the Earth at a zenith angle of 0°.
The extraterrestrial spectrum is also shown for reference.
TABLE 8.1. Instantaneous UV flux (zenith angle = 0°) and daily fluences (vernal
equinox for Earth and Mars, 2-week light period for moon) for UV-A, UV-B,
and UV-c.
Earth Moon Mars
Instantaneous Daily Instantaneous Daily Instantaneous Daily
flux fluence flux fluence flux fluence
(W/rn2) (kJ/rn 2) (W/rn2) (kJ/rn 2) (W/rn2) (kJ/rn2)
uv-c -0 -0 8.3 10,039 3.4 120
(200-280 nrn)
UV-B 2.0 39 18.5 22,377 7.9 286
(280-315 nrn)
UV-A 56.8 1,320 74.2 89,752 31.1 1,126
(315-400 nrn)
Total DNA-weighted 21 2,358 2.8 X 106 950 19,950
irradiance (relative
to present-day Earth)
For Mars, the mean distance from the Sun is taken.

DNA-weighted irradiances are given as relative values to the terrestrial instantaneous value at
IJ = 0°. Note that for daily fluence DNA weighted irradiances are divided by 1000.
Note that for the moon far UV (1-200 nrn) is also a concern.
der, then, the reduction in UV flux on Olympus Mons due to cloud cover is
enough to entirely cancel the effect of increased flux resulting from altitude rel-
ative to the reference datum.
What about the effects of this UV radiation environment on a biota transferred
to Mars? From Table 8.1 and Figure 8.3 it can be seen that there is a substan-
tially greater UV-B flux on Mars and also a UV-C flux. Because most action
spectra peak sharply at these wavelengths, these wavelengths should be removed
from any ecosystem. However, because the day length on Mars is almost iden-
tical to the Earth and so is the obliquity (tilt of the axis) of the planet, UV flux
at any given latitude can be made similar to Earth by simply changing the spec-
tral quality of the instantaneous flux using UV-screening materials. The trans-
mission characteristics of a material that would emulate the terrestrial UV flux
are shown in Figure 8.4.
On Mars, UV A radiation is less than on Earth (Table 8.1). The biological con-
sequences, if any, are unclear. UV-A radiation can cause reductions in growth
in plants and inhibition of photosynthesis in some microorganisms (Buhlmann,
Bossard and Uehlinger 1987; Kim and Watanbe 1994; Quesada, Mouget and Vin-
cent 1995). However, UV-A activates photolyase (required for thymine dimer
repair) and can counteract other effects of UVB radiation. Because no material
will be 100% efficient at removing UV-B or UV-C, UV-A is probably of some
use in ecosystems on Mars.
Furthermore, for some organisms UV-A radiation can be beneficial. Bees use
UV-A to recognize the portion of their field of view that constitutes "sky," and
they also employ polarized light for navigation and direction finding. In the nat-
1.0
0.8
CD
t..) 0.6 0
c:: c:
> ct
I
~
:t::
·E :::::l
en
c::
0.4
.=
~
0.2
0
200 250 300 350 400 450 500
Wavelength (nm)
FIGURE 8.4. The transmission characteristics for a material used on the surface of Mars to
reduce the Martian UV flux to similar values at the surface of the Earth. Because Mar-
tian day length and obliquity are similar to the Earth, the material can be used at any lat-
itude to simulate the terrestrial flux.
ural absence ofUV radiation (for example, during cloudy days), bees may switch
to a secondary form of navigation using landmarks such as foliage and rocks im-
printed by them during the most recent flight to the food source (Brusca and
Brusca 1990). However, this cannot be used as a long-term secondary system.
Early evidence shows that in some species of spiders UV-A reflectance of the
webs is used to lure prey (Craig and Bernard 1990). UV-A is also important in
tetrachromatic vision in some species of fish (Bowmaker and Kunz 1987), as
well as in vision (Makino et al. 1985) and pheromone recognition (Alberts 1989)
in some lizards. Whether the UV-A radiation at 55% of terrestrial levels at any
comparable latitude on Mars is detrimental to insects or other animals with UV
vision has not been examined over a long period. However, equatorial regions
of Mars receive similar levels of UV-A radiation to temperate regions on Earth.
Insects, lizards, and other animals with UV-A-dependent vision perform well at
these latitudes on Earth. It is likely that so long as polarization is maintained and
the Martian atmosphere is relatively cloud-free, the lower UV-A radiation regi-
men on Mars will not be detrimental.
For pollinators, UV -A might be allowed into a closed-loop ecosystem, prefer-
ably with natural polarization. Supplementary addition ofUV-A with lamps could
be arranged, at least in UV -poor environments where pollinators and animals
with UV-A-dependent vision are required to perform optimally.
A possible concern might be whether the UV A and blue light levels at 55%
of terrestrial values are sufficient to induce photolyase response to repair DNA
damage caused by UV-B radiation and whether other systems such as DNA ex-
cision repair can be effectively used to compensate. Probably this is not a con-
cern, as cloud cover on Earth frequently decreases the UV-A:UV-B ratio. How-
ever, experiments would be useful.
Changes in wavelength composition of radiation will also affect organisms dif-
ferently. For example, the relative amounts of visible radiation and UV radiation
reaching the inside of an ecosystem may result in changes in interspecies com-
petition (Gold and Caldwell 1983). Amphibians, for example, show differential
sensitivity to UV radiation, as do plants and coral morphs (see other chapters in
this volume for a detailed discussion). These interspecific differences will be a
factor for consideration in very complex extraterrestrial closed-loop ecosystems.
The degree to which free interspecies competition is allowed to occur will de-
termine the degree to which relative UV responses and, thus, wavelength com-
position of the UV radiation environment must be considered.
We can summarize the UV radiation strategy for artificial ecosystems on Mars:
UV -CO Attempt to eliminate all wavelengths below 290 nm, which show a steep
increase in effect in most known terrestrial biological action spectra. Their im-
pact is exacerbated when considered in terms of a biologically effective irra-
diance for the Martian or extraterrestrial UV flux. Of the 900 times more dam-
age estimated for free DNA on the Martian surface, almost 78% (biologically
effective irradiance) is caused by the UV-C portion of the spectrum.
UV-B. Eliminate the UV-B part of the spectrum as effectively as possible or at
least reduce it to terrestrial levels (about a three- to fivefold reduction on Mars).
UV-A. Given that UV-A on Mars is slightly less than found on the surface of
Earth, all ambient Martian UV-A might be allowed to reach the biota. This
condition will allow for normal repair processes against the very small amount
of UV-B that may penetrate through artificial screening materials. For com-
plex ecosystems, UV -A may be important for insect pollinators and other an-
imals with UV-A-dependent vision.
UV Radiation and Extrasolar Planets

Ultraviolet radiation has been a ubiquitous influence on the course of biological
evolution on Earth, and particularly on the anoxic Archean (3.9-2.5 Ga ago)
Earth before the formation of the ozone column. Because UV emissions are a
ubiquitous feature of all stars, the involvement of UV radiation in the early evo-
lution of life is likely to be a factor for extrasolar planets orbiting other stars.
Recently there have been great advances in our ability to detect and study ex-
trasolar planets, and it is likely that during the coming decades we will develop
the technology to study Earth-sized planets orbiting other stars. Through spec-
troscopy we will gather information on their atmospheric compositions. This in-
formation can be used in simple radiative transfer models to assess their surface
UV radiation regimes. Here I present some calculations on these environments

(see Cockell 1999).
Stars are generally classified according to the Hertzsprung-Russell classifica-
tion. This classification groups stars according to their luminosity and surface
temperature. F stars emit more UV radiation in the biochemically more damag-
ing UV-C region (200-280 nm) because they are hotter. Stars later in the
Hertzsprung-Russell classification, such as K stars, emit less UV radiation. Our
own sun, a typical G2 star, sits roughly between these two star types. Calcula-
tions using a photochemical model of the UV radiation environment of an Earth-
like world with an atmosphere containing oxygen and ozone orbiting typical F,
G, and K stars (Kasting, Whittet and Sheldon 1997) suggested that, with an ozone
column, UV flux may not be much worse than on Earth for an F star planet and
that K star planets would have a substantially better UV radiation environment.
Here an action spectrum for DNA (see Figure 1.2) is used as a generalized bi-
ological dosimeter to draw some exobiological conclusions on the degree to which
the UV radiation environment of anoxic planets orbiting F, G, and K main se-
quence stars may act as factor in the evolution of life. Anoxic planets are con-
sidered, because this is similar to the early atmospheres of the terrestrial planets
in which there was no significant net biotic contribution of O2 to the atmosphere
(Walker et al. 1983). Comparisons to UV irradiance calculations for Archean
Earth at a time about 3 Ga are made. These environments are also assessed us-
ing the UV -shielding habits of present-day terrestrial organisms.
The UV Radiation Environment of Extrasolar Planets

To calculate the incident UV flux received by a planet in orbit around an F, G,
or K main sequence star, three typical stars of these spectral classes were taken
from the IUE Low-Dispersion Spectra Reference Atlas, which provides the UV
data acquired by the International Ultraviolet Explorer (Heck et al. 1984). In this
chapter the G star is catalog number HD10307 (Henry Draper classification) and
the K star is number HD22049. These two stars are the same as were used by
Kasting, Whittet and Sheldon (1997). The F star used here is HD40136. The dis-
tance to these stars is calculated using trigonometric parallax with the parallax
measurements obtained either directly from the Hipparcos satellite observations
database or the SIMBAD astrophysical database (Centre de Donnees astro-
nomiques de Strasbourg, Strasbourg, France). Interstellar attenuation is assumed
to be negligible. These distances are 12.64, 3.22, and 15.04 pc, respectively. Fig-
ure 8.5 shows the spectrum across the UVC and UVB range (200-320 nm) at
the midpoint of the habitable zone for each of the stars. The habitable zone is
the zone around the star where temperature conditions are suitable for stable liq-
uid water to exist (see Kasting, Whittet and Reynolds 1993).
To calculate the UV flux on an anoxic planet orbiting these stars, these spec-
tral data are input into a UV radiative transfer model, identical to the one de-
scribed in Chapter 1. In this model, CO2 and N2 were considered as the major
......
.............
...........:
......
"
.
:" . _ _ _ Fstar
_._._._ Gstar FIGURE 8.5. The spectrum in the

•.•.•.•.•• K star UV -B region emitted from typical
10 -5 F, G, and K main sequence stars.
The spectrum is given for the mid-
200 220 240 260 280 300 320
point of the habitable zone (2.35,
Wavelength (nm) 1.38, and 0.69 AU, respectively).
atmospheric constituents of a primitive anoxic atmosphere, as they are believed

to have been on Archean Earth. A dust-free atmosphere was assumed, and grav-
ity was taken as 9.8 m S-2 for a planet with comparable density and size to Earth.
Data are provided for a stellar zenith angle of 0°. Other atmospheric constituents
are described later. For the purposes of this chapter, the inner limit of the habit-
able zone was taken as the distance at which a runaway greenhouse effect oc-
curs, such as has occurred on Venus, and the outer limit was taken as the dis-
tance for eady Mars-like conditions (Kasting, Whittet and Reynolds 1993).
Wavelengths below 200 nm are not taken into account. Most planetary atmo-
spheres effectively attenuate lower wavelengths, particularly those containing
CO 2 . However, greater fluxes of cosmic and gamma rays on planets in more en-
ergetic galactic environments may also cause biochemical damage and influence
the nature of biological evolution. This might be the case, for example, for stars
in dense star clusters.
Two partial pressures can be used to bound the parameter space of CO 2 par-
tial pressures. A partial pressure of 40 mb, which may be similar to the CO 2 par-
tial pressures on Earth 2.7-2.2 Ga suggested from Precambrian soil weathering
profiles (Rye, Kuo and Holland 1995), can be taken as the lower limit. Ten bar
can be taken as the upper limit, which is the highest value suggested for early
Earth (Walker 1985). The position in the habitable zone will affect the possible
CO2 concentrations. For example, at the upper limit of CO 2 partial pressure, con-
densation becomes a problem at the outer limits of the habitable zone (Kasting
1997), which is one of the key constraints in postulating high CO 2 atmospheres
as a mechanism for generating warm, wet conditions on early Mars. At the in-
ner region of the habitable zone, high CO 2 will contribute to a runaway green-
house effect. Indeed, these limitations are often used to help define the bounds
of the habitable zone. Given the wide parameter space of partial pressures that
have been suggested even for Archean Earth, which has a geologic record, here
values between 40 mb and lObar are considered for each star to cover a range
of possible values and to evaluate the effects of pC0 2 on the photobiological
environment.
Nitrogen is the second major constituent of the atmospheres of the terrestrial
planets. It does not absorb UV in the regions of biological interest, but at partial
pressures greater than 0.1 bar it can make a significant contribution to Rayleigh
scattering, particularly in atmospheres with CO 2 partial pressures below 1 bar.
Here data are provided for two N2 partial pressures (0.1 bar and 1 bar). The lat-
ter value approximates to present-day Earth and may have been similar to early
Earth (Kasting 1993); the former value provides an estimate of the effects of an
order-of-magnitude reduction of N2 in more diffuse atmospheres.
In Table 8.2, the DNA-weighted irradiances are provided for some typical
atmospheric compositions at distances from the stars described earlier. For com-
parisons to Archean Earth about 3 Ga ago, the biologically effective irradiance
on Earth at this time can be calculated as described in Chapter 1 for a zenith an-
gle of 0°. The value is about 100 Wm -2. As a direct comparison, the radiation
environment of a G star other than the sun has been calculated here (HDI0307).
At a distance of 1 AU (1 AU = 1 astronomical unit = distance from Earth to the
Sun = ~149 million km), the weighted irradiance for a 40 mb CO 2, 0.8 N2 bar
atmosphere is 132.7 W m- 2, which is similar to values using the UV spectrum
from our sun. If this is reduced according to a 25% reduction of luminosity (as
was the case for the early Sun), the value is approximately 97 W m- 2, almost
identical to the Archean calculations for our own sun.
The calculations made here are for a zenith angle of 0° because this provides
a generic comparison. It is also the upper bound for instantaneous UV exposure.
TABLE 8.2. DNA-weighted irradiances for the surface of planets orbiting the three star
types: F, G, and K main sequence stars.
Atmospheric K star G star F star
condition 0.4 AU 0.98 AU 0.84 AU 1.77 AU 1.5 AU 3.2 AU
0.1 bar N z
40 mb CO 2 47.9 8.3 324.6 73.1 2607 572.9
1 bar CO2 19.7 3.4 137.1 30.1 981.9 215.7
10 bar CO 2 2.9 0.5 20.4 4.6 141.3 31.0
1 bar N z
40 mb CO 2 25.8 4.3 178.4 40.2 1302 286.1
1 bar COz 14.3 2.4 100.2 22.6 708.8 155.7
10 bar CO2 0.4 0.3 19.3 4.3 133.8 19.2
AU, astronomical units.

Data are shown for the inner and outer region of the habitable zone (the region around the star where
liquid water is stable).
Data are shown for various atmospheric compositions. The values are for instantaneous UV flux
(zenith angle = 0°).
Calculation of total diurnal fluence is perhaps more useful for considering poten-
tial biological effects. However, without obliquity information and sidereal peri-
ods of extrasolar planets, then detailed calculations are less meaningful. Using in-
formation returned from extrasolar planetary searches, total daily fluences (in J
m- 2) could be calculated and time-integrated biochemically effective irradiances
derived. An example of the importance of this information is found on Archean
Earth. As was described in Chapter 1, Archean day length was shorter than today
(possibly -12-14 h compared to today's 24 h) and so daily fluence was approx-
imately 50% less than it would be if the planet had the same day length as today.
Life on Anoxic K Star Planets

The parameter space of the biochemically effective irradiances received in the
habitable zone of a K star planet is well below that estimated for Archean Earth
(see Table 8.2). The weighted irradiance at the outer edge of the zone is 11 %
that on Archean Earth, and even at the inner edge of the zone the irradiance is
63% of that on Archean Earth, taking the most diffuse atmosphere (40 mb CO 2 ,
0.1 bar N2 ). For higher column abundances of CO 2 and N2 , effective irradiances
are reduced still further (Table 8.2). The weighted irradiance is still substantially
greater than the surface of present-day Earth under an ozone shield (approxi-
mately 118 and 680 times greater at the outer and inner region of the habitable
zone, respectively). For a planet with a similar atmospheric composition as
Archean Earth ~3 Ga (40 mb CO 2 , 1 bar N2 ), weighted irradiances are 50% less
than the 40 mb CO 2 , 0.1 bar N2 atmosphere (Table 8.2). Although the early Earth
is thought to have had higher UV fluxes and biologically effective irradiances
than present-day Earth (Sagan 1973; Margulis, Walker and Rambler 1976;
Garcia-PicheI1998; Rettberg et al. 1998; CockellI998), they clearly did not pre-
vent the evolution of life as is evidenced by the Archean fossil record (Schopf
and Packer 1987). Many repair and protection strategies seen even on present-
day Earth would have been sufficient to reduce biologically effective UV irra-
diances on Archean Earth to values in exposed regions of present-day Earth
(CockellI998). However, these mechanisms, both physical and biological, would
probably have helped life to spread into exposed habitats. In comparison to
Archean Earth then, UV fluxes on K star planets do not prevent the evolution of
life, but they may well reduce the dependence on protection and repair processes
early in planetary history, assuming similar UV sensitivities as terrestrial bio-
chemical systems.
Because the solar output in the UV region as well as the surface UV flux on
early Earth are not precisely known, using them to consider the biochemical ef-
fects of UV radiation on extrasolar planets may result in an assumption inside
an assumption. For example, we do not know that Archean Earth did not have an
atmospheric UV absorber. It is therefore useful to demonstrate the survivability
of UV fluxes on anoxic K star planets using present-day terrestrial organisms.
Deinococcus radiodurans is an aerobic gram-positive coccoid microorganism
with high radiation resistance that is believed to result from high desiccation re-
sistance (Mattimore and Battista 1996). The latter selection pressure has resulted
in impressive levels of recombination repair. In analogy to the way in which

some hyperthermophiles provide us with the upper bounds for temperature tol-
erance, D. radiodurans provides us with a convenient upper UV radiation resis-
tance for an exposed and isolated single-celled organism. Gascon et al. (1995)
examined the UV tolerance of D. radiodurans under a 1.7 W m- 2 UV source,
emitting primarily at 254 nm. They demonstrated dose tolerances up to 400 J
m- 2 without significant loss of viability. The dose estimates they derive are sim-
ilarto those measured under a 254-nm UV source by Caimi and Eisenstark (1986).
If the UV source of Gascon et al. is weighted to the DNA action spectrum
value at 255 nm, then the organisms in these experiments are being subjected to
an equivalent DNA effective irradiance of approximately 43W m- 2. This value
is an estimate. For example, it would be better to weight the UV flux against a
specific action spectrum for D. radiodurans loss of viability. However, this spec-
trum has not been acquired. If we assume that DNA is the primary target of dam-
age (and indeed the loss of viability action spectra for a wide diversity of micro-
organisms follows the DNA absorbance profile), then the DNA action spectrum
provides us with a useful benchmark for comparison. The value is almost iden-
tical to the value for the biochemically effective irradiance for the surface of a
planet with the diffuse 40 mb CO2, 0.1 bar N2 atmosphere orbiting the inner edge
of a K star habitable zone, and it is about five times higher than for the same
planet at the outer region of the habitable zone. Thus, D. radiodurans can prob-
ably survive the instantaneous dose associated with exposed habitats on anoxic
planets orbiting a K star throughout the habitable zone.
As well as instantaneous dose, the total dose that an organism is capable of
surviving is also important. The dose at which D. radiodurans begins to show
appreciable loss of viability under a 1.7 W/m 2 source is about 500--600 J m- 2,
which corresponds to a time of about 5 min; this is clearly lower than a typical
day length. However, in combination with other strategies, survival and growth
over longer periods is possible. Many cyanobacterial mats can absorb and scat-
ter UV radiation in the upper layers of the mat such that, at a depth of 0.5 mm
or greater, UV radiation is reduced to 1% or less of incidence (Garcia-Pichel,
Mechling and Castenholz 1994). If we assume that reciprocity holds for D. ra-
diodurans, i.e., that total dose not dose rate is correlated to loss of viability, then
it is apparent that an organism that grows in a matlike structure with a 99% re-
duction of incident UV radiation in the lower layers of the mat and with the re-
pair processes of D. radiodurans could grow on the exposed surface of an anoxic
planet circling a K star at the inner region of the habitable zone with a day length
of about 17 h. Thus, direct comparisons with present-day terrestrial organisms
support the biological comparisons to Archean Earth and suggest that life in ex-
posed habitats on K star planets is possible.
Life on Anoxic F Star Planets

The UV radiation output of F stars has two significant differences to G and K
stars. First, the UV spectrum is essentially Planckian in the UV, unlike G and
K stars, where output is subluminous. Thus, the G- and K star UV radiation en-
vironment is more clement than would be expected from blackbody predictions.

Second, F stars emit proportionally more UV radiation in the UV -C region.
Because most action spectra show a sharp increase in biological effect in the
UV -C, any preferential increase in shorter wavelengths may result in a dispro-
portionately greater biochemical effect. Thus, for any given distance from an F
star and for most atmospheric compositions, UV -C radiation contributes a greater
proportion of the biochemically effective dose than is the case for G and K stars
(typically approximately 10% more).
At the inner limit of the habitable zone for a planet with 40 mb CO 2 and a 0.1
bar N2 atmosphere, the weighted irradiance is 27 times greater than Archean
Earth and for the outer limit it is just over six times greater. For a planet to
achieve the same or a lower value of weighted irradiance as Archean Earth, it
would have to be greater than 8.5 AU, nearly twice the outer limit of the habit-
able zone; even for a 1 bar CO 2 atmosphere, the required distance is still beyond
the habitable zone. Thus, for many F star planets, biochemically effective irra-
diances may be higher than Archean Earth.
As for other planets, higher CO 2 concentrations may provide significant UV
attenuation because absorbance and scattering in the UVC, particularly at high
partial pressures, can reduce biochemically effective irradiances. For a 1 bar CO 2
planet at 1.5 AU, the inner region of the habitable zone, the effective irradiance
is approximately 980 W m- 2, whereas for a 10 bar atmosphere it is an almost
an order of magnitude less and only slightly greater than that suggested for
Archean Earth with a 40 mb C02 atmosphere. If Archean Earth had higher C02
partial pressures, then it is possible that such anoxic planets may have photobi-
ological environments even more clement than early Earth.
On F star planets with CO 2 partial pressures of a few bar or less, abiotic UV-
specific atmospheric absorbers will improve the biological suitability of the planet
very significantly. If we take a planet with an atmosphere of 40 mb CO 2 and 1
bar N2 orbiting an F star at 1.5 AU and introduce a UV-C- and UV-B-absorb-
ing sulfur haze from volcanism into the radiative transfer model, as was origi-
nally considered by Kasting et al. (1989) for early Earth, and at a column abun-
dance of 1.5 X 10 17 mol cm- 2 (similar to the column abundances suggested for
early Earth), then the biochemically effective irradiance drops by more than an
order of magnitude from 1302 to just above 30 W m- 2. Although photochemi-
cal models are required to determine the concentrations of sulfur that would be
expected for any given planetary atmosphere, the data illustrate that in the F star
environment even modest column abundances of atmospheric sulfur can reduce
biochemically effective irradiances to values similar to many G and K star plan-
ets without such shields.
Sagan and Chyba (1997) consider an organic haze on early Earth as a possi-
ble shield for high ammonia mixing ratios required to heat early Earth. Organic
hazes such as the ones they considered (and the one found in the upper atmo-
sphere of Saturn's moon, Titan) typically may have an optical depth of about 7
in the UV region. Even with an optical depth of only 3, an organic haze would
be sufficient to reduce biochemically effective doses for a DNA-like molecule
by more than an order of magnitude to approximately 100 W m- 2 at the inner
region of the habitable zone on a planet with a diffuse 40 mb CO 2, 0.1 bar N2

atmosphere. For an optical depth of 7, the effective irradiances drop to about one
order of magnitude higher than present-day Earth, so that even a thinly matted
organism on a planet with a diffuse atmosphere would enjoy the same UV radi-
ation environment as present-day life on Earth in an exposed habitat.
Oceans may also be significant for the evolution of life because they can at-
tenuate UV radiation, particularly short UV-C wavelengths. The Archean Earth
was dominated by an oceanic lithosphere (Lowe 1992), and if the water inven-
tory during accretion was high enough around other stars then oceanic habitats
may constitute a significant percentage of some extrasolar planetary surfaces. For
an oceanic planet orbiting the F star in this paper (HD 40136), at the inner re-
gion of the habitable zone the depth that is required to achieve the same bio-
chemically effective irradiance at a zenith angle of 0° as an exposed habitat on
Archean Earth is about 10 m; to reduce DNA effective irradiances to values found
in exposed regions on the present-day Earth under the protection of an ozone
column, the depth is 45 m. These depths drop to 5 m and 35 m, respectively, for
the outer regions of the habitable zone. In the region between these depths, vis-
ible light from the F star is still greater than 1% and thus within the region that
corresponds to the photic zone on Earth. Thus life, including the data point of
terrestrial oceanic photosynthetic life, would find a photobiologically clement
habitat in the oceans of an F star planet.
Although atmospheric and oceanic UV attenuation may provide more clement
biological conditions-and certainly the discovery of such shields and oceans
on F star extrasolar planets will have significant photobiological implications-
planets without such shields cannot be ruled out as abodes for life. For a sub-
surface biota and completely shielded organisms living under rocks or similar
environments, the F star UV environment will clearly not be a limitation.
Again, present-day terrestrial organisms are a source of insight. Rocks are a sub-
strate that effectively attenuates light. Nienow, Friedmann and coworkers demon-
strated that at the lower depths of the cryptoendolithic communities that frequently
inhabit the subsurface layers of Antarctic sandstones, light levels may be reduced
to 0.005% of incidence (Nienow, McKay and Friedmann 1988; Nienow and Fried-
mann 1993). In the upper layers, irradiances drop to approximately 10% of inci-
dence. Short-wavelength UV radiation will be preferentially scattered, causing
greater reductions in the UV region, but if we assume for heuristic purposes that
the UV flux is also reduced to 0.005% of incidence at the lower levels of the rock,
then the biologically effective irradiance in such a rock on the surface of a planet
at the inner region of an F star habitable zone will be about 0.13 Wm- 2, similar
to exposed regions on present-day Earth. Even at higher levels of the rock where
UV may be 0.1 % of incidence and the DNA effective irradiance about 3 W m- 2,
an organism with the repair capabilities of D. radiodurans could inhabit these sub-
strates. Thus, endolithic habitats not only offer a microenvironment that might
shield organisms from extreme terrestrial and extraterrestrial planetary climatic con-
ditions (Friedmann et al. 1986; McKay 1993), but they are also a potential refuge
from extrasolar UV fluxes. This condition is true for other lithic habitats.
Evolution on Extrasolar Planets: Mode and Tempo

We cannot speculate on the physiologies that might specifically evolve on a planet
subjected to an F star UV flux from the beginning of evolution. It seems rea-
sonable to suppose that this selection pressure, if it had been more intense, would
be even more likely to result in organisms able to survive this flux. The ability
of organisms that have evolved on a G star planet and in some potentially uni-
versal planetary habitats such as rocks to illustrate survival and potential growth
on an F star planet suggests that the F star UV radiation environment would not
prevent the evolution of life, even in exposed habitats.
A further question regarding these environments is whether a different UV
flux could be responsible for positive evolutionary developments. These consid-
erations were touched upon in Chapter 1 in the context of high UV radiation on
early Earth. It is possible that in the earliest stages of prebiotic evolution, UV
flux may have had a contribution to make to organic complexification, some
products of which may have had prebiological significance (Sagan and Khare
1971; Bernstein et al. 1999). However, once a biochemical scaffolding did be-
gin to emerge from the more random building blocks of chemistry, most macro-
molecules would have had well-defined structure-function relationships. Dis-
ruption of structure by radiation invariably results in critical disruption of function
in any well-defined biochemical scaffolding.
As discussed in Chapter 1, higher UV fluxes such as those experienced on F
stars may have the potential to drive higher rates of mutation and thus a faster
tempo of evolution. However, given the potential damage caused by UV radia-
tion, it is clear that the overwhelming selection pressure is probably to protect
from UV radiation rather than to allow for increased rates of mutation. Thus, as
for early Earth, it is not necessarily clear that varying UV fluxes on extrasolar
planets would have a role to play in the rate of evolution on planetary surfaces.
It is plausible that other biochemistries might elvove to harness short-wavelength
UV radiation. Insofar as UV radiation represents a source of energy, then it could
be used in photosynthesis. The induction of photolyase by wavelengths as short
as 310 nm demonstrates that photoreceptors could evolve that absorb UV radia-
tion. By extension they could transfer this energy into photosystems and other
energy capturing reactions. The apparent nonuse of UV radiation in photosyn-
thesis on Earth might be because a tradeoff exists between energy required to re-
pair damage and energy potentially acquired in photosynthesis. In most terres-
trial phototrophs it would appear that the break-even point does not extend into
the short-wavelength UV region. Whether UV capturing photosystems ever
evolved on early Earth and whether they would evolve in a microbiota subjected
to higher doses of UV radiation (including UVC radiation) is currently specula-
tive.
The foregoing calculations provide insights into the potential theoretical tools
at our disposal to consider the photobiological environment of extrasolar plan-
ets. As we identify more of these bodies and discover the composition of their
atmospheres, so we will have the ability to define quite accurately the UV radi-
ation fluxes at their surfaces.
Conclusions
Extraterrestrial environments often have quite different UV radiation fluxes com-
pared to the Earth, both in absolute values and spectral quality. Using radiative
transfer models and biological insights, it is a relatively easy task to investigate
the potential biological effect of these environments. Although these calculations
are necessarily speculative, they provide a quite useful perspective point from
which to understand the unique photobiological history of Earth and to under-
stand how altered extraterrestrial photobiological regimens could result in quite
different outcomes. Here this was demonstrated with Mars and with extrasolar
planets. Finally, calculation of these regimes also has direct practical use. If we
intend to explore the surface of Mars and the moon and possibly to establish a
long-term human presence, then it will be necessary to understand the extrater-
restrial UV radiation regimens and the potential effects on materials and biota.
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Index
acid precipitation, 52, 68 bacterioplankton, 48, 154

action spectra, 3, 5, 15, 39, 85, 158, 203 beneficial effects of UV radiation
actinometers, 120 artificial ecosystems, 203
aerosols, 40, early Earth, 16
albedo, 42,45 extrasolar planets, 213
altitude. See atmosphere corals, 127
amino acids biogeochemical cycles, 101
leaf content, 103 biological weighting functions. (See
mycosporine-like. (See MAA) action spectra)
Antarctic bleaching, corals, 125, 134
lakes, 51, 160 boreal lakes, 48
ozone hole, 38,82,150,161,173
phytoplankton, 160 Calvin cycle, 99
primary productivity, 160, 177 carbaryl, insecticide, 69
anthocyanins, 92 carotenoids, 125, 135
anti-oxidants, 97, 135 canopy, plants, 44, 52, 81, 91
anti-predatory behavior, 67 cell size, 184
Archean Earth CFCs. See chlorofluorocarbons
atmospheric composition, 4, 6 chalcone synthase, 91, 98
day length, 5 chlorofluorocarbons, 38
oceanic UV attenuation, 8 chlorophyll, 49
Arctic Chlorojlexus, 14, 16
aquatic ecosystem, 161 Chroococcidiopsis, 11, 13
ozone hole, 38, 82, 150 chromophores, 48
artificial ecosystems, 200 closed-loop ecosystems, 200
asteroid and comet impacts, cloud cover, 40, 81, 173
photobiological effects of, 22 colonization of land, 19
astrobiology. See exobiology community composition, 26, 73, 141, 151,
attenuation coefficients, 8, 50 183
atmosphere copepods, 187
altitude effects, 45, 81, 202 cut-off filters, 64, 83, 204
clouds, 40, 81 cyanobacteria, 2, 49, 155, 179, 210
tropospheric pollutants, 40 cytoskeleton, 127
219
220 Index
Deinococcus radiodurans, 14, 209 Hertzsprung -Russell classification, 206

Delta-Eddington. See radiative transfer High Arctic, 50
development, effects of UV on, 67 human exploration, of Mars, 200
dinoflagellates, 118, 155 humic substances. See organic carbon,
dissolved organic carbon dissolved
in early oceans, 8 hydrogen peroxide, 97
in present day lakes and oceans, 46, 48,
151, 154 ice, attenuation by, 43, 174, 187
DNA damage insect herbivory, 103
amphibians, 71 International Ultraviolet Explorer (IUE),
cyanobacteria, 155 206
early Earth, 5 interspecies differences, 27, 74
in atmospheric modeling, 39 iron, as UV absorber, 2, 8, 11
Mars, 197
plants, 98 K!f extinctions, 23
DOC. See organic carbon, dissolved krill, 170, 186
dosimetry, 44, 120
lamps, use in UV supplementation, 84,
eggs, effects of UV on 103
amphibians, 63, 70 land plants, evolution of, 19
ELDONET,151 leaf development, effects of UV radiation
epidermal transmittance. See leaf optical on, 85, 90,96
properties leaf optical properties, 85, 93, 96, 100
erythemal irradiances. See sunburn lithic habitats, 11
eukaryotes, evolution of , 19 litter decomposition, 101
evolution, mode and tempo, 16,213 luminosity, solar, 3
evolutionary photobiology, 196
excision repair, 14, 71, 98 MAA, 13, 49, 128, 139, 141, 157
exclusion studies. See cut-off filters macroalgae, 159
exobiology, 195 Mars
extinction coefficients, 128 exploration of, 200
extraterrestrial flux, 201, 207 life on , 195
extrasolar planets, 206 UV environment of, 196
ferulic acid, 95 Martian poles, 197, 201
flavonoids, 13, 91, 97 measurements, UV radiation, 39, 42, 120,
fluoranthene, 67 151,177
ferric and ferrous iron, 9, 11 melanin, 70
food chain, effects of UV radiation, 185 mesocosm experiments, 186
forest canopy, 44 microbial mats, 11,211
freshwater lakes, UV penetration into, 48 microfossils, 2
fungus. See pathogens mixing, in lakes and oceans, 52, 160
Montreal Convention, 150
ge1bstoff. See organic carbon, dissolved morphs, corals, 138
global warming, 38, 53, 173 mucus, corals, 130
growth chambers, 83, 92 mutation rates, 17
growth rates, 100, 133, 158, 203
gymnosperms, 93,100 nitrogen oxides, 22, 41
nitrogen, 101, 103, 135, 159, 161, 183
Hellas Basin, UV radiation in , 202 nitrogen fixation, 91, 155
herbivory, 91, 102 nutrient metabolism, 182
Index 221
oceans sex, evolution of, 17

measurement of UV, 151 snow, reflection off, 43
UV penetration, 8, 46, 119, 121, 152, solar flares, 26
174,212 solar zenith angle, 4, 42, 44
Olympus Mons, 202 spectroradiometers, 122
organic carbon, dissolved, 8,48, 150, 153 sporopollenin, 160
organic haze, 211 stratospheric ozone depletion. See ozone
oxidative damage, 69, 91, 96, 125, 135 sublethal effects of UV, 63, 125, 186
ozone sulfate, 41
chemistry, 38 sulfur dioxide, 40, 41
depletion, 20, 38, 81, 150, 161, 173 supernovae, photobiological effects of, 25
Mars, 201 synergisms, effects with other stressors
seasonal and daily variations, 20 acid rain, 53, 68
asteroid/comet impact events, 22
pathogens, 68, 73, 91 chemical contaminants, 69
Phaeocystis, 184 fire, 75
phenolic compounds, 91 fungal infection, 68
phenyl-alanine ammonia-lyase, 91, 98 global warming, 52, 172
photolyase. See photoreactivation heat stress, 126
photobleaching, 48, 53 heavy metals, 159
photoreactivation, 14, 71, 98, 137, 154, low temperature, 181
203 supernovae, 25
photosynthesis, reduction, 99 water temperatures, 126
photosystem damage, 5, 99, 155 sunburn (erythemal), 39,41, 82
phytoplankton, 119, 157, 176
picoplankton, 154 thymine dimers. See photoreactivation
plants, UV tolerance of, 45, 80 Total Ozone Mapping Spectrometer, 39
pollution, 40 transplant experiments, 138
polycyclic aromatic hydrocarbons (PAH), troposphere,
69 dust, 40
positive roles of UV radiation. See infleunce on UV flux, 40, 81
beneficial effects of UV radiation
predators, 74, 186 UV -C radiation, 8, 202
primary productivity, 126, 150, 180 UV protection by physical substrates, 12
Proterozoic, 18
pyrimidine dimers, 71, 98, 121, 154 vacuum UV
vision, use of UV radiation in, 203
quasi-biennial oscillation, 20 volcanoes, photobiological effects of, 25,
41
radiative transfer, 3, 196
ratios, of UV radiation, 40, 44, 81, 83, water
171, 173 attenuation by, 8, 46, 50, 119, 151
reflectivity, water, 46 acidification, 52
repair mechanisms, 14, 71, 98, 137,203
reproduction, effects of UV radiation on, xenobiology. See exobiology
63, 90, 126, 158
Rubisco, 99, 126, 155 yield reductions, 99
scytonemin, 13,44, 157 zenith angle, 4, 42, 44, 46

shikimate pathway, 91, 129 zooxanthellae, 118, 125, 136

Ecosystems, Evolution, and Ultraviolet Radiation (PDFDrive)

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Ecosystems, Evolution, and Ultraviolet Radiation

Springer Science+Business Media, LLC

Ecosystems, Evolution, and

Library of Congress Cataloging-in-Publication Data

I. Photobiology. 2. Evolution (Biology). 3. Ultraviolet radiation. 4. Ecology.

Printed on acid-free paper.

© 2001 Springer Science+Business Media New York

Production managed by Michael Koy; manufacturing supervised by Jerome Basma.

In 1928, Harry Marshall speculated on the role of ultraviolet radiation in ex-

Cambridge, UK CHARLES S. COCKELL

1 A Photobiological History of Earth 1

2 Physical Factors Determining Ultraviolet Radiation Flux

3 Ultraviolet Radiation and Amphibians . . . . . . . . . . . . . . . . . . . . .. 63

4 Ultraviolet Radiation and Plant Ecosystems 80

5 Ultraviolet Radiation and Coral Communities ................ 118

6 Ultraviolet Radiation and Aquatic Microbial Ecosystems ........ 150

7 Ultraviolet Radiation and the Antarctic Coastal

8 Ultraviolet Radiation and Exobiology ...................... 195

ANDREW R. BLAUSTEIN THOMAS A. DAY

JOHN B. HAYS ADOLFO MARCO

PETER D. HOFFMAN DAVID W. SCHINDLER

UV Radiation from the Archean to the

and oceanic upwelling to mop up the O2 so produced. A diversity of direct ge-

Calculation of UV Radiation on Early Earth

The DNA-weighted irradiances received at the surface of the Earth may be

Archean Day Length

TABLE 1.1. Weighted irradiances for various atmospheric scenarios discussed

(Laskar, 10utel and Robutel 1993)-then although the instantaneous DNA-

Atmospheric Absorbers and Effects on

A plausible contaminant in the early Earth atmosphere was a CH4 -generated

Biological Effects of High UV Radiation Flux

Methods for Coping with UV Flux on Early Earth

_ _ _ Archean Oceans (8=60°)

Present·day Oceans (8=0°)

Biologically Effective Irradiance (DNA)Wm-2

Intertidal and Terrestrial Habitats

Ultraviolet Radiation-Screening Compounds

Adapted from Cockell (1998).

have been considerable advantages to be gained by exploiting higher PAR lev-

Photosynthesis in the Archean

thesis in cyanobacteria and similar organisms. The greater UV -A contribution in

Beneficial Effects of High UV Radiation on Archean Earth?

The Archean-Proterozoic Transition

UV and the Colonization of Land

UV Radiation in the Proterozoic and Phanerozoic

Seasonal and Daily Changes in Ozone Column Abundances

0 3 column is subject to natural variations in column abundance (Lean 1997 and

Stochastic "Catastrophic" Changes in Ozone

be increased twofold, with important biological consequences (Cockell and

---0-- Generalized DNA damage

--<:>--- Generalized plant damage

cause it depends on precipitation patterns and how much of the NO is washed

Relative Biological Effects of Different Mechanisms

1 -: Polar depletion for

The shielding of the Earth from ultraviolet radiation by stratospheric ozone is

Transmission of Solar UV through the Atmosphere

although seasonal variations in stratospheric ozone concentration also have

Stratospheric Ozone Layer

Weighting Functions and Action Spectra

Absorption of UVR by Tropospheric Pollutants and Aerosols

Light extinction by aerosols is highly dependent on the optical thickness of

Seasonality and Solar Zenith Angle

Plant Canopy Shape and the Influences on UV Exposures