UNITED NATIONS
ENVIRONMENT PROGRAMME
UNEP
ENVIRONMENTAL EFFECTS OF OZONE
DEPLETION AND ITS INTERACTIONS WITH
CLIMATE CHANGE:
2006 ASSESSMENT
Pursuant to Article 6 of the Montreal Protocol on Substances that Deplete the Ozone Layer under
the Auspices of the United Nations Environment Programme (UNEP).
Copies of the report are available from
United Nations Environment Programme (UNEP)
P. O. Box 30552
Nairobi , Kenya
Published December 2006 by the Secretariat for The Vienna Convention for the Protection of the
Ozone Layer and The Montreal Protocol on Substances that Deplete the Ozone Layer United
Nations Environment Programme (UNEP)
United Nations Environment Programme (UNEP), P. O. Box 30552, Nairobi, Kenya
UNEP, Environmental Effects of Ozone Depletion: 2006
Assessment, United Nations Environment Programme
ISBN: 978-92-807-2821-7
Job No: OZO/0947/NA
Cover photograph © Luo Hong.
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ENVIRONMENTAL EFFECTS OF OZONE DEPLETION AND
ITS INTERACTIONS WITH CLIMATE CHANGE:
2006 ASSESSMENT
Introduction
This assessment was prepared by the Environmental Effects Assessment Panel for the Parties to
the Montreal Protocol. The assessment reports on some of the new findings since the last full
assessment of 2002, again paying attention to the interactions between ozone depletion and
climate change and their consequences for environmental and health issues. Simultaneous
publication of the assessment in the scientific literature aims to show the scientific community
how their data, modeling, and interpretations are playing a role in information dissemination to
the Parties to the Montreal Protocol and other policy makers. It is also hoped that the publication
will stimulate the scientific community to continue working on the gaps in knowledge that still
exist.
The 2006 assessment will be published in the Journal Photochemical & Photobiological
Sciences, 2007.
Jan van der Leun
Janet F. Bornman
Xiaoyan Tang
Co-Chairs of the Environmental Effects Assessment Panel
UNEP
United Nations Environment Programme
PO Box 30552
Nairobi, Kenya
http://www.unep.org/ozone
http://www.unep.ch/ozone
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TABLE OF CONTENTS
EXECUTIVE SUMMARY ........................................................................................................ xv
CHAPTER 1. CHANGES IN BIOLOGICALLY ACTIVE ULTRAVIOLET
RADIATION REACHING THE EARTH’S SURFACE................................................. 1
CHAPTER 2. THE EFFECTS ON HUMAN HEALTH FROM STRATOSPHERIC
OZONE DEPLETION AND ITS INTERACTIONS WITH CLIMATE CHANGE .. 25
CHAPTER 3. TERRESTRIAL ECOSYSTEMS, INCREASED SOLAR
ULTRAVIOLET RADIATION, AND INTERACTIONS WITH OTHER
CLIMATE CHANGE FACTORS ................................................................................... 65
CHAPTER 4. EFFECTS OF SOLAR UV RADIATION ON AQUATIC
ECOSYSTEMS AND INTERACTIONS WITH CLIMATE CHANGE. .................... 95
CHAPTER 5. INTERACTIVE EFFECTS OF SOLAR UV RADIATION AND
CLIMATE CHANGE ON BIOGEOCHEMICAL CYCLING................................... 133
CHAPTER 6. CHANGES IN TROPOSPHERIC COMPOSITION AND AIR
QUALITY DUE TO STRATOSPHERIC OZONE DEPLETION AND
CLIMATE CHANGE. .................................................................................................... 165
CHAPTER 7. EFFECTS OF STRATOSPHERIC OZONE DEPLETION AND
CLIMATE CHANGE ON MATERIALS DAMAGE. ................................................. 185
ENVIRONMENTAL EFFECTS PANEL MEMBERS AND UNEP
REPRESENTATIVES 2006 ........................................................................................... 201
REVIEWERS OF THE 2006 UNEP EFFECTS ASSESSMENT PANEL .......................... 205
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LIST OF ABBREVIATIONS
1,25(OH)2D
1,25-dihydroxyvitamin d
25(OH)D
25-hydroxyvitamin d
AK
Actinic keratosis
AO
Arctic Oscillation. A large-scale variation in Arctic wind patterns
APase
Alkaline phosphatase
APC
Antigen presenting cell
ASL
Above sea level
BCC
Basal cell carcinoma (s)
Br
Bromine (an ozone depleting chemical)
BrO
Bromine monoxide
BSWF
Biological spectral weighting functions
BWF
Biological weighting function
CAS
Chemical Abstracts Service
CC
Cortical cataract(s)
CDFA
Chlorodifluoroacetic acid
CDK
Climatic droplet keratopathy
CDOC
Colored dissolved organic carbon
CDOM
Colored (or chromophoric) dissolved organic matter
CPD
Cyclobutane pyrimidine dimmer
CFC
Chlorofluorocarbon. Ozone-damaging chemical (e.g., CFC12:
dichlorodifluoromethane. CCl2F2), now controlled under the Montreal
Protocol
CH
Contact hypersensitivity
CH4
Methane (a greenhouse gas)
CIE
Commission Internationale de l'Eclairage (International Commission on
Illumination)
Cl
Chlorine (an ozone depleting chemical)
CM
Cutaneous melanoma
CO
Carbon monoxide
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CO2
Carbon dioxide (a greenhouse gas)
COS
carbonyl sulfide
CPD
Cyclobutane pyrimidine dimer
Cu
Copper (Cu(I) and Cu(II) being different oxidation states)
DIC
Dissolved inorganic carbon
DMS
Dimethylsulfide
DMSP
Dimethylsulfoniopropionate
DNA
Deoxyribonucleic acid
DOC
Dissolved organic carbon
DOM
Dissolved organic matter
DON
Dissolved organic nitrogen
DSB
Double strand break
DTH
Delayed type hypersensitivity
DU
Dobson Unit (used for the measurement of total column ozone (1 DU=2.69 ×
1016 molecule cm-2)
EAE
Experimental allergic encephalitis
EDUCE
European Database for Ultraviolet Radiation Climatology and Evaluation
EESC
Equivalent Effective Stratospheric Chlorine
ENSO
El Niño Southern Oscillation. A large-scale climate variability in the Pacific
region
EP
Earth Probe (a NASA satellite)
EPA
Environmental Protection Agency
EV
Epidermodysplasia verruciformis
Fe
Iron (Fe(II) and Fe(III) being different oxidation states)
FMI
Finnish Meteorological Institute
GHG
Greenhouse gas
Glu I
A pathogenesis-related (PR) protein
HALS
Hindered Amine Light Stabilizer
HCFC
Hydrochlorofluorocarbon. Interim replacements for CFCs with small ozone
depletion potential (e.g., R22: chlorodifluoromethane CHClF2) to be phased
out
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HFC
Hydrofluorocarbon. Long-term replacements for CFCs, with zero ozone
depletion potential
Hg
Mercury (Hg0aq and Hg(II) being different oxidation states)
HIV
Human immunodeficiency virus
HPV
Human papillomavirus
HSV
Herpes simplex virus
HY5
Transcription factor HY5, which is a key downstream effector of the UVR8
(UV-regulatory protein) pathway
IBD
Inflammatory bowel disease
IL
Interleukin
Ink4a
Murine inhibitor of kinase 4a protein (gene in italics)
IPCC
Intergovernmental Panel on Climate Change
IPF
Immune protection factor
kda
Kilodalton
KNMI
Dutch National Institute for Weather, Climate and Seismology (The
Netherlands)
L·
Lipid radical
MAA
Mycosporine-like amino acids
Mb
Megabase, equal to 1 million base pairs
MC1R
Melanocortin 1 receptor
MHC
Major histocompatibility complex
MS
Multiple sclerosis
N2O
Nitrous oxide (a greenhouse gas that is also a source of NO2)
NAO
North Atlantic Oscillation. A large-scale variation and redistribution of
atmospheric mass in the Atlantic region producing large changes in the NH
dynamics
NASA
National Aeronautic and Space Administration (USA)
NaTFA
Sodium trifluoroacetate
NC
Nuclear cataract(s)
NCAR
National Centre for Atmospheric Research, USA
NH
Northern Hemisphere.
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NIMBUS-7
A NASA satellite
NIVR
Netherlands Agency for Aerospace Programmes
NMHCs
Non-methane hydrocarbons
NMSC
Non-melanoma skin cancer
NO
Nitric oxide (an ozone depleting gas)
NO2
Nitrogen dioxide (an ozone depleting gas)
NOAA
National Oceanic and Atmospheric Administration, USA
NOEC
No observed effect concentration
NOx
Nitrogen oxides
O3
Ozone
OCS
Carbonyl sulfide (also COS)
ODS
Ozone depleting substance(s)
·OH
Hydroxyl radical (and important atmospheric cleaning agent)
OMI
Ozone Monitoring Instrument (on board the Aura satellite)
OTR
Organ transplant recipients
P
Phosphorous
PAH
Polycyclic aromatic hydrocarbon(s)
PAM
Pulse amplitude modulated (fluorescence)
PAR
Photosynthetically active radiation, 400-700 nm waveband
PAUR II
Photochemical Activity and solar Ultraviolet Radiation campaign 2
pCO2
Partial pressure of carbon dioxide
PEC
Predicted environmental concentration
Pg
Peta gram (1x1012 grams)
PHR1
The gene encoding CPD photolyase
PNEC
Predicted no effect concentration
POC
Particulate organic carbon
POM
Particulate organic matter
PR
Pathogenesis-related proteins
PSC
Posterior subcapsular cataract(s)
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PSC
Polar stratospheric cloud (ice crystals which form at high altitudes in Polar
regions when the temperature is below a critical threshold)
Ptc
Murine patch protein (gene in italics)
PTCH
Human patch protein (gene in italics)
QBO
Quasi biennial oscillation (a shift in wind patterns - especially over the
tropics - with a period of approximately 2.2 years)
RA
Rheumatoid arthritis
RAF
Radiation amplification factor (a measure of sensitivity to ozone change)
ROS
Reactive oxygen species (·OH, for example)
RT
Radiative transfer
SAGE
Stratospheric Aerosol and Gas Experiment, a satellite-based instrument
SCC
Squamous cell carcinoma
SCC
Squamous cell carcinoma
SH
Southern Hemisphere
SZA
Solar zenith angle (i.e. the angle between zenith and the centre of the solar
disk)
TFA
Trifluoroacetic acid
Th1
T-helper 1
Th2
T-helper 2
TOMS
Total Ozone Mapping Spectrometer, a satellite-based instrument
Treg cell
T-regulatory cell
Troposphere
Lowest part of the earth's atmosphere (0-16 km)
UCA
Urocanic acid
UV
Ultraviolet. Wavelengths from 100 nm to 400 nm. Ozone and other
atmospheric gases progressively absorb more and more of the radiation at
wavelengths less than 320 nm. Only those greater than 290 nm are
transmitted to the Earth's surface
UV index
A standardised unit for providing UV information to the public
UV-A
Electromagnetic radiation of wavelengths in the 315 to 400 nm range
UV-B
Wavelength range 280-315 nm, as defined by CIE
UV-B
Electromagnetic radiation of wavelengths in the 280 to 315 nm range
UV-C
Electromagnetic radiation of wavelengths in the 100 to 280 nm range
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PSC
Polar stratospheric cloud (ice crystals which form at high altitudes in Polar
regions when the temperature is below a critical threshold)
Ptc
Murine patch protein (gene in italics)
PTCH
Human patch protein (gene in italics)
QBO
Quasi biennial oscillation (a shift in wind patterns - especially over the
tropics - with a period of approximately 2.2 years)
RA
Rheumatoid arthritis
RAF
Radiation amplification factor (a measure of sensitivity to ozone change)
ROS
Reactive oxygen species (·OH, for example)
RT
Radiative transfer
SAGE
Stratospheric Aerosol and Gas Experiment, a satellite-based instrument
SCC
Squamous cell carcinoma
SCC
Squamous cell carcinoma
SH
Southern Hemisphere
SZA
Solar zenith angle (i.e. the angle between zenith and the centre of the solar
disk)
TFA
Trifluoroacetic acid
Th1
T-helper 1
Th2
T-helper 2
TOMS
Total Ozone Mapping Spectrometer, a satellite-based instrument
Treg cell
T-regulatory cell
Troposphere
Lowest part of the earth's atmosphere (0-16 km)
UCA
Urocanic acid
UV
Ultraviolet. Wavelengths from 100 nm to 400 nm. Ozone and other
atmospheric gases progressively absorb more and more of the radiation at
wavelengths less than 320 nm. Only those greater than 290 nm are
transmitted to the Earth's surface
UV index
A standardised unit for providing UV information to the public
UV-A
Electromagnetic radiation of wavelengths in the 315 to 400 nm range
UV-B
Wavelength range 280-315 nm, as defined by CIE
UV-B
Electromagnetic radiation of wavelengths in the 280 to 315 nm range
UV-C
Electromagnetic radiation of wavelengths in the 100 to 280 nm range
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UVEry
Erythemally-weighted UV irradiance, where the irradiance is weighted by the
erythemal action spectrum.
UVI
A standard scale for reporting UV irradiance to the public. The UVI is a
unitless number which is 40 times the erythemally-weighted irradiance,
measured in units of W m-2.
UVR
Ultraviolet radiation
UVR8
UV-regulatory protein
VDR
Vitamin d receptor
VOC
Volatile organic compound (s)
WMO
World Meteorological Organization
WOUDC
World Ozone and UV Data Centre
XP
Xeroderma pigmentosum
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Environmental Effects of Ozone Depletion: 2006 Assessment
Interactions of Ozone Depletion and Climate Change
Executive Summary
Ozone and UV Changes
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The Montreal Protocol is working. The concentrations of ozone depleting substances in
the atmosphere are now decreasing. Outside Polar Regions, the decline of ozone seen in the
1980s and 1990s has not continued. In Polar Regions, there is much higher variability. Each
spring, large ozone holes continue to develop in Antarctica and less severe regions of depleted
ozone continue to develop in the Arctic. There is evidence that some of these changes are driven
by changes in atmospheric circulation rather than being solely attributable to reductions in
ozone-depleting substances, which may indicate a linkage to climate change. Global ozone is
still less than in the 1970s. Changes in ozone directly influence UV-B radiation, so elevated
UV-B radiation due to reduced ozone is expected to continue.
The future evolution of atmospheric ozone remains uncertain. It is expected to increase
slowly in the decades ahead, but it is not known whether it will return to higher,
similar, or lower levels than those prior to the onset of ozone depletion. Current chemical
models are unable to reproduce accurately all of the observed ozone variability, the rates of
future increases in greenhouse gases are not yet established, and interactions between ozone
depletion and climate change are not yet fully understood. Current models predict that ozone
will have recovered from the effects of man-made ozone-depleting gases by mid-century at
mid-latitudes, and about 1-2 decades later at polar latitudes.
Long term responses in UV-B radiation caused by ozone changes have been observed.
Increases in UV-B irradiance have occurred over the period of ozone depletion. At
unpolluted sites in the Southern Hemisphere, there is some evidence that UV-B irradiance
has diminished since the late 1990s. Because of improvements in the availability and
temporal extent of UV data we are now able to evaluate the changes in recent times
compared with those estimated since the late 1920s, when ozone measurements first became
available. The increases in UV-B radiation from about 1980 to the end of the 20th century
have been larger than the long-term natural variability.
The effects of aerosols and air pollutants on long-term variations in UV-B irradiance
may be comparable with those due to changes in ozone. At some sites in the Northern
Hemisphere, UV-B radiation may continue increasing because of the continuing reductions
in the attenuation by aerosols since the 1990s despite the cessation of ozone depletion.
Interactions between ozone depletion and climate change are complex and can be
mediated through changes in chemistry, radiation, and atmospheric circulation
patterns. The changes are in both directions: ozone changes affect climate, and climate
changes affect ozone. Contrary to what was predicted from some models in previous
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assessments, more recent models and the observational evidence suggest that stratospheric
ozone (and therefore UV-B radiation) has responded relatively quickly to changes in ozone
depleting substances, implying that climate interactions have not delayed these responses.
There is greater uncertainty about future surface UV-B radiation than future ozone,
since UV-B radiation will be additionally influenced by climate change. Climate change
can also affect UV-B radiation through changes in cloudiness, aerosols and surface
reflectivity, without involving ozone. The rate of climate change is accelerating. Temperature
changes over the 21st century are likely to be about 5 times greater than in the past century.
This will affect future cloud, aerosol and surface reflectivity. Consequently, unless strong
mitigation measures are undertaken with respect to climate change, profound effects on the
biosphere and on the solar UV radiation received at the Earth’s surface can be anticipated.
Health
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In addition to cortical cataract, nuclear cataract has been found to be associated with
polar UV radiation. Numerous studies have implicated exposure to solar UV radiation as a
causative factor in the development of cortical cataract. Several reports now confirm an
association between nuclear cataract and UV exposure. In addition, higher ambient temperatures
may increase the risk of nuclear cataract development. In contrast, there is insufficient evidence
to infer a causative role for solar UV radiation in the induction of posterior subcapsular cataract.
Exposure to sunlight is a significant risk factor for pterygium on the surface of the eye.
Pterygium is an inflammatory, proliferative and invasive lesion of the human cornea that can
severely impair vision. It is induced, in part, by the intracellular damage caused by UV-B
exposure. Genetic factors and the degree of long-term exposure to sunlight are important
parameters for the development of pterygia in populations of all skin colours.
Adverse photobiological effects of UV radiation on the eye can be enhanced by the
presence of clouds and are thus affected by climate change. Although direct sunlight does
not play a major role in acute solar photokeratitis, sunburn of the eye, or in cataract
formation, scattered and reflected UV-B radiation contribute to these disorders. Under
conditions of cloud cover and with lower light levels, the natural defence mechanisms of the
eye are relaxed, permitting greater exposure of the anterior surface of the eye and its internal
structures. At the same time, the effective UV-B exposure of the eye can be increased during
cloud cover due to scatter.
The incidence of squamous cell carcinoma (SCC), basal cell carcinoma (BCC) and
melanoma continues to rise. Approximate doublings in the incidence of all three types of
skin cancer have been projected in the Netherlands for the years 2000 to 2015 and in many
other countries with predominantly fair-skinned populations. The major increase in
melanoma incidence has been for thin (early) melanomas that have high survival rates. In
children, the incidence of melanoma is still rising and has been positively correlated with
environmental UV radiation exposure.
Susceptibility to skin cancer is increasingly recognised as being linked with subtle
variations in genes that code for proteins involved in prevention and repair of DNA
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damage. Such proteins function in defensive mechanisms that are crucial to the prevention
of skin cancers. The relevance of certain gene variations differ between skin cancer types and
these variations provide clues regarding the types of DNA damage and repair that are
important in each of the skin cancer types. Thus, there is a wide range in the occult
genetically determined susceptibility in a population. In the future, gene profiling may
accurately identify high-risk individuals.
UV-induced immunosuppression is a crucial factor in the generation of skin cancers. In
some subjects, this immunomodulation may lead to viral reactivation and a reduction in
vaccine efficacy. The lack of repair of UV-induced DNA changes decreases the resistance to
skin cancers and is a significant factor in the generation of such tumours. By effects both on
the virus itself and on suppression of immunity, solar UVR exposure can induce the
reactivation of latent herpes simplex virus leading to the re-emergence of cold sores. The
virus is a co-factor in the development of some skin cancers and conjunctival squamous cell
carcinomas in association with human papillomavirus infection. Limited evidence indicates
that UV radiation exposure can reduce the efficacy of vaccination, at least in genetically
predisposed individuals.
Vitamin D, formed by exposure of the skin to UV-B (with subsequent hydroxylation to the
active vitamin), may play a protective role against the development of several internal
cancers, autoimmune and some other diseases. A number of studies link low solar UV
exposure with a higher risk of some internal cancers, such as colorectal and prostate, and
autoimmune disease, such as multiple sclerosis and type 1 diabetes. As lack of exposure to
the UV-B in sunlight leads to suboptimal vitamin D levels, vitamin D has been proposed as
the protective factor in helping to prevent these diseases. The evidence to support the
protective role of solar UV-B exposure and whether this is mediated through vitamin D is not
definitive.
Personal strategies to protect the eye and skin from the adverse effects of high solar UVR
exposure are being adopted increasingly by the general public. Health campaigns in
several countries such as Australia, Canada, UK, and USA have raised the awareness of the
general public regarding protection from the sun. Broad-spectrum sunscreens, in widespread
use in mid-latitudes by fair-skinned individuals, minimise the erythemal effects of high sun
exposure. UV-absorbing soft contact lenses covering the entire cornea provide excellent
protection from solar UV-B for the eye, and are superior to some tinted sunglasses as the soft
contact lenses shield against UV radiation entering from the side or below.
It is not feasible to give a single recommendation for optimal solar UV-B exposure to allow
sufficient vitamin D synthesis while not increasing the risk of skin cancer. The solar UV-B
dose experienced by an individual varies greatly depending on time of the day, latitude,
altitude, season of the year, cloud cover, activity and type of clothing worn. Skin colour, age
and genetic background are other critical factors in determining the positive or negative
outcome of the exposure. Therefore the message regarding “safe” sun exposure depends on
the individual and place of residence.
The interaction between ozone depletion and global climate change may adversely affect
human health. At present, it is impossible to predict how global warming might alter the
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behaviour of people, especially those living in mid-latitudes, with respect to the amount of
time spent outdoors in sunlight. If temperatures rise, then personal solar UV radiation
exposure might be greater than at present. This would then have detrimental effects on the
incidence of skin cancer and cataract and on the immune system, although benefiting vitamin
D status.
Terrestrial Ecosystems
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Field studies, in which solar UV-B radiation is either augmented or attenuated, report
many effects on higher plants and on bacteria, fungi and other microbes. Although
photosynthesis of higher plants and mosses is seldom affected in field studies by UV-B
radiation, growth and morphology (form) of higher plants and mosses are often changed. This
can lead to small reductions in shoot growth and changes in the competitive balance among
species. Fungi and bacteria are generally more sensitive to damage by UV-B radiation than are
higher plants. However, the species differ in their UV-B sensitivity to damage. This can lead to
changes in species composition of microbial communities with subsequent influences on
processes such as litter decomposition. Changes in plant chemical composition are commonly
reported from experiments using enhancement or attenuation of UV-B radiation in sunlight.
Enhanced UV-B often leads to substantial reductions in consumption of plant tissues by
insects. In some cases this is because of altered insect behaviour, but changes in plant chemical
and physical characteristics induced by UV-B radiation usually account for the reduced
herbivory. Such modifications affect many interactions of plants with other organisms, both
above and below ground. More is now understood about the mechanisms of these interactions.
Although sunlight does not penetrate significantly into soils, the biomass and morphology
of plant root systems can be affected to a much greater degree than plant shoots. Root
mass can exhibit large declines with enhanced UV-B radiation. Also, UV-B-induced changes in
soil microbial communities and biomass, as well as altered populations of small invertebrates
have been reported and these changes have important implications for processing of mineral
nutrients in the soil. Many of these ecosystem-level phenomena appear to be the result of
systemic changes in chemical and physical properties of plants and in the nature of root
exudates.
UV-B radiation and other environmental factors that are undergoing changes such as
temperature, CO2, moisture and available nitrogen over large areas may interact to
produce a complex plant response. In several studies, plant growth was augmented by higher
CO2 levels, while on the other hand many of the effects of UV-B radiation were usually not
ameliorated by the elevated CO2. UV-B radiation often increases both plant frost tolerance and
survival under extreme high temperature conditions. Conversely, extreme temperatures
sometimes influence the UV-B sensitivity of plants. Plants that are drought tolerant are likely to
be more tolerant of high UV-B flux. Furthermore, UV-B radiation has been reported to alleviate
some symptoms of water stress. Biologically available nitrogen is exceeding historical levels in
many regions due to human activities. Studies show that plants well supplied with nitrogen are
generally more sensitive to UV-B radiation.
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Many new developments in understanding the underlying mechanisms mediating plant
response to UV-B radiation have emerged. UV-B radiation results in an activation of as yet
uncharacterised receptor molecules. These initial events engage signalling pathways that result
in altered plant gene expression and response. Exposure to UV-B induces some signals that are
UV-B-specific and some that have elements in common with those elicited by other
environmental factors. The use of shared signalling elements generates overlapping patterns of
gene expression and functional responses. This new information is helpful in understanding
common responses of plants to UV-B radiation, such as diminished growth, acclimation to
elevated UV radiation, and interactions of plants with plant consumer organisms. It also helps
in interpreting the interaction of various environmental stresses on plant growth and function.
Technical issues concerning the use of biological spectral weighting functions (BSWFs)
have been further elucidated. The BSWFs are multiplication factors assigned to different
wavelengths giving an indication of their relative biological effectiveness. They are critical to
the proper conduct and interpretation of experiments in which organisms are exposed to UV
radiation, both in the field and in controlled environment facilities. The characteristics of
BSWFs vary considerably among different plant processes, such as growth, DNA damage,
oxidative damage and induction of changes in secondary chemicals. Thus, use of a single
BSWF for plant or ecosystem responses is not appropriate.
Aquatic Ecosystems
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Recent field studies continue to show that even current solar UV-B radiation can
adversely affect aquatic organisms. Reductions in productivity and impaired reproduction
and development have been shown for phytoplankton, fish eggs and larvae, zooplankton and
other primary and secondary consumers exposed to UV-B radiation. UV-B-related decreases
in biomass productivity can be transferred through all levels of the food web, as well as cause
changes in species composition and structure and function of ecosystems. Decreases in
primary production would result in reduced sink capacity for atmospheric carbon dioxide,
with its related effect on climate change.
Experiments in large enclosures show that changes in community structure may be more
ecologically important than effects of enhanced UV-B on overall algal biomass. These
mesocosm experiments allow the experimenter to control the level of UV radiation on
plankton communities to simulate various levels of ozone depletion. Growth was inhibited by
ambient UV radiation in fixed-depth experiments but not in mesocosms where vertical
mixing exposed planktonic organisms to variable radiation regimes. A synthesis model
simulating mesocosm experiments suggests that enhanced UV-B could cause a shift from
primary producers to bacteria at the community level. Shifts in community structure could
have important consequences for carbon dioxide concentration in oceanic surface waters.
Recent studies have expanded our understanding of UV-B protection mechanisms for
aquatic organisms. UV radiation impairs photosynthesis, nitrogen fixation and damage
DNA, but most phytoplankton have developed mitigating measures including UV-absorbing
substances, repair enzymes and reactive oxygen species scavenging systems. However,
protection is not complete. Picoplankton cyanobacteria do not produce absorbing substances
but rely on fast cell division; these organisms have recently been found to be ubiquitous and
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to contribute more than 50 % to the productivity in aquatic habitats. Solar UV controls the
vertical position of macroalgae in the tidal zone. Organisms in the upper tidal zone have
developed effective screening and repair mechanisms.
UV-B-related decreases in primary-producer biomass have a negative effect on the growth
and survival of consumers, which form the higher levels in the aquatic food web. Specific,
direct UV B effects have been identified in a wide variety of consumers, including copepods
and other zooplankton, corals and sea urchins.
In their natural habitat, zooplankton face conflicting selection pressures, including
exposure to UV-B radiation and factors of global climate change. Invertebrate predators
cause an upward movement of the zooplankton during daylight hours, exposing them to high
levels of UV radiation at the surface. Besides vertical migration and UV screening,
zooplankton rely on photorepair of UV-B-induced DNA damage. Increases in water
temperature resulting from climate change are expected to increase enzymatic activity, which
would enhance photorepair.
Primary causes for a decline in fish populations are predation and poor food supply for
larvae; however, exposure of the larvae to enhanced UV-B radiation may further
contribute to this decline. Other major factors are overfishing, increased water temperature
due to global climate change, pollution, and disease. Imprecisely defined habitat
characteristics and the naturally high mortality rates of fish larvae render quantitative
assessment of specific UV-B effects difficult.
The concentration and chemical composition of dissolved organic matter in aquatic
ecosystems govern the penetration of UV radiation in the water column. UV radiation
affects the species composition of plankton communities and thus the concentration of DOM.
There is a strong link between early succession of zooplankton communities and terrestrial
plant communities within watersheds, which in turn are affected by climate change.
Consequently, climate change and UV radiation have the potential to affect species
composition in lakes and also to increase the invasion potential by imported species.
Biogeochemical Cycles
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Climate-related changes can alter the transfer of organic matter from terrestrial to
freshwater and coastal ecosystems and thereby influence UV radiation penetration into
water bodies, with major consequences for aquatic biogeochemical processes. These
changes are particularly prevalent in high latitude systems. Dissolved organic matter leaching
from or running off terrestrial ecosystems enters streams, rivers, lakes and, ultimately the
oceans. The coloured part of dissolved organic matter controls the penetration of UV radiation
into water bodies, but is also photodegraded by solar UV to release small inorganic molecules,
mainly CO2.
Future increases in the temperature of surface waters will enhance stratification of lakes
and the ocean, which will intensify effects of UV-B radiation on biogeochemistry in the
surface layer. This important effect is manifested by the extensive increase in transparency of
the water to UV-B radiation in the upper layer of stratified aquatic environments. These effects
The Environmental Effects Assessment Panel Report for 2006
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of climate change increase the impacts of UV-B radiation on biogeochemical cycles in the upper
layer of aquatic systems, thus partially offsetting the beneficial effects of an ozone recovery.
Climate change and changes in UV-B radiation influence the concentration of halogencontaining compounds that are involved in ozone chemistry in the atmosphere. Emissions
of halogen-containing compounds, for example, methyl bromide from higher plants, increase
with increasing air temperature. Recent observations indicate that methyl bromide
concentrations in the atmosphere are decreasing at a rate of 2.5 – 3.0 % per year but future
global warming may reduce the current rate of decline. Bromine and other halogen radicals are
also generated in UV-B radiation induced reactions of halogen-containing compounds both in
atmospheric aerosols present in the marine boundary layer and in surface waters. These
halogen-containing compounds may be transported by convection to the upper troposphere
where the bromine radical participates in ozone destruction.
UV-B can alter the biological availability and toxicity of metals in aquatic environments.
Although many trace metals are essential trace nutrients, all metals are toxic above a certain
concentration. In sunlit surface waters, however, they often exist in forms that are biologically
not available. Increased UV-B can alter the chemical form of metals to produce forms that are
available to aquatic organisms. For example, the UV-induced oxidation of elemental mercury
results in the formation of precursors to methyl mercury that can adversely affect human health
through bioaccumulation in aquatic food webs.
UV radiation drives photoreactions involved in cycling of marine sulphur, leading to the
production of atmospheric aerosols and cloud formation. Oceanic emissions of
dimethylsulphide (DMS) produce atmospheric aerosols that influence atmospheric radiation
and temperature. UV radiation induced transformation is an important sink of DMS in the
upper ocean. Carbonyl sulphide, another important sulphur compound in the upper ocean, is
produced in UV-B radiation induced reactions involving chromophoric DOM.
In terrestrial systems UV-B radiation can affect cycling of carbon and nutrients through
changes in decomposition and soil biology. Exposure to solar UV-B radiation causes direct
photodegradation of dead plant material, especially in arid climates. When plants are exposed to
UV-B radiation, changes in plant root exudation and/or the chemistry of dead plant material
influence soil organisms and biogeochemistry. Changes in carbon and nutrient cycling induced
by UV-B radiation can interact with responses to climate change and so may influence longterm ecosystem carbon budgets.
Air Quality
•
Models and measurements suggest that ozone transport from the stratosphere to the
troposphere may have decreased by approximately 30% in the last 30 years. Ozone
concentrations near the ground are a key indicator of air quality. Tropospheric ozone
concentrations are affected by UV-B radiation, local weather systems, and pollutant
concentrations. Stratospheric ozone depletion has increased the rate of ozone production in
the troposphere due to enhanced UV-B radiation but reduced the amount of ozone
transported from the stratosphere to the troposphere.
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The predicted future increase in stratospheric ozone may increase tropospheric
temperature and concentrations of ozone in the atmospheric boundary layer. Models
predict that ozone concentrations in the atmospheric boundary layer will increase globally by
33 to 100% during the period 2000 to 2100 due to the combined effects of climate change,
atmospheric pollution, and increases in stratospheric ozone. The impact of this increase on
climate is difficult to quantify as tropospheric ozone concentrations are very variable, both in
space and time.
Changes in the concentration of tropospheric hydroxyl radical caused by changes in
UV-B radiation are now much better quantified. Tropospheric hydroxyl radical (OH) is
one of the major oxidizing agents in the atmosphere, destroying trace gases that are involved
in ozone depletion, climate change, and urban air pollution. The globally averaged OH has
been observed to change on short time scales (months – years) but not in the longer term.
Recent measurements in a relatively clean location over 5 years showed that OH
concentrations can be predicted by the intensity of solar ultraviolet radiation. If this
relationship is confirmed by further observations, this approach could be used to characterize
the oxidation efficiency of the troposphere in different chemical regimes using UV radiation
measurements, thus simplifying assessment of air quality.
Confidence in models estimating the impact of ozone change on the oxidation capacity
of the atmosphere has improved for unpolluted locations. Measurements of UV radiation
and chemical composition, including OH in the lower atmosphere, now normally agree with
chemical models to within the measurement accuracy in unpolluted air both for clear skies
and uniform cloud cover. However, in moderately and heavily polluted urban regions or
forested environments, models and measurements disagree. These model uncertainties
underline the importance of local measurements of tropospheric ozone, especially in areas
where air may be polluted.
An analysis of surface-level ozone measurements in Antarctica suggests that there has
been a significant change in the chemistry of the atmospheric boundary layer in this
region as a result of stratospheric ozone depletion. Measurements of ozone
concentrations in the atmospheric boundary layer show a recent (since 1990) increase in
surface ozone concentrations consistent with more UV radiation reaching the earth’s surface
during ozone hole episodes, and the enhanced production of nitrogen oxides from the ice.
Thus, the Antarctic lower atmosphere is estimated to be more oxidizing now than before the
development of the ozone hole, which may have adverse consequences through changing
bioavailability of metals.
The tropospheric concentration of HFC-134a, a potent greenhouse gas and the main
known anthropogenic source of trifluoroacetic acid, is increasing rapidly. The increase
is in agreement with the known usage and atmospheric loss processes. Observations in both
hemispheres between 1998 and 2002 show that the concentration of HFC-134a has been
increasing by up to 12% per year. The good agreement between observations and known
sources and sinks gives increased confidence in predictions of the environmental build-up of
trifluoroacetic acid. The increasing concentration of HFC-134a may contribute to an
acceleration of climate change.
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Risks to humans and the environment from substances produced by atmospheric
degradation of hydrochlorofluorocarbons (HCFCs) and hydrofluorocarbons (HFCs)
are considered minimal. These include trifluoroacetic acid (TFA) and chlorodifluoroacetic
acid. Recent studies reinforce the conclusion of small environmental and human health risks
from current environmental loadings in fresh- and salt-water. Although the amounts of these
compounds are expected to continue to increase in the future because of climate change and
continued use of HCFCs and HFCs, current information suggests that this is not an issue of
great importance.
Perfluoropolyethers, substances proposed as HCFC substitutes, have very large global
warming potential and show great stability to chemical degradation in the atmosphere.
These compounds are commonly used as industrial heat transfer fluids. It is not known
whether these substances will contribute significantly to global warming and its interaction
with ozone depletion. Their risks should be further evaluated.
Materials Damage
•
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Plastics and wood exposed to solar UV radiation undergo degradation losing their useful
properties over a period of time. This damage is dose-dependent and limits the outdoor
lifetimes of most materials. The damage is exacerbated by higher ambient temperatures, higher
humidity levels, and atmospheric pollutants. Light stabilizers and surface coatings are generally
used to control the solar-UV induced damage to materials. Higher UV levels will require higher
levels of stabilizers resulting in higher cost of materials used outdoors.
Several novel UV stabilizers and product fabrication techniques that improve UVresistance have been reported. New variants of effective light stabilizers, such as stabilizer
compounds that bind to the polymer and are therefore less likely to be lost by leaching, have
been reported recently. Mechanisms of synergistic effects of stabilizer blends have been further
elucidated and will contribute to the design of new light-stabilizer blends. Continued research on
this topic will facilitate the development of strategies that are better able to protect materials
exposed to solar UV-B radiation.
An emerging trend towards the use of nanoscale fillers may improve the UV stability of
plastics formulations. These nanoscale fillers have smaller average particle sizes and often
yield better mechanical properties than conventional fillers. Initial data suggest some of the
nanoscale fillers may also act as good light stabilizers and extend the service life of products
exposed to outdoor UV radiation. However, potential interference of these fillers with the
effects of conventional light stabilizers or other additives such as antioxidants or flame
retardants has not yet been fully evaluated.
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Using powdered wood as a filler in plastics is continuing to be explored, and the effect of
these fillers on UV-stability depends on the type of wood. Powdered wood and other plant
materials are used as low-cost natural fillers in some plastics products intended for outdoor
use. Recent research indicates that several of these plant-derived fillers can either enhance
the photodamage or act as a photostabilizer for the plastic material, depending on the source
of the natural filler material and processing method used with the material. However, the
lignin content in wood filler absorbs solar UV-B radiation and promotes photodamage of the
polymer component. Identifying sources and processing technologies for these bio-based
fillers without compromising light stability of filled polymers can lead to low-cost UV-stable
plastics products for certain outdoor applications.
The Environmental Effects Assessment Panel Report for 2006
Chapter 1. Changes in biologically active ultraviolet radiation
reaching the Earth’s surface
R. L. McKenziea, P. J. Aucampb, A. F. Baisc, L.O. Björnd, M. Ilyase
a
National Institute of Water and Atmospheric Research, NIWA Lauder, PB 50061 Omakau,
Central Otago, New Zealand.
b
Ptersa Environmental Management Consultants, PO Box 915751, Faerie Glen, 0043, South Africa.
c
Laboratory of Atmospheric Physics, Aristotle University of Thessaloniki,
Campus Box 149, 54124 Thessaloniki, Greece.
d
Department of Cell and Organism Biology, Lund University, Sölvegatan 35, SE-22362, Lund, Sweden.
e
School of Environmental Engineering, University College of Engineering North Malaysia, Kangar, Malaysia.
Summary
The Montreal Protocol is working. Concentrations of major ozone-depleting substances in
the atmosphere are now decreasing, and the decline in total column amounts seen in the
1980s and 1990s at mid-latitudes has not continued. In polar regions, there is much greater
natural variability. Each spring, large ozone holes continue to occur in Antarctica and less
severe regions of depleted ozone continue to occur in the Arctic. There is evidence that some
of these changes are driven by changes in atmospheric circulation rather than being solely
attributable to reductions in ozone-depleting substances, which may indicate a linkage to climate change. Global ozone is still lower than in the 1970s and a return to that state is not expected for several decades. As changes in ozone impinge directly on UV radiation, elevated
UV radiation due to reduced ozone is expected to continue over that period.
Long-term changes in UV-B due to ozone depletion are difficult to verify through direct
measurement, but there is strong evidence that UV-B irradiance increased over the period of
ozone depletion. At unpolluted sites in the southern hemisphere, there is some evidence that
UV-B irradiance has diminished since the late 1990s. The availability and temporal extent of
UV data have improved, and we are now able to evaluate the changes in recent times compared with those estimated since the late 1920s, when ozone measurements first became
available. The increases in UV-B irradiance over the latter part of the 20th century have been
larger than the natural variability.
There is increased evidence that aerosols have a larger effect on surface UV-B radiation than
previously thought. At some sites in the Northern Hemisphere, UV-B irradiance may continue to increase because of continuing reductions in aerosol extinctions since the 1990s.
Interactions between ozone depletion and climate change are complex and can be mediated
through changes in chemistry, radiation, and atmospheric circulation patterns. The changes
can be in both directions: ozone changes can affect climate, and climate change can affect
ozone. The observational evidence suggests that stratospheric ozone (and therefore UV-B)
has responded relatively quickly to changes in ozone depleting substances, implying that climate interactions have not delayed this process. Model calculations predict that at midlatitudes a return of ozone to pre-1980 levels is expected by mid 21st century. However, it
may take a decade or two longer in polar regions. Climate change can also affect UV radiation through changes in cloudiness and albedo, without involving ozone and since temperaThe Environmental Effects Assessment Panel Report for 2006
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
ture changes over the 21st century are likely to be about 5 times greater than in the past century. This is likely to have significant effects on future cloud, aerosol and surface reflectivity.
Consequently, unless strong mitigation measures are undertaken with respect to climate change, profound effects on the biosphere and on the solar UV radiation received at the Earth’s
surface can be anticipated.
The future remains uncertain. Ozone is expected to increase slowly over the decades ahead,
but it is not known whether ozone will return to higher levels, or lower levels, than those present prior to the onset of ozone depletion in the 1970s. There is even greater uncertainty
about future UV radiation, since it will be additionally influenced by changes in aerosols and
clouds.
Introduction
UV-B radiation (280-315 nm) has important influences on biological processes, and is
strongly absorbed by atmospheric ozone (in both the stratosphere and the lower atmosphere).
Reductions in stratospheric ozone are therefore important because of the corresponding increases in UV-B radiation reaching the Earth’s surface. While some UV radiation is needed
to synthesize vitamin D, which is necessary for human health, increases in UV-B radiation
are also harmful for human health, for example, for melanoma and other health effects (see
Chapter 2). Increases in UV-B radiation also increase damage to a wide range of organic
molecules, including DNA molecules, and generally lead to increased harm to a diverse range
of biological (see Chapters 3-5), and physical (see Chapters 6-7) processes. UV-B radiation
is influenced by many factors other than ozone. These include changes in clouds, aerosols,
air pollution, and surface reflection, all of which are influenced by climate change. Since the
publication of the 2002 UNEP Effects Panel Assessment1, 2 there has been continuing progress in research to understand the causes and effects of ozone change. There have been no
changes in our understanding of basic principles since the previous assessment, but there
have been significant improvements in our knowledge of past ozone and UV radiation, which
put recent changes into a better historical context. Here we assess this new knowledge of
ozone changes, their effects on UV radiation, and the interactions between ozone depletion
and climate change.
Generally, the damaging effect of UV radiation increases towards shorter wavelengths. In
this paper we focus on the erythemally-weighted UV radiation (UVEry),3 for which a 1% reduction in ozone leads to a 1.2% increase in damaging radiation at high sun elevations.4
However, other weighting functions with different sensitivities to ozone are more appropriate
for other processes.4 In some cases, the wavelength dependence of the effects is not yet well
quantified. The continued availability of spectral measurements of solar radiation will therefore be crucial to quantifying these effects.
Ozone changes
The science of ozone depletion has recently been assessed by the WMO Scientific Assessment Panel.5 In recent years, the geographic and seasonal extent of Antarctic ozone depletion
has varied greatly from year to year (Figure 1-1), depending on the prevailing meteorological
conditions. The springtime stratospheric ozone “hole” is expected to recur over the next decades, and there will continue to be a large year-to-year variability in its severity and environmental impact.
Ozone depletion is less severe in the Arctic, where there is also very large year-to-year variability (Figure 1-1), which is expected to continue, depending on the minimum temperatures
reached. With global climate change, temperatures in the Arctic stratosphere are expected to
2
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
continue to decrease, increasing the likelihood of severe ozone depletion due to heterogeneous chemistry on the surfaces of polar stratospheric clouds. For every degree of stratospheric
cooling, a reduction in ozone of 15 Dobson Units can be expected.6 This sensitivity is three
times larger than had been estimated previously from model calculations. Therefore, future
polar ozone depletion may be more susceptible to climate change than previous models had
suggested.
Ozone depletion in polar regions
has an impact on the ozone depletion at mid latitudes.7-9 For example, it has been shown that approximately 50% of the ozone depletion at mid-southern latitudes is
attributable to the export of ozonepoor air from Antarctica.8
Since the previous assessment,1, 2
there has been increased evidence
for a cessation of ozone reductions
at mid-latitudes. A statistical
analysis of satellite-derived ozone
profiles indicated that the rate of
ozone loss in the upper stratosphere (at 35-45 km altitude) has
diminished globally, and that these
changes are consistent with
changes in total stratospheric chlorine.11 In a follow-up study it was
shown that the slow-down extended to the lower stratosphere.12
Figure 1-1. Total average column ozone poleward of latitude 63° in
the springtime of each hemisphere (March for the Northern Hemisphere (NH) and October for the Southern Hemisphere (SH)), in
Dobson Units (DU), based on data from various satellite instruments. The horizontal lines represent the average total ozone for
the years prior to 1983 for the NH and SH. Based on Fig 4-7 in,5
updated from.10
It had been predicted that detection of any recovery in the total column of ozone, which is
most relevant for environmental impacts of UV radiation at the Earth’s surface, would not be
expected for several years,13, 14 because of the natural inter-annual variation in several contributing dynamical factors,15-17 which recent studies have shown may be larger than previously assumed.18-20
Statistical trend analyses have demonstrated that the total column amount of ozone at midlatitudes reached a minimum in the late 1990s, and since then may have started to increase.21
At mid-latitudes, the column amount of ozone in the 2002-2005 period was approximately
3% below 1980 levels in the Northern Hemisphere, and 6% below 1980 levels in the Southern Hemisphere,5 which is similar to that in the period ending 1998-2001.10, 22
The observed changes in ozone are broadly consistent with those expected from changes in
atmospheric chemistry that would result from the actions mandated by the Montreal Protocol.
Changes in observed ozone are compared with estimated changes in effective equivalent
stratospheric chlorine in Figure 1-2. However, changes in atmospheric circulation were also
found to have a substantial influence on ozone variability, especially in the lower stratosphere,23, 24 and have contributed to a significant portion of the observed increase in ozone in
the Northern Hemisphere in recent years. These dynamical changes may be a consequence of
climate change. If that is the case, these interactions may be important considerations for
predicting future changes in ozone.
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
The future evolution of atmospheric ozone remains uncertain, firstly because current chemical models are unable to reproduce accurately all of the observed ozone variability,5 secondly because the rates of future increases in greenhouse gases are not yet established,25 and
thirdly because interactions between ozone depletion and climate change are not yet fully understood, as discussed later in this document. A full recovery to ozone amounts present in the
1970s prior to the onset of ozone depletion is not expected for several decades at best.
Factors affecting UV radiation received at the
Earth’s surface
Solar ultraviolet radiation is attenuated by interaction with atmospheric constituents in the
Earth’s atmosphere through absorption and scattering processes.
Furthermore, its variability is
controlled by astronomical facFigure 1-2. Area-weighted total ozone deviations for 60°S-60°N,
tors, including those that deterestimated from ground-based measurements. Data have been
mine the angle at which solar ra- deseasonalised and adjusted to remove the effects of solar-cycle and
diation arrives at the Earth’s atthe quasi-biennial oscillation (QBO). The thick line represents the
mosphere and the irradiance that effective equivalent stratospheric chlorine (EESC), scaled to fit the
data from 1964-2005 (scale on right). Adapted from Fig 3-1
is distributed per unit area at the ozone
in.5
top of the atmosphere. These
astronomical factors and their roles are known very accurately.
Absorption in the UV-B region is due to ozone primarily, to a lesser extent to SO2, NO2 and
other minor species, and also to aerosols. Scattering occurs on molecules, aerosols, and
clouds. Solar UV radiation is reflected by the clouds and the Earth’s surface (land and water). All these processes have been extensively investigated. Although the physical interactions are well understood, the quantitative description is incomplete. Because of their complexity, the effects of clouds in particular remain difficult to calculate. As discussed later,
clouds, aerosols, and surface albedo are factors that are likely to be affected by climate
change, and may therefore impact the long-term variability of surface UV radiation. The effects of ozone on UV radiation are well understood. Since the previous assessment,1, 2 new
studies have quantified the effects of other factors on UV radiation and the related uncertainties, as discussed below.
Clouds constitute by far the most important factor controlling UV radiation for any given solar elevation angle, (e.g., 26) and introduce a high variability in surface UV irradiance that
limits the detection of influences from ozone.27 Although clouds mainly attenuate radiation,
new experimental data have confirmed results from previous studies by reporting large enhancements of UV radiation under partly cloudy skies.28-31 Enhancements up to 40% have
been observed at 420 nm (blue light) when the solar disk is visible, but are smaller in the UVB region.32, 33 The biological importance of enhancements of UV radiation under broken
clouds, which may at times be sustained for hours, must be taken into consideration.
The most relevant radiation quantity for atmospheric chemistry is the actinic flux, which is
the omni-directional flux passing through a sphere, rather than the cosine-weighted irradiance
on a horizontal surface (see Chapter 6, Figure 6-2). Above clouds, localised increases of the
UV actinic flux of between 60–100% have been observed.34 Below the clouds, the actinic
flux was found to be 55–65% smaller compared to clear skies. In both cases there is a direct
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
influence on photochemistry, with consequences on tropospheric atmospheric composition.
Although these effects can be adequately modelled for homogeneous and stratified clouds, it
is extremely difficult to simulate broken cloud conditions adequately.
The interaction of clouds with other processes produces significant effects on radiation that
either reaches the surface or is reflected to space. Increased scattering within the clouds interacts with molecular scattering, producing complex wavelength dependencies in the radiation scattered towards space and detected by satellite instruments.35 Similarly, increased scattering by cloud droplets increases the possibility that these photons are absorbed by atmospheric constituents that are inside the cloud (e.g., ozone, NO2, aerosols).36, 37 A cloud layer
over snow or ice covered surfaces may substantially increase the UV dose at the surface,
through strengthening of multiple scattering. A twofold increase in UV radiance from the
overhead sky has been observed under cloudy conditions compared with the clear sky in Antarctica, whereas the increases in the visible and in the infrared were much larger, with enhancements of up to factor of 100 in the near infrared.38
Aerosols and trace gases emitted near the surface of the Earth can also have large impacts on
UV radiation.39-41 Several studies have quantified aerosol radiative properties - particularly
their UV absorbing efficiency - from ground based measurements of solar UV radiation.42-48
Some satellite retrievals (e.g., TOMS) overestimate surface UV radiation by between 5 and
10% over areas with high aerosol load, especially in the presence of strongly absorbing aerosols. By combining measurements and radiative transfer (RT) modelling,47-50 methods have
been suggested for applying corrections to satellite retrievals.51 These corrections will enable
more accurate satellite estimates of UV irradiance in the future.
New evidence has shown that in urban areas, aerosols and air-pollutants such as ozone and
nitrogen dioxide can significantly attenuate solar UV radiation.40, 52-54 Recent studies have
shown that aerosols and trace gases from biomass burning can penetrate into the stratosphere,55 and consequently affect its chemistry. Increases in UV-B and UV-A solar radiation
observed during the last two decades in Germany and Greece56, 57 cannot be explained by
changes in ozone amounts alone, and thus it is necessary to include diminishing influences
from other factors such as pollution at these sites.58-60
Aerosols and trace gases that absorb UV radiation efficiently may provide protection to the
ecosystem from UV radiation. On the contrary, aerosols that scatter UV radiation redistribute
the incoming direct radiation to diffuse radiation, and therefore have little effect on the UV
dose received at the surface. In the presence of such scattering aerosols, the total exposure to
UV radiation is increased in locations shaded from direct sunlight. Moreover, changes in the
distribution of surface radiation have important effects on the penetration of UV-B radiation
into tree canopies (see Chapter 3) and aquatic environments (see Chapter 4).
UV irradiance variations can be affected by ozone changes caused by weather patterns. At
middle latitudes, ozone variations, at time scales of 1-3 days, depend primarily on the scales
of atmospheric motions related to weather systems, while ozone sources and sinks play a minor role. Several examples have been reported where dynamical mechanisms have led to the
formation of short-lived episodes of extreme total ozone values.61, 62
Limitations in modelling UV radiation
The great complexity and heterogeneity of cloud structure cause difficulties for their accurate
parameterization, despite the progress that has been recently achieved (e.g., 34, 63). Similarly,
the effects from topography, surface albedo for snow- or ice-covered terrains, have also been
investigated. However, accurate representation of the actual radiation field is very difficult,
requiring three-dimensional RT modelling, which is expensive and time consuming. Most
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
RT models do not yet account for polarization effects, which can be important for estimating
the UV radiation, especially in unpolluted conditions.
Influences on satellite-derived UV radiation of aerosols and trace gases in the lower troposphere are well understood, but the implementation of procedures for eliminating these effects depends on the availability and spatial extent of additional information gathered near the
surface (e.g., aerosol optical properties from measurements or from climatology).48, 49 Information on aerosol optical properties is available at only a few sites and is derived either directly from measurements or indirectly with the aid of radiation measurements and model
calculations. There is usually no information available about aerosol extinctions in the UV-B
region. Tropospheric NO2 may also affect satellite UV retrievals and retrieval of aerosol
properties from ground-based radiation measurements.64, 65 The variability of aerosol optical
parameters (e.g., the single scattering albedo and phase function of the aerosols) with altitude,
which are important in RT modelling, is known only from in situ measurements that are generally rare. New methodologies are required to derive these parameters at different altitudes
by remote sensing techniques (e.g., 45).
Air pollutants are generally efficient absorbers of UV radiation. Because they are extremely
variable in time and space, their influence on the UV radiation received at the surface is important for determining the exposure of the biosphere in urban areas. Of particular importance is the role of tropospheric ozone which may increase as a consequence of stratospheric
ozone reduction, which leads to increased photochemical production in the troposphere (the
so called “self-healing” effect).60
The global distribution of UV radiation
UV data are available from satellite-borne sensors such as the new Ozone Monitoring Instrument (OMI) on NASA’s Aura satellite, which supersedes the older Total Ozone Mapping
Spectrometers (i.e., the TOMS instruments).66 The retrievals of UV irradiances are from
model calculations using derived ozone and cloud reflectances. Sample maps are shown in
Figure 1-3, which show a strong peak in UV daily doses at the sub-solar latitudes, near 20ºN
in June and near 20ºS in December. This is expected because solar elevation is a strong determinant of UV, and because ozone amounts are generally smaller in the tropics. Outside
the tropics, the daily doses of UV radiation decrease markedly as one moves towards the
poles, and there are large seasonal variations at mid to high latitudes. Although ozone depletion is most severe in Antarctica, the UV doses there are not particularly high during December (though still elevated substantially compared with the Arctic in June). However, in late
spring, the peak UV irradiance, as well as the daily doses, can exceed even the peaks of the
corresponding values observed at mid-latitudes. For example, in the spring of 1998, the daily
doses of erythemally weighted UV irradiance measured by the National Science Foundation
(NSF) network of spectrometers at several Antarctic stations, including the South Pole
(where there are 24 hours of daylight in summer), greatly exceeded those that occurred in the
summer at San Diego (see chapter 5 from10). The highest daily UV doses (and peak irradiance) occur in the tropics, and at high altitude sites, particularly when snow is present.
Recent ground-based measurements have confirmed that, in rural locations, the peak erythemally-weighted UV irradiance (or UVI values, where UVI = 40 x UVEry in Wm-2)2, 22 are
typically 40% greater in the southern hemisphere than at the corresponding latitude in the
northern hemisphere.67 Similar differences are also apparent in the mean summer UV irradiance from spectrometers. Such marked differences are not seen in UV data from satellite instruments that utilize backscattered ultraviolet radiation (e.g., TOMS, OMI) because these
sensors do not adequately probe the lowermost regions of the atmosphere where aerosol and
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
cloud extinctions are most important.1 Previous studies have shown that altitudinal gradients
in UV irradiance are largest in the lowest kilometer or two.67, 68, 69
Long-term changes
in UV
Measured changes
The long-term variability of surface UV radiation has been studied
using measurement records and model simulations of past UV irradiance based on proxy
data, which are available
for several decades back
in time. In most cases,
these proxies include
total ozone, shortwave
solar radiation, and
cloudiness. Depending
on the location, sunshine
duration, snow depth,
and aerosols may also be
included, as discussed
below.
Increases in surface UV
irradiance in the 1990s
have been observed
from spectral measurements at a few stations
Figure 1-3. Global distribution of the average cloud corrected erythemal daily
in the northern hemidose (in kJ m-2) for June 2005 (left) and Dec 2005 (right) derived from OMI
sphere. This is evident, measurements. These Surface UV irradiance images were supplied by Aapo
for example, in the upTanskanen of the Meteorological Institute. OMI is a joint effort of KNMI,
dated record of Thessa- NASA, and FMI, and is managed by NIVR/Netherlands. The unshaded (white)
loniki, Greece (up to end areas are those with no UV data coverage.
of 2005),70, 71 at Hohenpeissenberg, Germany72, and at Bilthoven, The Netherlands.73 The continuous increase in
surface UV irradiance, even at longer wavelengths, during the 1990s cannot be explained
only by ozone depletion. It is attributed, in part, to reductions in atmospheric pollution leading to less aerosol extinctions,74 and to decreases in cloudiness.72 The period since the ozone
stabilised at mid-latitudes is too short to reveal unequivocal changes in UV radiation. However, data since the late 1990s from one Southern Hemisphere site, where ozone does appear
to have increased, indicate that surface UV radiation may be decreasing (see Figure 1-4).75, 76
Note however that, in these data, there is an unexplained decrease around the turn of the century, which exaggerates the decreases in UVI since that time. At higher latitude southern
hemisphere sites, the natural variability is generally much larger, masking any trends in
UV.77, 78
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Figure 1-4. Long term changes in summertime
ozone (upper panel) and in peak summertime UVI
(lower panel) at Lauder, New Zealand. The symbols show the average ozone and corresponding
noontime UV Index for the 5 highest UVI days in
December, January and February of each summer
derived from UV spectral irradiance measurements. The lines represent the average summertime ozone from satellite-derived ozone, and the
corresponding UVI calculated from those ozone
values.
Examples of long-term changes in UV irradiance from
high quality spectrometers are illustrated in Figure 15. The summertime UV irradiance generally increased
over the observation period, but in some cases, especially in the Southern Hemisphere, there have been
decreases in recent years. The larger gradient at
Lauder can, in part, be attributed to the lower sampling frequency prior to 1994, when observations were
made only during fair weather. Further, in the period
between 1994 and September 1998, no data were
Figure 1-5. Long-term changes in UV Intaken during wet weather.
Long-term measurements of UV radiation with broadband radiometers were reported for Moscow, Russia
(1968-2003)53 and for Norrköping, Sweden (19832003),79 which show an overall increase towards the
late 1990s. Some of this increase is due to ozone reductions. However, decreases in aerosol optical thickness and effective cloud amount during this period80, 81
have also occurred, and have led to increases in irradiance at longer wavelengths which are unaffected by
ozone.79
8
dex averaged over the three summer
months for all weather conditions within
±1 hour around local noon measured at 11
sites distributed worldwide. Linear regressions on the data (straight lines) were used
to estimate the corresponding linear trends.
This figure was prepared using updated
series of published UV datasets. The significance level (** for 99%, and * for 95%)
was calculated from the data variability
only, neglecting the uncertainties in the
measurements. Note that periods for the
trends differ from site to site. Adapted
from5
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Reconstructed time series of UV irradiance, extending several decades back from the start of
the ozone depletion, are now available.40, 73, 82, 83 For example, a method for estimating daily
erythemal UV doses using total ozone, sunshine duration, and snow depth has been developed and applied at Sodankylä, Finland for the period 1950–1999.84 The longest reconstructed time series of UV irradiance to date is from Davos, Switzerland, starting in 1920s
when ozone measurements first became available.85 This series demonstrates fluctuations in
surface erythemal dose of similar magnitude to those observed since the late 1970s when the
problem of human-induced ozone depletion began, and satellite derived ozone data became
available (see Figure 1-6).
The changes deduced from
reconstructed historical UV
irradiance records, and
from direct observations in
recent decades, reflect
those expected from
changes in ozone and atmospheric transmission
(since ozone changes are an
input to the retrieval).
Measurements of UV irradiance at various locations over northern midlatitudes show that surface
UV irradiance has increased in the 1980s and
1990s as a consequence of
ozone depletion and increasing atmospheric
Figure 1-6. (Upper panel) Time series of reconstructed erythemal irradiance
transmission.53, 58, 71, 73, 84-86 over Switzerland shown as deviation from the 1940-1969 mean. (Lower
duration and snow depth
Radiative transfer calcula- panel) Percentage contribution of ozone, sunshine
to the variability in UV irradiance. From 85.
tions have also been used to
determine past UV irradiance from routine observations of total ozone, aerosol, albedo, and
clouds at two locations in Central Europe, Würzburg, and Hohenpeissenberg.87 The results
show that, at these sites, UV-B radiation has increased over the period 1968 to 2000. Because there were supporting data records for cloud cover, aerosol and albedo in this study, the
increase in UV-B irradiance could clearly be associated with a reduction in stratospheric
ozone. Depending on the action spectra for specific effects, increases in the annual UV exposure are ~ +2 % to +5 % per decade. Regional differences have been found in the influence
of clouds on UV radiation. For example, the UV-B irradiance increase due to ozone reduction is enhanced by clouds by about 1% per decade for Hohenpeissenberg and reduced by
nearly the same amount for Würzburg.
From the above discussion it appears that UV radiation at the surface has been changing in
the last three decades at rates (and even signs) which vary over time and between sites. The
changes have been attributed in part to decreases in total ozone column, but other factors such
as changes in clouds and aerosol are also important. Since the beginning of the 1990s, there
have been indications that atmospheric transmission in the northern hemisphere has been increasing following reductions in cloudiness88 and aerosols86 which would have amplified
any increases in UV irradiance attributable to ozone depletion.
The Environmental Effects Assessment Panel Report for 2006
9
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Possible changes that precede the instrumented record
To assess more fully the present changes in ozone and UV-B radiation and their effects, it is
desirable to gain knowledge about their historical long-term, non-anthropogenic changes.
For example, it has been speculated that ozone depletion has been one of the factors contributing to large extinctions of organisms, such as that which took place 251 million years
ago.89, 90
There have been speculations that damage to the ozone layer may have occurred 65 Myr ago,
as a result of widespread combustion of biomass following a large meteoritic impact.91 These
authors estimate that the concentrations of organic chlorine and bromine may have been an
order of magnitude greater than at present, resulting in ozone loss and increased UV radiation
which could have damaged life on Earth. However, there is no proof that this contributed to
any biospheric extinctions.
To assess possible changes, biological proxies for UV-B radiation have been considered using lake sediments92, 93 (see Chapter 4). Analyses of plant pigments94 have had limited success so far. It has been suggested that changes in UV-B radiation due to ozone depletion may
have been responsible for a departure in the relationship between tree rings and temperature
over the period since the 1970s.95. However, the changing behaviour seems to precede the
period of most significant ozone depletion, and may be due to other factors. One possible
factor is the decreasing irradiance due to increasing cloud and aerosols that occurred over this
period, sometimes called “global dimming”,88 a trend which may have reversed to a “global
brightening” since the late 1980s.86 Further work on biological proxies for past UV-B radiation is currently being conducted by several groups, and reliable results may eventually be
produced. Promising attempts include the chemical composition and structure of pollen
grains and spores.96, 97
The UV-B irradiance depends not only on the ozone layer and other atmospheric properties
(clouds, aerosol), but also on the variable emission of the sun98 and the variable geometry of
the solar system.99 Although several proxies for past solar emission exist, and though modelling and comparison with other stars can provide further information, the uncertainties remain
great, and published values must be used with caution.
In a very long-term perspective,100 calculations based on the oxygen content of the atmosphere101 can give some information about the historical development of the ozone layer, as
can measurements of the isotope composition of certain minerals (reviewed by Rumble102).
In turn, these provide information about past UV radiation. Quantitative information about
the ozone layer in the early 20th century can be obtained from the study of historic spectrographic plates used in astronomical studies.103 This offers the promise of more accurate estimation of UV radiation prior to the 1920s at a few sites.
Interactions between ozone depletion, UV radiation, and climate change
Interactions between ozone depletion and climate change have recently been assessed and
summarized in the IPCC/TEAP report.25 Further details regarding these interactions are
given in Chapter 1 of the full IPCC Report.104 A recent review has also been undertaken by
the WMO.105
These interactions can be complex, and they can act either way, with ozone depletion impacting on climate change, or with climate change impacting on ozone depletion. The interactions can involve chemistry, radiation, and dynamics, as well as feedbacks between those
three processes. Examples of climate change affecting ozone through dynamical feedbacks
have been discussed already (see section on ozone changes). Some of these feedbacks are
10
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
summarised in Figure 1-7. See Chapter 5 for further details on interactions that involve biogeochemical feedbacks.
Figure 1-7. Update of ozone/climate feedback linkages. From 106.
Impacts of climate change on ozone depletion
Impacts of climate change on ozone depletion have been further explored, but there is not yet
a consensus on whether the overall effect will be to delay or accelerate ozone recovery.
Some processes would result in slowing of ozone recovery,6, 107 while others would result in
an acceleration.108 Ozone-depleted air exported from polar latitudes comprises a significant
portion of ozone losses at mid-latitudes7-9. This has negative implications for future ozone
recovery at mid-latitudes: since further cooling of the polar stratosphere is expected as a consequence of global climate change, the cooling will be conducive to further rapid loss of
ozone.
Changes in atmospheric circulation (dynamics) seem increasingly important for ozone variability.109-112 For example, strong links have been found between stratosphere/troposphere
exchange and the El Nino Southern-Oscillation (ENSO) climate pattern.112 Model simulations show that much of the ozone increase seen in recent years at mid-northern latitudes can
be explained by changes in dynamics, rather than being caused solely by reductions in atmospheric chlorine and bromine.23 This has important implications for our confidence about
future ozone recovery.
Ozone heats the stratosphere by absorbing incoming solar energy and outgoing infrared radiation from the Earth’s surface. A significant component of the observed stratospheric cooling
(-0.17 °C/decade) can be attributed to ozone depletion, rather than being solely a radiative
effect of climate change.113 Therefore, if ozone amounts were to increase in the future, this
The Environmental Effects Assessment Panel Report for 2006
11
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
would tend to warm the stratosphere, diminishing the future cooling there due to increasing
greenhouse gases (GHG). The warming effect would aid further recovery of the ozone layer
in polar regions where heterogeneous chemistry on ice crystals dominates the ozone loss
processes, but would have the opposite effect in other regions where gas-phase chemistry
dominates. Consequently, the future impact of climate change may aid ozone recovery at
mid-latitudes.
An analysis of four decades of ozone sonde data in Antarctica concluded that, while ozone
depletion has been less severe in recent years, this cannot be necessarily linked to any recovery attributable to reductions in chlorine.114 That result supported an earlier study,115 which
demonstrated that reduced Antarctic ozone loss during 2001 to 2004 is a consequence of
warmer springtime temperatures at altitudes between 20 and 22 km in recent years.
Recent model calculations that include climate feedbacks suggest that, because of these interactions, ozone is expected to return to pre-1980 levels somewhat later in polar regions than at
mid-latitudes. However, the observational evidence available so far suggests that these interactions have not yet introduced large delays in ozone recovery (e.g., see Figure 1-1 and 1-2).
As discussed above, there is evidence that ozone has already started to recover at mid latitudes. In recent years, springtime ozone losses in Antarctica have generally been less severe,* but this has been attributed to increased temperatures in the lower stratosphere, which
in turn may be attributed to changes in circulation patterns that have resulted from global
warming.114 In contrast, in the absence of changes in circulation patterns, climate change is
expected to cause lower temperatures in the Arctic stratosphere, which will, in turn, lead to a
greater probability of rapid ozone depletion on the surfaces of ice crystals.
The effects of climate change on ozone depletion may be most pronounced - yet least understood - at high latitudes,116 where springtime ozone losses are expected to continue.117 In
polar regions especially, interactions with global warming complicate the recovery. Increases
in water vapour and cooling of the stratosphere will be more important than elsewhere. Further, we have less confidence in the performance of models in this region, which tend to
overestimate ozone concentrations and underestimate the ozone loss. The ozone loss depends
critically on temperature. In polar regions, changes in climate (surface temperature) can trigger changes in circulation which affect ozone. Conversely, changes in ozone lead to changes
in stratospheric temperature, which, in turn, may lead to changes in circulation which can
trigger changes in climate.
Finally, one cannot simply assume that effects of climate change on ozone and UV radiation
will continue at the present rate. According to recent assessments of climate change,118 the
average rate of surface temperature change over the 21st century is likely to be about 5 times
that in the past century. Consequently, unless strong mitigation measures are undertaken
with respect to climate change, profound effects on the ecosystem and on the solar UV radiation received at the Earth’s surface could be anticipated.
* The WMO reported that in 2006 the ozone depletion in Antarctica has been one of the most
severe on record, with respect to the mass deficit of ozone. See Antarctic Ozone Bulletin
2006, No 4 at http://www.wmo.ch/web/arep/ozone.html
12
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Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Impacts of ozone depletion on climate change
Changes in ozone and UV radiation can potentially influence climate through impacts on tropospheric photochemistry, as discussed in Chapter 6. Observational data and a new modelling study have both suggested that decreases in stratospheric ozone in Antarctica have led to
climatic changes both in the stratosphere and at the Earth’s surface. These changes in ozone
have led to increased westerly winds at latitudes 50 to 60ºS. This, in turn, has resulted in a
surface cooling in Antarctica and a warming at high latitudes outside the Antarctic continent.119
Changes in atmospheric temperatures lead to important changes in modes of atmospheric circulation, in particular the North Atlantic Oscillation (NAO) and the Arctic Oscillation (AO).
These are responsible for large scale redistributions of atmospheric mass, which produce
large scale variability in NH dynamics, and have a profound effect on winter climate variability around the Atlantic basin. Temperature increases in the troposphere as well as temperature decreases in the stratosphere both contribute to these changes.110, 111 A potentially important impact of changing ozone on climate has been proposed recently to explain the
strengthening of the NAO in recent decades.120 This strengthening has altered the surface
climate in these regions at a rate far in excess of global mean warming. Although weak NAO
trends are reproduced in climate simulations of the 20th century, the unexplained strengthening of the NAO was fully simulated in a climate model by imposing observed ozone trends in
the lower stratosphere. This implies that stratospheric variability needs to be reproduced in
models to fully simulate surface climate variations in the North Atlantic sector.
As discussed further in Chapter 5, climate change can also be mediated through UV-induced
changes121 in dimethyl sulphide (DMS), a substance emitted from oceanic phytoplankton
that can modify the reflectivity of the atmosphere.
Other factors that may affect ozone depletion and climate change
As discussed previously, volcanic eruptions, and long-term periodic variations in planetary
motions can directly affect UV radiation, ozone, and climate. Changes in solar activity may
also be important. Solar UV radiation arriving outside the Earth’s atmosphere follows an 11year cycle. Counter-intuitively, when the solar activity is highest, UV-B radiation at the surface has a minimum due to the increased production of ozone. Recent studies have demonstrated that the changes in solar UV radiation can also induce changes in some modes of atmospheric dynamics (e.g., the Southern Annular Mode (SAM), and the AO).122, 123 Interactions with solar activity may also be more important for ozone depletion and UV irradiance
increases than previously thought.71, 122, 124-129
Recent modelling studies have shown larger effects of increased CFCs, HCFCs and other
halocarbons (and their effects on ozone) on tropical tropopause temperatures than had previously been calculated.130 These temperatures are critical because they control the amount of
water vapour entering the stratosphere, which in turn is converted to OH which then destroys
ozone through catalytic cycles. The model indicates that the halocarbons have led to temperature increases in that region of about 0.4ºC over the last 50 years, which exceeds the
cooling effect from the major GHGs. The fact that this region has actually cooled implies
that other factors that are not included in the model must also be important. These could include increases in cirrus cloud, increases in water vapour (both of which have been observed), or increases in the strength of the mean atmospheric circulation. The model also
shows that the indirect effect of ozone depletion in the stratosphere at mid to high latitudes
has offset approximately half of the global surface warming to date. Consequently a slightly
faster rate of surface warming is predicted in the future as ozone recovers.
The Environmental Effects Assessment Panel Report for 2006
13
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Interactions between different regions of the stratosphere may also be important. Even in the
event of a complete recovery in chlorine, ozone in the lower tropical stratosphere will not recover before ~2050, because of a reduction in UV irradiance due to more-rapidly increasing
ozone at higher altitudes131. This can be thought of as a reverse example of the well-known
“self-healing” effect for ozone, whereby ozone losses at high altitudes are partially compensated by ozone production from increased UV irradiance at lower altitudes. In some cases it
is not obvious whether changes in ozone are driving changes in dynamics, or whether
changes in dynamics are causing changes in ozone.112
Although there is speculation about the effects of climate change introducing lags to ozone
recovery, the observational data so far suggests that global ozone may, in fact, be increasing
faster than expected, given the estimated rate of decrease of Equivalent Effective Stratospheric Chlorine (EESC).5
Future changes in methyl bromide and methyl chloride emissions resulting from climate
change may also be important. Methyl bromide constitutes the largest source of bromine atoms entering the stratosphere and therefore plays an important role in the depletion of stratospheric ozone,132 and thus on UV radiation. The major source of methyl bromide is natural,
but a significant fraction (about 20%, and reducing) is man made.5 Methyl bromide emissions from rice paddies will increase appreciably with global warming,133 (see Chapter 5).
Future expectations
The future pathway for UV radiation is uncertain because the pathway for ozone recovery is
uncertain. As reported in recent assessments,5, 25 there are wide variations between models
that predict future ozone, and there are large discrepancies between past measurements, and
model simulations of the past (see Figure 1-8).
A recent study of trends in total
column ozone from several models
and from satellite observations
from the period 1979-2003 found
large discrepancies between the
models and measurements.134 The
observed positive trends in both
hemispheres in the recent 7-year
period are much larger than predicted by the models. Most models
underestimate the past trends at
mid- and high latitudes. Quantitatively, there is much disagreement
among the models concerning future trends. However, the models
Figure 1-8. The future outlook for ozone recovery is uncertain.
agree that future ozone trends are
Observed and modelled column ozone amounts (60ºS–60ºN) as
expected to be positive and less
25
than half the magnitude of the past percent deviations from the1980 values. From .
downward trends.
Substantial research efforts in the 1980s and 1990s have advanced our knowledge about solar
UV radiation and its interactions with the atmosphere and biosphere. In recent years, there
have been significant improvements in instrumentation technology and radiative transfer
modelling which have helped our understanding of the various processes relevant to UV radiation. There are still areas where further development is needed.
14
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
Important effects on UV radiation may be expected from long-term changes in ozone, clouds,
and aerosols. According to the predictions of climate models, column ozone is expected to
increase during the next decades. The response of surface UV radiation solely due to changes
in ozone can be estimated from RT model calculations. Such estimates are shown in Figure
1-9, where any direct or indirect effects from clouds and aerosols are neglected. The ozone
losses calculated by this model are larger than observed, especially in the Southern Hemisphere. Therefore, the corresponding increases in the calculated UV irradiance are overestimated. At mid-latitudes surface UV irradiance is predicted to peak between about 2000 and
2010 and is expected to return to the pre-1980 levels between 2040 and 2070, but the these
phases occur later at the southern high latitudes. Figure 1-9 also shows that the predicted
changes in UV irradiance are significantly larger in the southern hemisphere than in the
northern hemisphere.
Despite the great progress
that has been made in the last
decade in understanding the
relations and interactions of
surface UV radiation with
atmospheric composition and
structure, there are still areas
where scientific research is
not sufficiently advanced.
There is lack of widespread
observational evidence, especially in the tropics and in
urban environments, to quantify the influence of tropospheric ozone, aerosols, and
other pollutants on surface
UV radiation. Knowledge of
interactions between climate
change and UV radiation will
improve as more modelling
studies and observational
evidence become available.
Figure 1-9. Estimated changes in erythemally weighted surface UV irradiance at local noon in response to projected changes in total column
ozone for the period 1970-2099, using zonal-averages in total ozone in the
latitude bands 35°N-60°N, 35°S-60°S, and 60°S-90°S, and the solar zenith angle corresponding to 45°N in July, 45°S in January and 65°S in
October respectively. At each latitude, the irradiance is expressed as the
ratio to the 1970-1980 average. The results have been smoothed with a 5
year running mean filter to remove some of the year to year variability in
the ozone predictions in the model. From 5
References
1
2
3
4
UNEP, Environmental effects of ozone depletion and its interactions with climate
change: 2003 progress report, United Nations Environment Programme (UNEP), Nairobi, 2003.
McKenzie RL, Björn LO, Bais A, Ilyas M, Changes in biologically active ultraviolet
radiation reaching the Earth's surface, Photochemical & Photobiological Sciences, 2003,
2, 5-15.
McKinlay AF, Diffey BL, A reference action spectrum for ultra-violet induced erythema
in human skin, in Human Exposure to Ultraviolet Radiation: Risks and Regulations
eds.: Passchier WF, Bosnajakovic BFM, Elsevier, Amsterdam, 1987, pp. 83-87.
UNEP, Environmental effects of ozone depletion: 1998 assessment, UNEP, Nairobi,
1998.
The Environmental Effects Assessment Panel Report for 2006
15
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
16
WMO, Scientific Assessment of Ozone Depletion: 2006, World Meteorological Organisation Report No. ISBN 92-807-2261-1, Geneva.
HTTP:\\www.WMP\ldr_groups\Publications\WMO_Scientific-Assess_2002.pdf
Rex M, Salawitch RJ, von der Gathen P, Harris NRP, Chipperfield MP, Naujokat B,
Arctic ozone loss and climate change, Geophys Res Lett, 2004, 31,
DOI:10.1029/2003GL018844.
Lee AM, Jones RL, Kilbane-Dawe I, Pyle JA, Diagnosing ozone loss in the extratropical
lower stratosphere, J. Geophys. Res., 2002, 107, 10.1029/2001JD000538.
Ajtic J, Connor BJ, Randall CE, Lawrence BN, Bodeker GE, Heuff DN, Antarctic air
over New Zealand following vortex breakdown in 1998., Ann. Geophys., 2003, 21,
2175-2183.
Hadjinicolaou P, Pyle J, The impact of Arctic ozone depletion on northern middle latitudes: Interannual variability and dynamical control, J Atmos Chem, 2004, 47, 25-43.
WMO, Scientific Assessment of Ozone Depletion: 2002, World Meteorological Organisation Report No., Geneva, p. 498
Newchurch MJ, Yang E-S, Cunnold DM, Reinsel GC, Zawodny JM, Russell JM, III,
Evidence for slowdown in stratospheric ozone loss: First stage of ozone recovery, J.
Geophys. Res., 2003, 108, 4507 4510.1029/2003JD003471.
Newchurch MJ, Yang E-S, Cunnold DM, Reinsel GC, Salawitch RJ, Zawodny JM, Russell JM, III, McCormick MP, First stage of stratospheric ozone recovery, in XX Quadrennial Ozone Symposium, Vol. 1 (Ed.: Zerefos CS), International Ozone Commission,
Kos, 2004, pp. 27-28.
Weatherhead EC, Reinsel GC, Tiao GC, Jackman CH, Bishop L, Frith SMH, DeLuisi J,
Keller T, Oltmans SJ, Fleming EL, Wuebbles DJ, Kerr JB, Miller AJ, Herman J,
McPeters R, Nagatani RM, Frederick JE, Detecting the recovery of total column ozone,
J. Geophys. Res., 2000, 105, 22201-22210.
Reinsel GC, Weatherhead E, Tiao GC, Miller AJ, Nagatani RM, Wuebbles DJ, Flynn
LE, On detection of turnaround and recovery in trend for ozone, J. Geophys. Res., 2002,
107, 10.1029/2001JD000500.
Bhartia PK, McPeters R, Stolarski R, Flynn LE, Wellemeyer CG, A Quarter Century of
Ozone Observations by SBUV and TOMS, in XX Quadrennial Ozone Symposium, Vol.
1 (Ed.: Zerefos CS), International Ozone Commission, Kos, 2004, pp. 89-90.
Solomon S, The hole truth: What’s news (and what’s not) about the ozone hole, Nature,
2004, 427, 289-290.
Weatherhead EC, Anderson SB, The search for signs of recovery of the ozone layer, Nature, 2006, 441, 39-45.
Brönnimann S, Staehelin J, Farmer SFG, Cain JC, Svendby T, Svenoe T, Total ozone
observations prior to the IGY. I: A history, Q J Roy Meteor Soc, 2003, 129, 2797-2817.
Brönnimann S, Luterbacher J, Staehelin J, Svendby TM, An extreme anomaly in stratospheric ozone over Europe in 1940-1942, Geophys Res Lett, 2004, 31,
DOI:10.1029/2004GL019611.
Dameris M, Matthes S, Deckert R, Grewe V, Ponater M, Solar cycle effect delays onset
of ozone recovery, Geophys Res Lett, 2006, 33, DOI:10.1029/2005GL024741.
Reinsel GC, Miller AJ, Weatherhead EC, Flynn LE, Nagatani RM, Tiao GC, Wuebbles
DJ, Trend analysis of total ozone data for turnaround and dynamical contributions, J.
Geophys. Res., 2005, 110, DOI:10.1029/2004JD004662.
UNEP, Environmental effects of ozone depletion and its interactions with climate
change: 2002 assessment, Photochem. Photobiol. Sci., 2003, 2, 1-72.
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
Hadjinicolaou P, Pyle JA, Harris NRP, The recent turnaround in stratospheric ozone
over northern middle latitudes: A dynamical modeling perspective, Geophys Res Lett,
2005, 32, DOI:10.1029/2005GL022476.
Yang E-S, Cunnold D, Salawitch R, McCormick P, Russell III JM, Zawodny J, Oltmans
S, Newchurch MJ, Attribution of recovery in lower-stratospheric ozone, J. Geophys.
Res, 2006, 111, DOI:10.1029/2005JD006371.
IPCC, IPCC/TEAP Special report: Safeguarding the ozone layer and the global climate
system: Issues related to hydrofluorocarbons and perflorocarbons. Summary for policymakers, IPCC, Geneva, 2005.
Calbo J, Pages D, Gonzalez J, Empirical studies of cloud effects on UV radiation: A review, Rev. Geophys., 2005, 43.
Glandorf M, Arola A, Bais A, Seckmeyer G, Possibilities to detect trends in spectral UV
irradiance, Theotet. Appl. Climatol., 2005, 81, 33-44.
Cede A, Blumthaler M, Luccini E, Piacentini RD, Nunez L, Effects of clouds on erythemal and total irradiance as derived from data of the Argentine Network, Geophys Res
Lett, 2002, 29, 2223, DOI:10.1029/2002GL015708.
Crawford J, Shetter RE, Lefer B, Cantrell C, Junkermann W, Madronich S, Calvert J,
Cloud impacts on UV spectral actinic flux observed during the International Photolysis
Frequency Measurement and Model Intercomparison (IPMMI), J. Geophys. Res., 2003,
108, 8545, DOI:10.1029/2002JD002731.
Pfister G, McKenzie RL, Liley JB, Thomas A, Forgan BW, Long CN, Cloud coverage
based on all-sky imaging and its impact on surface solar irradiance, J. Appl. Meteorol.,
2003, 42, 1421-1434.
Piacentini RD, Cede A, Barcena H, Extreme solar total and UV irradiances due to cloud
effect measured near the summer solstice at the high-altitude desertic plateau Puna of
Atacama (Argentina), J Atmos Sol-Terr Phy, 2003, 65, 727-731.
Lovengreen C, Fuenzalida, A. H, Videla L, On the spectral dependency of UV radiation
enhancements due to clouds in Valdivia, Chile (39.8°S), J. Geophys. Res., 2005, 110,
DOI:10.1029/2004JD005372.
Sabburg JM, Parisi AV, Spectral dependency of cloud enhanced UV irradiance, Atmos.
Res., 2006, in press.
Kylling A, Webb AR, Kift R, Gobbi GP, Ammannato L, Barnaba F, Bais A, Kazadzis S,
Wendisch M, Jakel E, Schmidt S, Kniffka A, Thiel S, Junkermann W, Blumthaler M,
Silbernagl R, Schallhart B, Schmitt R, Kjeldstad B, Thorseth TM, Scheirer R, Mayer B,
Spectral actinic flux in the lower troposphere: measurement and 1-D simulations for
cloudless, broken cloud and overcast situations, Atmos. Chem. Phys., 2005, 5, 19751997.
Mayer B, Fischer CA, Madronich S, Estimation of surface actinic flux from satellite
(TOMS) ozone and reflectivity measurements, Geophys Res Lett, 1998, 25, 4321-4324.
Ahmad Z, Bhartia PK, Krotkov N, Spectral properties of backscattered UV radiation in
cloudy atmospheres, J. Geophys. Res., 2004, 109, D01201,
DOI:10.1029/2003JD003395.
Winiecki S, and J. E. Frederick, Ultraviolet radiation and clouds: Couplings to tropospheric air quality, J. Geophys. Res., 2005, 110, D22202, DOI:10.1029/2005JD006199.
Wuttke S, Seckmeyer G, Spectral Radiance and Sky Luminance in Antarctica: A Case
Study, Theotet. Appl. Climatol., 2005.
Balis DS, Amiridis V, Zerefos C, Kazantzidis A, Kazadzis S, Bais AF, Meleti C, Gerasopoulos E, Papayannis A, Matthias V, Dier H, Andreae MO, Study of the effect of different type of aerosols on UV-B radiation from measurements during EARLINET, Atmos. Chem. Phys., 2004, 4, 307-321.
The Environmental Effects Assessment Panel Report for 2006
17
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
18
Chubarova NE, Influence of aerosol and atmospheric gases on ultraviolet radiation in
different optical conditions including smoky mist of 2002, Doklady Earth Sciences,
2004, 394, 62–67.
Chubarova NE, Role of tropospheric gases in the absorption of UV radiation, Doklady
Earth Sciences, 2006, 407, 294–297.
Petters JL, Saxena VK, Slusser JR, Wenny BN, Madronich S, Aerosol single scattering
albedo retrieved from measurements of surface UV irradiance and a radiative transfer
model, J. Geophys. Res., 2003, 108, DOI:10.1029/2002JD002360.
Arola A, Koskela T, On the sources of bias in aerosol optical depth retrieval in the UV
range, J. Geophys. Res., 2004, 109, DOI:10.1029/2003JD004375.
Bergstrom RW, Pilewskie P, Pommier J, Rabbette M, Russell PB, Schmid B, Redemann
J, Higurashi A, Nakajima T, Quinn PK, Spectral absorption of solar radiation by aerosols during ACE-Asia, J. Geophys. Res., 2004, 109, DOI:10.1029/2003JD004467.
Bais AF, Kazantzidis A, Kazadzis S, Balis DS, Zerefos CS, Meleti C, Deriving an effective aerosol single scattering albedo from spectral surface UV irradiance measurements,
Atmos. Environ., 2005, 39, 1093-1102.
Goering CD, L'Ecuyer TS, Stephens GL, Slusser JR, Scott G, Davis J, Barnard JC, Madronich S, Simultaneous retrievals of column ozone and aerosol optical properties from
direct and diffuse solar irradiance measurements, J. Geophys. Res., 2005, 110,
DOI:10.1029/2004JD005330.
Krotkov NA, Bhartia PK, Herman JR, Slusser JR, Labow GJ, Scott GR, Janson GT, Eck
T, Holben BN, Aerosol ultraviolet absorption experiment (2002 to 2004), part 1: ultraviolet multifilter rotating shadowband radiometer calibration and intercomparison with
CIMEL sunphotometers, Optic. Eng., 2005, 44, 0410051-1, 041005-17.
Krotkov NA, Bhartia PK, Herman JR, Slusser JR, Scott GR, Labow GJ, Vasilkov AP,
Eck T, Doubovik O, Holben BN, Aerosol ultraviolet absorption experiment (2002 to
2004), part 2: absorption optical thickness, refractive index, and single scattering albedo,
Optic. Eng., 2005, 44, 041006-01, 041006-17.
Arola A, Kazadzis S, Krotkov N, Bais A, Gröbner J, Herman JR, Assessment of TOMS
UV bias due to absorbing aerosols, J. Geophys. Res., 2005, 110, D23211,
DOI:10.1029/2005JD005913.
Meloni D, di Sarra A, Herman JR, Monteleone F, Piacentino S, Comparison of groundbased and Total Ozone Mapping Spectrometer erythemal UV doses at the island of
Lampedusa in the period 1998-2003: Role of tropospheric aerosols, J. Geophys. Res.,
2005, 110, DOI:10.1029/2004JD005283.
Cede A, Luccini E, Nunez L, Piacentini RD, Blumthaler M, Herman J, TOMS-derived
erythemal irradiance versus measurements at the stations of the Argentine UV Monitoring Network, J. Geophys. Res., 2004, 109, D08109 10.1029/2004JD004519.
Koronakis PS, Sfantos GK, Paliatsos AG, Kaldellis JK, Garofalakis JE, Koronaki IP,
Interrelations of UV-global/global/diffuse solar irradiance components and UV-global
attenuation on air pollution episode days in Athens, Greece, Atmos. Environ., 2002, 36,
3173-3181.
Chubarova NY, Nezval YI, Verdebout J, Krotkov N, Herman J, Long-term UV irradiance changes over Moscow and comparisons with UV estimates from TOMS and METEOSAT, in Ultraviolet Ground- and Space-based Measurements, Models, and Effects
V, Vol. 5886 eds.: Bernhard G, Slusser JR, Herman JR, Gao W, SPIE, San Diego, 2005,
pp. 63-73.
Barnard WF, Saxena VK, Carolina N, Wenny BN, DeLuisi JJ, Daily surface UV exposure and Its relationship to surface pollutant measurements, J. Air & Waste Manage.
Assoc., 2003, 53, 237–245.
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56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
Fromm M, R. Bevilacqua, Servranckx R, Rosen J, Thayer JP, Herman J, Larko D, Pyrocumulonimbus injection of smoke to the stratosphere: Observations and impact of a super blowup in northwestern Canada on 3-4 August 1998, J. Geophys. Res., 2005, 110,
DOI: 10.1029/2004JD005350.
Zerefos C, Balis D, Tzortziou M, Bais A, Tourpali K, C. Meleti, Bernhard G, J. Herman,
A note on the interannual variations of UV-B erythemal doses and solar irradiance from
ground-based and satellite observations, Ann. Geophys., 2001, 19, 115-120.
Zerefos CS, Long-term ozone and UV variations at Thessaloniki, Greece, Phys. Chem.
Earth, 2002, 27, 455-460.
Cheymol A, De Backer H, Retrieval of the aerosol optical depth in the UV-B at Uccle
from Brewer ozone measurements over a long time period 1984-2002, J. Geophys. Res.,
2003, 108, 4800, DOI:10.1029/2003JD003758.
Arola A, Lakkala K, Bais A, Kaurola J, Meleti C, Taalas P, Factors affecting short and
long term changes of spectral UV irradiance at two European stations, J. Geophys. Res.,
2003, 108, 10.1029/2003JD003447.
Isaksen ISA, Dalsøren SB, Sundet JK, Grini A, Zerefos C, Kourtidis K, Meleti C, Balis
D, Zanis P, Tropospheric ozone changes at unpolluted and semipolluted regions induced
by stratospheric ozone changes, J. Geophys. Res., 2005, 110, 1-15.
Siani AM, Galliani A, Casale GR, An investigation on a low ozone episode at the end of
November 2000 and its effect on ultraviolet radiation, Optic. Eng., 2002, 41, 3082-3089.
Iwao K, Hirooka T, Dynamical quantifications of ozone minihole formation in both
hemispheres, J. Geophys. Res., 2006, 111, DOI:10.1029/2005JD006333.
Mayer B, Madronich S, Actinic flux and photolysis in water droplets: Mie calculations
and geometrical optics limit, Atmos. Chem. Phys., 2004, 4.
Cede A, Herman JR, Richter A, Krotkov NA, Burrows J, Measurements of nitrogen dioxide total column amounts at Goddard Space Flight Center using a Brewer spectrometer in direct sun mode, J. Geophys. Res., 2005, 111, DOI:10.1029/2005JD006585.
Krotkov NA, Herman JR, Cede A, Labow G, Partitioning between aerosol and NO2 absorption in the UV spectral region, in Ultraviolet Ground- and Space-based Measurements, Models, and Effects V, Vol. 1-8 (Eds.: Bernhard G, Slusser JR, Herman JR, Gao
W), SPIE, 2005.
Tanskanen A, Krotkov N, Herman J, Arola A, Surface ultraviolet irradiance from OMI,
IEEE, Transactions on Geoscience and Remote Sensing (Aura special issue), 2006, 44.
McKenzie RL, Bodeker GE, Scott G, Slusser J, Geographical differences in erythemally-weighted UV measured at mid-latitude USDA sites, Photochemical & Photobiological Sciences, 2006, 5, 343 - 352.
Schmucki DA, Philipona R, Ultraviolet radiation in the Alps: the altitude effect, Optic.
Eng., 2002, 41, 3090-5.
Pfeifer MT, Koepke P, Reuder J, Effects of altitude and aerosol on UV radiation, J.
Geophys. Res., 2006, 111, DOI:10.1029/2005JD006444.
Zerefos CS, Meleti C, Balis DS, Bais AF, Gillotay D, On changes of spectral UV-B in
the 90's in Europe, Adv Space Res, 2001, 26, 1971-1978.
Garane K, Bais AF, Tourpali K, Meleti C, Zerefos CS, Kazadzis S, Variability of spectral UV irradiance at Thessaloniki, Greece, from 15 years measurements, in Ultraviolet
Ground- and Space-based Measurements, Models, and Effects V, Vol. 5886 (Eds.: Bernhard G, Slusser JR, Herman JR, Gao W), SPIE, San Diego, USA, 2005.
Trepte S, Winkler P, Reconstruction of erythemal UV irradiance and dose at Hohenpeissenberg (1968-2001) considering trends of total ozone, cloudiness and turbidity, Theotet. Appl. Climatol., 2004, 77 (3-4), 159-171.
The Environmental Effects Assessment Panel Report for 2006
19
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
20
den Outer PN, Slaper H, Tax RB, UV radiation in the Netherlands: Assessing long-term
variability and trends in relation to ozone and clouds, J. Geophys. Res., 2005, 110,
DOI:10.1029/2004JD004824.
Kazadzis S, Bais A, Kouremeti N, Gerasopoulos E, Garane K, Blumthaler M, Schallhart
B, Cede A, Direct spectral measurements with a Brewer spectroradiometer: absolute
calibration and aerosol optical depth retrieval, Appl. Optic., 2005, 44, 1681-1690.
McKenzie RL, Connor BJ, Bodeker GE, Increased summertime UV observed in New
Zealand in response to ozone loss, Science., 1999, 285, 1709-1711.
McKenzie RL, Bodeker GE, Johnston PV, Kotkamp M, Long term changes in summertime UV radiation in New Zealand in response to ozone change, in Proceedings of the
XX Quadrennial Ozone Symposium, Vol. 1 (Ed.: Zerefos CS), International Ozone
Commission, Kos, Greece, 2004, pp. 257-258.
Bernhard G, Booth CR, Ehramjian JC, Version 2 data of the National Science Foundation's Ultraviolet Radiation Monitoring Network: South Pole, J. Geophys. Res., 2004,
109, DOI:10.1029/2004JD004937.
Bernhard G, Booth CR, Ehramjian JC, Nichol SE, UV climatology at McMurdo Station,
Antarctica, based on version 2 data of the National Science Foundation's Ultraviolet Radiation Monitoring Network, J. Geophys. Res., 2006, 111, DOI:10.1029/2005JD005857.
Josefsson W, UV-radiation 1983–2003 measured at Norrköping, Sweden, Theotet. Appl.
Climatol., 2006, 83, 59-76.
Jaroslawski J, Krzyscin JW, Puchalski S, Sobolewski P, On the optical thickness in the
UV range: Analysis of the ground-based data taken at Belsk, Poland, J. Geophys. Res.,
2003, 108, art. no.-4722.
Makhotkina EL, Plakhina IN, Lukin AB, Some features of atmospheric turbidity change
over the Russian territory in the last quarter of the 20th century, Russian Meteorology
and Hydrology (Meteorologiya i Gidrologiya), 2005, 1, 20-27.
Engelsen O, Hansen GH, Svenoe T, Long-term (1936-2003) ultraviolet and photosynthetically active radiation doses at a north Norwegian location in spring on the basis of
total ozone and cloud cover, Geophys Res Lett, 2004, 31, DOI:10.1029/2003GL019241.
Krzyscin JW, Eerme K, Janouch M, Long-term variations of the UV-B radiation over
Central Europe as derived from the reconstructed UV time series, Ann. Geophys., 2004,
22, 1473-1485.
Lindfors AV, Arola A, Kaurola J, Taalas P, Svenoe T, Long-term erythemal UV doses
at Sodankyla estimated using total ozone, sunshine duration, and snow depth, J. Geophys. Res., 2003, 108, DOI:10.1029/2002JD003325.
Lindfors A, Vuilleumier L, Erythemal UV at Davos (Switzerland), 1926-2003, estimated using total ozone, sunshine duration, and snow depth, J. Geophys. Res., 2005,
110, DOI:10.1029/2004JD005231.
Wild M, Gilgen H, Roesch A, Ohmura A, Long CN, Dutton EG, Forgan B, Kallis A,
Russak V, Tsvetkov A, From dimming to brightening: Decadal changes in solar radiation at Earth's surface, Science., 2005, 308, 847-850.
Reuder J, Koepke P, Reconstruction of UV radiation over Southern Germany for the
past decades, Meteorologische Zeitschrift, 2005, 14, 237-246.
Pinker RT, Zhang B, Dutton EG, Do satellites detect trends in surface solar radiation?,
Science., 2005, 308, 850-854.
Foster CB, Afonin SA, Abnormal pollen grains: an outcome of deteriorating atmospheric conditions around the Permian-Triassic boundary, J. Geological Soc. (London),
2005, 162, 653-659.
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
106
107
108
Visscher H, Looy CV, Collinson ME, Brinkhaus H, van Konijnenburg-van Cittert JHA,
Kürschner WM, Sephton M, Environmental mutagenesis during the end-Permian ecological crisis, Proc. Natl Acad. Sci. USA, 2004, 101, 12952-12956.
Kourtidis K, Transfer of organic Br and Cl from the biosphere to the atmosphere during
the Cretaceous/Tertiary Impact: Implications for the stratospheric ozone layer, Atmos.
Chem Phys. Disc., 2004, 4, 6769-6787.
Hodgson DA, Vyverman W, Verleyen E, Levitt PR, Sabbe K, Squier AH, Keely BJ,
Late Pleistocene record of elevated UV radiation in an Antarctic lake, Earth and Planetary Sci. Lett, 2005, 236, 565-572.
Verleyen E, Hodgson DA, Sabbe K, Vyverman W, Late Holocene changes in ultraviolet
radiation pentration recorded in an East Antarctic lake, J. Paleolimnol., 2005, 34, 191202.
Huttunen S, Taipale T, Lappalainen NM, Kubin E, Lakkala K, Kaurola J, Environmental
specimen bank samples of Pleurozium schreberi and Hylocomium splendens as indicators of the radiation environment at the surface, Environ. Pollut., 2005, 133, 315-326.
Briffa KR, Osborn TJ, Schweingruber FH, Large-scale temperature inferences from tree
rings: a review, Glob. Planet. Change, 2004, 40, 11-26.
Blokker P, Yeloff D, Boelen P, Broekman RA, Rozema J, Development of a proxy for
past surface UV-B irradiation: A thermally assisted hydrolysis and methylation pyGC/MS method for the analysis of pollen and spores, Anal. Chem., 2005, 77, 60266031.
Lomax B, Beerling D, Callaghan T, Fraser W, Harfoot M, Pyle J, Self S, Sephton M,
Wellman C, The siberian traps, stratospheric ozone, UV-B flux and mutagenesis, in
Earth System Processes 2, 2005.
Fröhlich C, Lean J, Solar radiative output and its variability: evidence and mechanisms,
The Astron. Astrophys. Rev., 2004, 12, 273–320, DOI:10.1007/s00159-004-0024-1.
Shaffer JA, Cerveny RS, Long-term (250,000 BP to 50,000 AP) variations in ultraviolet
and visible radiation (0.175–0.690 um), Glob. Planet. Change, 2004, 41, 111-120.
Segura A, Krelove K, Kasting JF, Sommerlatt D, Meadows V, Crisp D, Cohen M,
Mlawer E, Ozone concentrations and ultraviolet fluxes on earth-like planets around
other stars, Astrobiol, 2003, 3, 689-708.
Canfield DE, The early history of atmospheric oxygen: Homage to Robert M. Garrels.,
Ann. Rev. Earth. Planet. Sci, 2005, 33, 1-36.
Rumble D, A mineralogical and geochemical record of atmospheric photochemistry
(Presidential address to the Mineralogical Society of America, Seattle, November 4,
2003), Am. Mineral., 2005, 90, 918-930.
Griffin REM, The detection and measurement of telluric ozone from stellar spectra, Pub.
Astron. Soc. Pacific, 2005, 117, 885-894.
Pyle J, Shepherd TG, Bodeker G, Canziani P, Dameris M, Forster P, Gruzdev A, Mueller R, Muthama J, Pitari G, Randel W, Ozone and Climate, Vol. in press, Geneva, 2005.
Barrie LA, Borrell P, Langen J, The changing atmosphere. An integrated global atmospheric chemistry observation theme for the IGOS partnership. Report of the Integrated
Global Atmospheric Chemistry Observation Theme Team, WMO, Geneva, 2004.
Isaksen ISA, (Editor) EC Air Pollution Report No. 81: Ozone-Climate Interactions,
2003.
Lemmen C, Guenther G, Mager F, Konopka P, Dameris M, Mueller R, Recalculation of
Arctic ozone hole recovery predictions with a detailed chemistry Lagrangian transport
model, in 3rd SPARC General Assembly, Victoria, Canada, 2004.
Marchand M, Bekki S, Lefevre F, Hauchecorne A, Godin-Beekmann S, Chipperfield
MP, Model simulations of the northern extravortex ozone column: Influence of past
The Environmental Effects Assessment Panel Report for 2006
21
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
22
changes in chemical composition, J. Geophys. Res., 2004, 109,
DOI:10.1029/2003JD003634.
Huck PE, McDonald AJ, Bodeker GE, Struthers H, Inter-annual variability in Antarctic
ozone depletion controlled by planetary waves and polar temperature, Geophys Res Lett,
2005, 32, DOI:13810.11029/12005GL022943.
Rind D, Perlwitz J, Lonergan P, AO/NAO response to climate change: 1. Respective
influences of stratospheric and tropospheric climate changes, J. Geophys. Res., 2005,
110, DOI:10.1029/2004JD005103.
Rind D, Perlwitz J, Lonergan P, Lerner J, AO/NAO response to climate change: 2. Relative importance of low- and high-latitude temperature changes, J. Geophys. Res., 2005,
110, DOI:10.1029/2004JD005686.
Zeng G, Pyle JA, Influence of El Nino Southern Oscillation on stratosphere//troposphere
exchange and the global tropospheric ozone budget, Geophys Res Lett, 2005, 32,
DOI:10.1029/2004GL021353.
Hare SHE, Gray LJ, Lahoz WA, O'Neill A, Steenman-Clark L, Can stratospheric temperature trends be attributed to ozone depletion?, J. Geophys. Res., 2004, 109, DOI:
10.1029/2003JD003897.
Solomon S, Portmann RW, Sasaki T, Hofmann DJ, Thompson DWJ, Four decades of
ozonesonde measurements over Antarctica, J. Geophys. Res., 2005, 110,
DOI:10.1029/2005JD005917.
Hoppel K, Nedoluha G, Fromm M, Allen D, Bevilacqua R, Alfred J, Johnson B, KönigLanglo G, Reduced ozone loss at the upper edge of the Antarctic Ozone Hole during
2001–2004, Geophys Res Lett, 2005, 32, DOI:10.1029/2005GL023968.
Weatherhead B, Tanskanen A, Stevermer A, Chapter 5. Atmospheric ozone and UV radiation, in ACIA Report, 2005, pp. 151-185.
Knudsen BM, Harris NRP, Andersen SB, Christiansen B, Larsen N, Rex M, Naujokat B,
Extrapolating future Arctic ozone losses, Atmos. Chem. Phys., 2004, 4, 1849-1856.
IPCC, Climate Change 2001: The Scientific Basis. Contribution of Working Group I to
the Third Assessment Report of the Intergovernmental Panel on Climate Change., Cambridge University Press, Cambridge, UK, 2001.
Gillett NP, Thompson DWJ, Simulation of recent Southern Hemisphere climate change,
Science., 2003, 302, 273-275.
Scaife AA, Knight JR, Vallis GK, Folland CK, A stratospheric influence on the winter
NAO and North Atlantic surface climate, Geophys Res Lett, 2005, 32,
DOI:10.1029/2005GL023226.
Toole DA, Siegel DA, Light-driven cycling of dimethylsulfide (DMS) in the Sargasso
Sea: Closing the loop, Geophys Res Lett, 2004, 31, L09308,
DOI:10.1029/2004GL019581.
Kuroda Y, Kodera K, Solar cycle modulation of the Southern Annular Mode, Geophys
Res Lett, 2005, 32, DOI:10.1029/2005GL022516.
Tourpali K, Schuurmans CJE, van Dorland R, Steil B, Bruhl C, Manzini E, Solar cycle
modulation of the Arctic Oscillation in a chemistry-climate model, Geophys Res Lett,
2005, 32, DOI:10.1029/2005GL023509.
Solanki SK, Usoskin IG, Kromer B, Schüssler M, Beer J, Unusual activity of the Sun
during recent decades compared to the previous 11,000 years, Nature, 2004, 431, 10841087.
Langematz U, Grenfell JL, Matthes K, Mieth P, Kunze M, Steil B, Brühl C, Chemical
effects in 11-year solar cycle simulations with the Freie Universität Berlin Climate Middle Atmosphere Model with online chemistry (FUB-CMAM-CHEM), Geophys Res Lett,
2005, 32, DOI:10.1029/2005GL022686.
The Environmental Effects Assessment Panel Report for 2006
Changes in biologically active ultraviolet radiation reaching the Earth’s surface
126 Muscheler R, Joos F, Müller SA, Snowball I, How unusual is today’s solar activity?,
Nature, 2005, 436, E3-E4.
127 Randall CE, Harvey VL, Manney GL, Orsolini Y, Codrescu M, Sioris C, Brohede S,
Haley CS, Gordley LL, Zawodny JM, Russell JM, III, Stratospheric effects of energetic
particle precipitation in 2003–2004, Geophys Res Lett, 2005, 32,
DOI:10.1029/2004GL022003.
128 Rohen G, von Savigny C, Sinnhuber M, Llewellyn EJ, Kaiser JW, Jackman CH, Kallenrode M-B, Schroter J, Eichmann K-U, Bovensmann H, Burrows JP, Ozone depletion
during the solar proton events of October/November 2003 as seen by SCIAMACHY, J.
Geophys. Res., 2005, 110, DOI: 10.1029/2004JA010984.
129 Solanki SK, Usoskin IG, Kromer B, Schüssler M, Beer J, Solanki et al. Reply to: R.
Muscheler et al. doi:10.1038/nature04045 (2005), Nature, 2005, 436, E4-E5.
130 de F. Forster PM, Joshi MJ, The role of halocarbons in the climate change of the troposphere and stratosphere, Climatic Change, 2005, 71, 249–266, DOI: 10.1007/s10584005-5955-7.
131 Rosenfield JE, Schoeberl MR, Recovery of the tropical lower stratospheric ozone layer,
Geophys Res Lett, 2005, 32, DOI:10.1029/2005GL023626.
132 Bill M, Conrad ME, Goldstein AH, Stable carbon isotope composition of atmospheric
methyl bromide, Geophys Res Lett, 2004, 31, DOI:10.1029/2003GL018639.
133 Redeker KR, Cicerone RJ, Environmental controls over methyl halide emissions from
rice paddies, Glob. Biogeochem. Cycles, 2004, 18, DOI: GB1027.
134 Andersen SB, Weatherhead EC, Stevermer A, Austin J, Bruhl C, Fleming EL, Grandpre
Jd, Grewe V, Isaksen I, Pitari G, Portmann RW, Rognerud B, Rosenfield JE, Smyshlyaev S, Nagashima T, Velders GJM, Weisenstein DK, Xia J, Comparison of recent
modeled and observed trends in total column ozone, J. Geophys. Res., 2006, 111,
DOI:10.1029/2005JD006091.
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Chapter 2. The effects on human health from stratospheric ozone
depletion and its interactions with climate change
M. Norvala, A. P. Cullenb, F. R. de Gruijlc, J. Longstrethd, Y. Takizawae, R. M. Lucasf, F. P.
Noonang and J. C. van der Leunh
a
Medical Microbiology, University of Edinburgh Medical School, Teviot Place, Edinburgh, EH8
9AG, Scotland
b
School of Optometry, University of Waterloo, Waterloo, Ontario, N2L 3G1, Canada
c
Leiden University Medical Centre, Sylvius Laboratories, Wassenaarseweg 72, NL-2333 AL
Leiden, The Netherlands
d
The Institute for Global Risk Research, LLC, Bethesda, Maryland 20817, USA
e
National Institute for Minamata Diseases, 4058 Hama, Minamata City, Kumamoto 867-0008,
Japan
f
National Centre for Epidemiology and Population Health, The Australian National University,
Canberra, 0200 Australia
g
School of Public Health and Health Services, The George Washington Medical Center,
Washington, DC 20037, USA
h
Ecofys, Kanaalweg 16G, NL-3526 KL Utrecht, The Netherlands
Summary
Ozone depletion leads to an increase in the ultraviolet-B (UV-B) component (280-315 nm) of
solar ultraviolet radiation (UVR) reaching the surface of the Earth with important consequences
for human health. Solar UVR has many harmful and some beneficial effects on individuals and,
in this review, information mainly published since the previous report in 20031 is discussed. The
eye is exposed directly to sunlight and this can result in acute or long-term damage. Studying
how UV-B interacts with the surface and internal structures of the eye has led to a further
understanding of the location and pathogenesis of a number of ocular diseases, including
pterygium and cataract. The skin is also exposed directly to solar UVR, and the development of
skin cancer is the main adverse health outcome of excessive UVR exposure. Skin cancer is the
most common form of malignancy amongst fair-skinned people, and its incidence has increased
markedly in recent decades. Projections consistently indicate a further doubling in the next ten
years. It is recognised that genetic factors in addition to those controlling pigment variation can
modulate the response of an individual to UVR. Several of the genetic factors affecting
susceptibility to the development of squamous cell carcinoma, basal cell carcinoma and
melanoma have been identified. Exposure to solar UVR down-regulates immune responses, in
the skin and systemically, by a combination of mechanisms including the generation of
particularly potent subsets of T regulatory cells. Such immunosuppression is known to be a
crucial factor in the generation of skin cancers. Apart from a detrimental effect on infections
caused by some members of the herpesvirus and papillomavirus families, the impact of UV-
The Environmental Effects Assessment Panel Report for 2006
25
Effects on human health from stratospheric ozone depletion and its interactions with climate change
induced immunosuppression on other microbial diseases and on vaccination efficacy is not clear.
One important beneficial effect of solar UV-B is its contribution to the cutaneous synthesis of
vitamin D, recognised to be a crucial hormone for bone health and for other aspects of general
health. There is accumulating evidence that UVR exposure, either directly or via stimulation of
vitamin D production, has protective effects on the development of some autoimmune diseases,
including multiple sclerosis and type 1 diabetes. Adequate vitamin D may also be protective for
the development of several internal cancers and infections. Difficulties associated with
balancing the positive effects of vitamin D with the negative effects of too much exposure to
solar UV-B are considered. Various strategies that can be adopted by the individual to protect
against excessive exposure of the eye or the skin to sunlight are suggested. Finally, possible
interactions between ozone depletion and climate warming are outlined briefly, as well as how
these might influence human behaviour with regard to sun exposure.
Introduction
There are many harmful and some beneficial effects of solar ultraviolet radiation (UVR) on
human health. Skin cancer and cataract are examples of the former category while the synthesis
of vitamin D is one example of the latter category. With ozone depletion and the consequent
increase in terrestrial UV-B, these effects may be enhanced. Various models predict increases in
the number of skin cancers and cataracts that can be attributed to ozone depletion over the
baseline that occurred before ozone depletion.1, 2 However, as stated previously1, human choice
in determining where, when, how and for how long an individual is exposed to solar radiation is
a major, if not the principal, factor that establishes the health outcomes. Assuming the same
human exposure habits, ozone depletion with resulting increase in UV-B will increase the
numbers of skin cancers and cataracts, while a positive effect could be a general improvement in
vitamin D status.
In this report, discussion will centre first on interactions between solar UVR and the eye and,
secondly, on interactions between solar UVR and the skin, concentrating on the risks of, and
trends in, the incidence of skin cancers and the genetic factors involved in their development. A
section on the immune effects of UVR comes next, followed by another on the UV-induced
synthesis of vitamin D and its relationship with a range of diseases. Finally, strategies for
responding to the problem of ozone depletion are considered, especially those that protect the
individual. In most instances, only new information available since the previous full report in
2003 is included although in certain instances reference is made to earlier key publications. It
should be noted that the topic of air pollution relating to ozone depletion is addressed in Chapter
6 of this report, this includes reference to aspects concerning human health.
The eye
The eye and the skin are the only organs of the body that are exposed to solar UVR. The effects
of sunlight on the eye may be acute (usually after a latent period of several hours), long-term
after an acute exposure, or long-term following chronic exposure to levels of UVR below those
required for acute effects (Table 1). In our last report we focused on cataract, the UV-B related
eye disease with the most serious public health implications.1 This section of the report
concentrates first on how UV-B reaches and interacts with the surface and internal structures of
the eye, and then provides an update on chronic effects that may impair vision.
26
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
Interaction of solar UV-B with target tissues in the eye
At low solar zenith angles (high solar elevation angles), the UV-B photons most likely to fall on
the cornea and other ocular tissues are those from indirect sunlight, i.e., those scattered by
atmospheric components or reflected from surfaces. In contrast to its effects on the skin, direct
sunlight plays a minor role in UV-B-related eye disorders due to a natural aversion to looking
directly at the sun, and shadowing by the brows when the sun is high is the sky. Under
conditions of cloud cover (with lower light levels), the natural defence mechanisms of the eye,
for example squinting, are relaxed, permitting greater exposure of the outer surface and internal
structures of the eye, such as the lens. At the same time, scattering and reflection by clouds
increases the diffuse radiation incident on the eye.3, 4 UV reflectance values vary considerably
for different natural terrains and manufactured materials. Grass and other green vegetation are
natural strong absorbers of UV-B and reflect this waveband poorly (2-3%), whereas fresh snow
is an excellent reflector (more than 90%). These variations can result in significant errors in
estimating UV-B exposure based solely on location, as was commonly done in early
epidemiologic studies of the role of sunlight in eye disease.
Table 1. Potential acute and chronic effects of exposure to UV-B on the eye and adjacent
tissues
Tissue
Acute Effect
Lid and peri-ocular skin Sunburn: erythema (redness)
Chronic Effect
Freckling
blistering
Lentigines (age spots)
exfoliation (peeling)
Hypomelanosis (vitiligo)
Tanning
Non-melanoma skin cancer
Actinic keratosis
Cutaneous melanoma
Conjunctiva
Photoconjunctivitis
Pinguecula (local degeneration)
Chemosis (swelling)
Dyskeratosis (abnormal epithelial
cell differentiation)
Intraepithelial neoplasia
Cornea
Photokeratitis
Endothelial damage (swelling)
Reactivation of latent herpes
viruses
Lens
Climatic droplet keratopathy
(epithelial degeneration)
Pterygium (see text)
Endothelial changes
Anterior subcapsular opacities Age-related cataract (see text)
Peripheral light focussing by the eye (see Figure 2-1). A factor that must be considered when
assessing exposure of the internal structures of the eye to UV-B is that the various zones of the
cornea direct the radiation to different locations within the eye. Coroneo et al.5 suggested that
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
light and UVR incoming from the side is focussed on specific areas of the cornea, resulting in a
twenty-fold increase in exposure that may be important in the induction of pterygia and cataract.
They also proposed that UVR was similarly concentrated in the lower nasal quadrant of the
crystalline lens, the location where age-related cortical cataract is commonly first detected.
Human6 and mannequin7 studies have confirmed that incoming temporal UVR from behind the
coronal plane (100o to 135o to the sagittal
plane, see Figure 2-1) was focussed into the
anterior chamber angle. This is modified by
corneal shape, anterior chamber depth, and
location of the eye within the bony orbit,
squinting, eyelashes, prominence of
cheekbones and presence of lid skin folds on
the temporal side of the eye.
Transmittance of the ocular media. In
order for UV-B incident on the surface of
the eye to reach the crystalline lens, it must
first pass through the cornea and the
aqueous humour. Although the aqueous
humour absorbs little environmental UV-B,
the cornea has a significant role in
preventing UV-B from reaching the lens,
with some parts of the cornea being more
effective than others. Kolozsvari et el.8 have
shown that UV-B absorption is about twice
as high in the anterior layers (epithelium and
Bowman layer) of the human cornea as in
the posterior layers. Their data indicate that
the whole cornea begins to transmit at 280
nm (<0.01%), increases to 1% at 295 nm
and approaches 5% at 300 nm. Although
the actual amount of UV-B transmitted is
low, it should be noted that UV-B at 300 nm
is about 600 times more biologically
effective at damaging ocular tissue than UVA at 325 nm.
Figure 2-1. Peripheral light focussing. Top: Photograph
showing how a beam directed towards the temporal side of
the cornea is focussed into the anterior chamber angle.
Bottom: A beam of light (or UVR), from behind the
coronal plane, directed onto the temporal periphery of the
cornea is refracted and focussed into the nasal angle of the
anterior chamber of the eye, as shown by arrows. If the
incident beam originates in front of the coronal plane, the
focus shifts into the nasal part of the lens.
At birth the human lens is colourless and
allows both UV-B and UV-A to pass
through to the retina. As the lens ages, there are significant changes in the lens proteins,
including a decrease in their solubility, that result in increased, wavelength independent, scatter
and consequent degradation of vision (clinically called nuclear sclerosis). Frequently there is
also a yellowing which can eliminate the passage of UVR and limit the passage of light in the
violet-blue end of the visible spectrum.
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Chronic effects of UVR on the eye
Pterygium. This wing-shaped, inflammatory, proliferative and invasive growth occurs on the
conjunctiva and cornea of the human eye (Figure 2-2). It is induced, in part, by intracellular
damage caused by UV-B exposure9 and most commonly occurs in the superficial layers of the
nasal cornea. Pterygia grow towards the centre of the cornea and can severely impair vision. In
their early stages, they appear as small opacities at the nasal edge of the cornea and then spread
to become a fleshy raised area. A number of causal factors, other than UVR, have been proposed
as important to pterygium development including mechanical irritation, heredity, heat, cold, and
wind. None of these adequately explains the predominately nasal location of pterygia. This
preferred location has been explained, however, on the basis of the peripheral light focussing
effect discussed above.10
Pterygia are more prevalent and progress more
rapidly in individuals living in regions near to the
equator or at very high altitudes. Al Bdour and
Latayfey11 reported a strong correlation between
pterygia and environmental UVR in Australian
aborigines. In the more temperate climate of the
northeastern U.S., a significant relationship was
found between the cumulative dose of solar UVA and UV-B and the prevalence of pterygium.12
The higher prevalence of pterygium in outdoor
occupations has been attributed to exposure to
excessive amounts of sunlight. In a populationbased sample of residents of the Australian state Figure 2-2. An early pterygium.
of Victoria who were aged 40 years and older,
statistical modelling revealed that 43.6% of the risk of pterygium could be attributed to
cumulative dose of sunlight.13 This result was the same when cumulative dose of ocular UV-B
was substituted in the model for cumulative dose of sunlight. Pterygium continues to be
considered a significant public health problem in rural areas and occurs primarily as a result of
ocular sun exposure.13 In a study conducted in Perth, Western Australia14, there were strong
positive associations between pterygium and measures of potential and actual sun exposure. The
strongest associations were seen for the estimated daily ocular solar radiation dose at any age,
which in those in the highest quartile of exposure resulted in about a 7-fold greater risk.
Although other agents may contribute to pterygium development15-17, in most epidemiological
studies the common factor is UVR exposure, thereby indicating that UVR can be considered a
causal agent. Thus, the implication for prevention of pterygium is that ocular protection from
sunlight is beneficial at all ages.
Cataract. Three main types of age-related cataract can be distinguished, based on their location:
cortical cataract involving the anterior (and posterior) cortices of the lens; posterior subcapsular
cataract at the extreme posterior cortex lining the lens capsule1 and nuclear (sclerotic) cataract at
the nucleus of the lens. However by the time the individual requires surgery, mixed categories
are most commonly present. Cortical cataract arises from localised changes occurring in the
cortex of the lens, where opaque radial spokes begin to develop on the periphery and extend
towards the centre, eventually affecting vision.18, 19 The second form of cataract, posterior
subcapsular cataract, is thought to develop when the lens epithelial cells migrate to form a plaque
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of opacities and cysts at the posterior surface of the lens. These lesions are particularly
detrimental to vision when the pupil constricts due to sunlight or other bright sources, or during
near tasks. The third form of cataract, nuclear cataract, occurs as the crystalline lens of the eye
ages and the nucleus loses its transparency, becoming more opalescent and sometimes turning
yellowish to brown in hue.20, 21
A number of publications has reviewed the epidemiologic information linking UVR exposure to
cataract.22-24 Although earlier reviews concluded that the range and variability of the study
designs precluded definitive conclusions, most of the more recent analyses suggest a role for
UV-B in some types of age-related cataract, particularly cortical cataract. A frequently cited
early estimate of risk from personal ocular exposure to solar UV-B is that of Taylor et al.25 in the
Chesapeake Bay Waterman Study. Watermen in the highest quartile had a three-fold increased
risk for cortical cataract. It is important to note that the subjects in this cohort were only exposed
to levels of solar UV encountered in mixed, often overcast, climate at intermediate latitude. The
same group26 that conducted the Chesapeake Bay Waterman Study also conducted a populationbased epidemiologic study in Salisbury, Maryland. The increased risk of 10% of developing
cortical cataract associated with UV exposure in this study (the Salisbury Eye Evaluation [SEE ]
project27) was more modest, but the population was considered more representative of the U.S.
as a whole. West and her colleagues subsequently used these data from the SEE project as the
basis from which to develop risk estimates for the entire U.S. population under conditions of
ozone depletion.26 These risk estimates, which were calculated for fixed levels of ozone
depletion ranging between 5 and 20%, indicated that the number of cortical cataract cases seen
by 2050 would increase between 1.3 and 6.9% respectively, with associated health costs for the
U.S. of between about $0.6 and $3 billion respectively. There are, in addition, important social
costs associated with cataract development.
A recent review found that there was insufficient evidence to conclude that UVR exposure
played a causal role in the development of posterior subcapsular cataract.28 However, a recent
study in Japan29 showed that the severity of nuclear cataract increased with UV-B exposure.
Furthermore, lifetime cumulative UV-B exposure and particularly exposure in the teenage years
correlated with the presence of nuclear cataract in females. Another report indicated that the
association between nuclear cataract and occupational sun exposure was significant for exposure
between the ages of 20 and 29 years.30 Supporting evidence for such a difference in a period of
age susceptibility is provided by an animal study in which the same dose of UVR induced more
severe cataracts in young than in older animals.31
The skin
Sunburn is the effect most frequently experienced by the human population due to excessive
solar UV-B exposure. It is an inflammatory reaction to a toxic assault on the skin. Although
human skin is adapted to the ambient UVR, the sunburn reaction demonstrates that excessive
exposures can stretch defensive mechanisms to the limit, or even exceed them (pain and blister
formation). Despite the remembered discomfort from past episodes, about a third of US residents
report at least one sunburn per year.32 Fair-skinned people are most susceptible to sunburn, and
they correspondingly run a higher risk of long term adverse effects, such as skin cancer. In the
following sections, the relationship between various types of skin cancer and solar UVR is
outlined.
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Skin cancer types and trends
Skin cancer is the most common form of cancer among fair-skinned populations and its
incidence has increased markedly over the last century. Many skin cancers are detected early, at
a stage where they can be easily and effectively treated. This limits morbidity and mortality. In
addition, for the majority of skin cancers, the ‘non-melanoma’ skin cancers (NMSC) consisting
of basal cell carcinomas (BCC) and squamous cell carcinomas (SCC), the malignant potential is
low which also reduces death from these diseases. This is not the case for the most malignant
form of skin cancer, melanoma, that arises from pigment cells (melanocytes), and is responsible
for most of the deaths from the skin cancer. Projections show an approximate doubling in all
types of skin cancer from 2000 to 2015 in the Netherlands, but this is also due, in large part, to
ageing of the population.33
Melanoma
As found in earlier epidemiological studies, cutaneous malignant melanomas are related to sun
exposure in early life, to episodes of severe sunburn, and to the number of moles (nevi), which in
turn is related to sun exposure in early life.34 In the last decade, much progress has been made in
identifying genetic changes in melanoma cells, and the functional importance of these genetic
changes for melanoma development has been demonstrated in genetically modified mice.
However, the precise mechanisms underlying nevus formation and progression to melanoma,
and the role of solar UVR in this process, remain to be resolved.35, 36
Epidemiology of melanoma. Although rates of increase in melanoma incidence appear to be
levelling off in countries with the highest number of cases37-39, the absolute incidence is
continuing to rise. Mortality, however, has risen much less or has even stabilized especially in
females, and in younger age cohorts, although not in older males in countries such as the USA,
Scotland and Australia. The major increase in incidence recently has been attributed to the thin
melanomas that have high survival rates.40 A thin melanoma is defined as being less than or
equal to one mm thick. This predominance of the early stages of melanoma could be due to
greater awareness in the general population regarding the dangers of suspicious-looking moles.
Prompt diagnosis and treatment may then limit any increase in mortality.41, 42 Melanomas with
an attached nevus from which they apparently originated are on average thinner, of the more
superficial spreading type and occur more often in irregularly exposed skin than melanomas that
show no remnants of a precursor nevus.43 Patients with the nevus-associated melanomas are
younger and have more nevi.
Strouse et al.44 found that the incidence of melanoma in children in the USA is rising rapidly but
survival is improving. They showed that the incidence rate of melanoma was positively
correlated with environmental UVR exposure. The chance of surviving a melanoma decreases
with age and is lower for boys compared with girls. It is also lower if the primary tumour occurs
on body sites other than the extremities and the torso (i.e., locations other than those exposed
intermittently to the sun). The latter finding is in agreement with a study of adults by Berwick et
al.45 who found that survival from melanoma was higher in individuals with a history of
increased intermittent sun exposure and episodes of sunburn. However, these authors also found
improved survival with a history of increased skin awareness and increased solar elastosis (i.e., a
skin ‘aged’ by chronic sun exposure).
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Earlier reports regarding a seasonal variation in the diagnosis of melanoma were confirmed in
recent European and Australian studies. These revealed maximum incidence for thin melanomas
on extremities in the summer in females.46, 47 This effect may be attributable to enhanced skin
awareness in the hotter months or to stimulation of melanoma growth after (over-)exposure to
the sun. Boniol et al.47 found that survival from melanomas diagnosed in the summer was
higher, as might be expected from the higher number of thin melanomas diagnosed at that time
of the year, but, after correction for tumour thickness, the effect was still significant. The authors
therefore suggest that patients in whom melanomas are diagnosed after recent sun exposure may
show better survival.
Trends and changes in skin cancer incidence over recent decades clearly indicate the importance
of human behaviour, particularly in relation to exposure to solar UVR.37 For example, Gandini
et al.48 undertook a meta-analysis of 57 observational studies which showed that intermittent sun
exposure and sunburn history played considerable roles as risk factors for melanoma, and
Agredano et al.49 found a very strong relationship between increasing access to air travel to
leisure destinations and increasing melanoma incidence. However, case-control studies
generally find that genetic factors carry more risk than behavioural aspects, such as moderating
UV exposure.50 It should be noted, however, that the genetic factors can be determined more
accurately than personal UV exposure; the latter is assessed by very poor surrogates (e.g.
recalled number of sunburns in youth or lifetime hours of sun exposure). This inaccuracy in
determining past UV exposure will tend to lead to lower estimates of relative risk. Moreover, an
individual’s behaviour with regard to UV exposure can be altered to reduce risk, very much in
contrast to an individual’s genetic background.
Latitudinal and temporal trends in skin cancer, notably in melanomas, underline the major
importance of UV exposure as an environmental risk factor. The integrity of the stratospheric
ozone layer, as the prime atmospheric UV filter, therefore remains crucial in protection against
melanoma.
Genetic risk factors for melanoma. There are well-established genetic factors conferring
susceptibility to melanoma – notably inherited mutations in the cell-cycle control gene,
p16INK4a, and in the “hair-colour” gene which codes for the melanocortin 1 receptor (MC1R).
The MC1R gene contributes to the control of pigmentation in hair and skin51 and is an important
risk factor for all types of skin cancer, including melanoma.52 Other additional genes are related
to melanoma risk, e.g., the OCA2 gene which also controls skin and eye colour53, and an as yet
unknown gene located on chromosome 1.54
UVR causes DNA damage which can give rise to gene mutations which in turn can contribute to
skin cancer formation (see below). Hence, repair of this damage is of crucial importance. The
solar UV-B induced DNA damage (mainly cyclobutane pyrimidine dimers, CPDs) is removed by
a ‘cut-and-paste’ type of DNA repair (‘nucleotide excision repair’). A complete dysfunction in
one of the enzymes in this repair system results in a dramatic increase in risk of skin cancer,
including melanoma. More subtle genetic variations (polymorphisms) in the repair enzymes can
modify the efficacy of DNA repair, and thus affect skin cancer risk. Certain genetic variations in
repair enzymes were indeed found to be associated with melanoma risk.55-61
UVR can generate reactive oxygen species and thus inflict damage to cell components,
particularly DNA. Although melanin pigment is generally protective, it may also contribute to
oxidative damage under certain conditions62, especially its red variety, pheomelanin.63 Certain
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inherited or acquired traits that increase oxidative stress appear to be associated with melanoma
and its precursor lesion, dysplastic nevus.64-66 Genetic variation in a protein (APE1) involved in
the repair of oxidized DNA modifies melanoma risk.67
These inherited predispositions to develop melanoma will help to identify high risk groups who
may be particularly susceptible to increases in ambient UV-B radiation.
Oncogenic alterations in melanomas. In terms of molecular mechanisms, melanomas from
chronically exposed, from intermittently exposed and unexposed skin sites have different
molecular signatures.68 Notably, the melanomas from intermittently exposed skin have a high
frequency of activating mutations in a critical signalling molecule, B-RAF. MC1R variants,
which are associated with enhanced risk of melanoma, are strongly associated with B-RAF
mutations.51 Ten to 20% of melanomas from chronically exposed skin bear mutations in N-RAS,
a protein preceding B-RAF in the signal cascade for cell proliferation.69 Mutations in B-RAF and
N-RAS genes are already present in some cells in nevi70, but nevus cells do not proliferate and are
kept in a ‘senescent state’.71, 72 The mutations in the B-RAF oncogene are not typical of UV-B
radiation, but could be due to UV-induced oxidative damage.
The epidemiological finding that melanomas associated with intermittent sun exposure45 show
better survival may be linked to the specific molecular changes found in these tumours.
Animal experiments on UVR and melanoma. Because of the well-established role of UVR in
NMSC and the known mutagenic and carcinogenic properties of UV-B radiation, it seems most
likely that UV-B wavelengths are also contributing to the development of melanoma. However,
human melanomas show no gene mutations that are typical of UV-B radiation. Animal models
may serve to elucidate whether, and if so, how UV-B radiation contributes to the development of
melanoma.
Experiments with transgenic mice confirmed the epidemiological finding that the neonatal period
can be critical to the development of melanomas later in life.73, 74 More specifically, a study in
transgenic mice showed neonatal UV-B exposure to be highly effective.75 These melanomas,
which closely mimic the human disease, could not be evoked by neonatal UV-A exposure.75 The
latter finding is in accordance with earlier experiments in opposums76, but differs from the
results obtained with small Xiphophorus fish.77 In the fish, both UV-B and UV-A neonatal
exposure proved to be very effective in causing melanomas, and the variation in effectiveness
with wavelength was recently found to closely follow the variation in the UV induction of
oxidant radicals from melanin in the skin of the fish.78 In the initial experiments with neonatal
UV exposure, the HGF transgenic mice were albino, but recent experiments showed that these
mice crossed into a pigmented background were also susceptible to melanoma induction by
neonatal UV-B exposure (Noonan and De Fabo, personal communication). Further
experimentation with this model may shed more light on the wavelength dependency of
melanoma induction in mammals. In another model, melanomas were induced by massive doses
of UV-B radiation delivered to repair-deficient transgenic mice.79 However, the severe skin
trauma inflicted may have caused non-specific tumour promotion.80
In support of the epidemiological finding that intermittent sunburning exposures increase the risk
of melanoma, experiments in hairless mice have shown this type of exposure regimen to be
considerably more effective in inducing nevi (potential precursors of melanoma) than a regimen
in which the exposure was more evenly spread over time.81 Thus, sunburning UV-B exposure of
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adults may indeed also contribute to melanoma development by stimulating the proliferation of
melanocytes.82
Immunity and melanoma. There are indications that immune mechanisms against melanomas
are present in humans as demonstrated by the occasional spontaneous regression of some
pigmented skin lesions. Further, immune responses against melanoma antigens are readily
detectable in patients and immunotherapy is actively used for melanoma treatment.83, 84 As
found earlier for BCC, melanoma risk appears to be related to the density of mast cells in
unexposed skin85 so that the higher the number of mast cells, the greater the chance of
developing melanoma. Interestingly, children with eczema (atopic dermatitis) develop fewer
melanocytic nevi than children without eczema86, and the therapeutic effect of UV exposure on
the eczema might be related to a possible effect of the radiation on the cytokine network in the
skin, the products of which then stimulate melanocytic growth.
Whereas there is substantial evidence for a role for UV-induced immunosuppression in NMSC, it
is not known as yet if this mechanism is a factor in melanoma progression; this is currently an
area of intense investigation.
Non-melanoma skin carcinomas (NMSCs)
In epidemiological studies prior to 1980, the skin carcinomas, SCC and BCC, were not
considered separately, and were commonly found in people who had accumulated excessive
hours of solar (UV) exposure. In more recent studies, important differences between SCC and
BCC have emerged. SCC is associated mainly with chronic and life-long accumulated sun
exposure87 whereas BCC, similar to melanoma, is more closely associated with early-life and
intermittent exposures resulting in episodes of severe sunburn. In addition, while SCCs occur on
body sites most regularly exposed to the sun such as the face, BCCs are also found frequently on
sites exposed intermittently to sunlight. Also the genetic alterations identified in SCC and BCC
show important differences.
Epidemiology of NMSC. Studies continue to show increases in the incidence of both SCC and
BCC33, 88, 89, with disproportionately high increases in BCC in young females on the lower
limbs.90, 91 Sunbathing is associated with a five-fold rise in the risk of BCC on the trunk.57
Although BCC is locally invasive, it is usually a slow growing and not very aggressive tumour;
superficial BCC on the trunk is often misdiagnosed and confused with eczematous skin lesions.
Detailed skin examination of subjects in a Queensland community established that the incidence
of BCC on sites other than head, neck, hands and arms was 3-fold higher than actually treated92;
a smaller study in Spain produced a similar result.93 Hence, the large majority of the BCC on
irregularly exposed sites appear to remain ‘sub-clinical’, i.e., cause no great discomfort, are
never presented to a physician and remain essentially undetected.
Death due to NMSC in the USA has declined, and when it occurs, is often related to an
excessively long delay before seeking medical care.94
Genetic risk factors for NMSC. UV-B radiation inflicts highly characteristic DNA damage
(mainly CPDs), and the repair of this damage in human skin diminishes with age.95 This type of
DNA damage causes specific ‘point mutations’ which are found in the P53 tumor suppressor
gene in NMSC (see below). However, NMSC also show frequent crude chromosomal
aberrations.96 Such aberrations are already abundantly present in the benign precursor lesions of
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SCC, the actinic keratoses (AKs). Complete double strand breaks (DSB) in the DNA cause these
gross chromosomal losses and duplications. Interestingly, variants in genes involved in the
repair of DSB in DNA appear to be related to NMSC risk, but not to melanoma risk97 The
association between NMSC and DSB repair ties in nicely with the recent finding that UV-Bexposed blood cells from patients with skin carcinomas are more prone to develop chromatid
breaks than equivalent cells from melanoma patients and control subjects.17
Genetic variations in specific antioxidant proteins are associated with NMSC risk.98 Variants of
a repair enzyme, involved in excision of oxidized bases in DNA, affect SCC risk, but not the risk
of BCC or melanoma.97 Hence, there appear to be considerable differences in how oxidative
DNA damage (such as induced by UVR) and its repair are related to the various types of skin
cancer.
Oncogenic alterations in NMSC. Although considerably less efficient than UV-B, long-wave
UV-A radiation can cause the same type of DNA damage as UV-B radiation, and thus give rise
to ‘UV-B-like’ mutations in the P53 tumor suppressor gene. However, oxidative damage
contributes substantially at these longer wavelengths and causes different P53 mutations from
those induced by UV-B.99, 100 Microscopic clusters of cell clones with strong expression of
mutant-p53 protein in sun-exposed skin carry the same types of ‘UV-B-like’ P53 mutations as
skin carcinomas.100, 101 Hence, all of these common microscopic clusters of cells with mutantp53 in human skin could be potential precursors of skin carcinomas. In Swedish studies,
microdissection of skin carcinomas showed consistent mutations in the P53 gene throughout the
tumour masses, i.e., most tumours appeared to be a clonal expansion from a founder cell with a
particular ‘UV-B-like’ P53 mutation.101, 102 This conclusion is in agreement with earlier studies
that found dominant ‘UV-B-like’ mutations in SCCs and BCCs.103, 104 In contrast to these
findings, a recent Australian study reported P53 mutations to be very diverse, heterogeneous and
disjunctive in SCCs and adjacent skin, i.e., every microdissected part of a tumour showed
different P53 mutations without any suggestion of a founder mutation or any clear overall
indication of UVR as the cause.105 By arguably separating out UV-B-like, UV-A-like, oxidative
and ‘other’ P53 mutations, the authors found the UV-B-like mutations to be located in the
shallow parts of the tumours and the UV-A-like mutations in the deeper parts. This issue clearly
needs to be investigated further.
Although both SCC and the precursor AK frequently carry various chromosomal aberration, the
loss of a particular part of chromosome 18 appears to be related to the progression from AK to
SCC.96 The presence of multiple copies of parts of chromosomes may explain the amplification
of the H-RAS oncogene frequently found in SCC.106
As reported in our previous review1 and confirmed recently107, nearly all BCCs display
activation of the Hedgehog proliferative pathway, mostly through a defect in the PTCH protein
in the cell membrane by mutations or loss of the coding gene. Some of these mutations are ‘UVB-like’. Further research has shown that certain variations in the PTCH gene may predispose
towards BCCs108, and that UV-B radiation can suppress PTCH function and thus potentially
stimulate BCC development.109
Hence, the oncogenic alterations found in NMSC are attributable largely to UVR, and in some
cases more specifically to UV-B radiation.
Animal experiments on UV and NMSC. Experiments in transgenic mice have identified the
type of UV-B-induced damage (CPDs) that causes SCC and more immediate effects such as
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
sunburn and thickening of the outer viable layer of skin (the epidermis).110 Clones of cells with
mutations in the P53 gene – such as found in human skin – have been induced in well-controlled
experiments in which mice were exposed to UV-B radiation.111 Here these p53-mutant clones
were tightly linked to the subsequent occurrences of SCC. In mice, UV-B-induced DNA damage
gives rise to DSBs and strong signals for DSB repair.112 Thus, UV-B radiation may induce the
chromosomal aberrations present in human NMSC.
Immunity and NMSC. Organ transplant recipients (OTR) have a dramatically increased risk of
developing SCC and, until recently, this was considered to be solely the result of taking
immunosuppressive medication to prevent rejection of the transplant. Evidence is now
accumulating to indicate that conventional immunosuppressive drugs can also adversely affect
UV-induced DNA damage and repair in skin cells113-115 and thus they may increase the risk of
SCC. Immunosuppressed patients other than the OTR may be affected similarly.116 A new
generation of immunosuppressive drugs with a different mode of action may substantially reduce
the risk of SCC.117 Hence, the increased incidence of SCC in relation to immunosuppressive
drugs may be due in large part to detrimental effects on UV defensive mechanisms in the skin,
rather than to immunosuppression per se.
Immune effects of solar UVR
Mechanisms of UV-induced immunosuppression
When the skin is exposed to UVR, a complex cascade of events begins that ends in the
suppression of certain types of immune responses, mainly those involving cell-mediated
immunity. The main interactions affected are between three types of immunologically active
white blood cells: antigen-presenting cells (APCs), T-helper (Th) lymphocytes and T-regulatory
(Treg) lymphocytes. The degree of suppression and the forms of cell-mediated immunity affected
can vary depending on the quality, quantity and timing of the UVR, the frequency of the
exposures, and the extent and location of the body surface irradiated.
One distinction commonly made is between local and systemic immunosuppression. Local
immunosuppression occurs when an antigen (a “non-self” molecule that the host recognises as
foreign and makes an immune response to) is applied directly to the irradiated body site soon
after the UV exposure, resulting in a down-regulation of immunity to that antigen. In systemic
immunosuppression, following UV exposure of one part of the body, the antigen is applied to a
distant unirradiated body site, again leading to systemic down-regulation of immunity to that
antigen. Certain steps of the two pathways differ such as whether the APCs have been directly
exposed to the UVR or not.
The process for local immunosuppression is outlined in Figure 2-3, and details of both local and
systemic mechanisms can be found in several excellent reviews.118-121 In brief, at least three
photoreceptors located at or near the skin surface are involved – DNA, trans-urocanic acid and
membrane components. On absorption of photons, the respective structural changes include
formation of thymine dimers in DNA, isomerisation of trans to cis-urocanic acid, and lipid
peroxidation in membrane components. These alterations initiate the pathway and stimulate the
local production of the large range of immune mediators shown in Figure 2-3. Such molecules
have profound effects on various cell populations in the irradiated site and possibly elsewhere in
the body. In particular, there are changes in the numbers and function of the APCs which lead to
alterations in particular T lymphocyte subsets. For example, inhibition in the release of certain
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(type 1) cytokines from T helper 1 (Th1) cells occurs. This is significant as the type 1 cytokines
are very important in the responses to simple chemicals, such as nickel, and in the
immunological control of tumours and intracellular infections, such as those caused by viruses.
At the same time, Treg cells are stimulated to release immune mediators that are involved in the
control of other T-cell subsets. Upon activation by a specific antigen, these Treg cells are capable
of down-regulating immunity by the production of immunosuppressive cytokines. There is
much interest currently in trying to characterise populations of Treg cells, particularly as they may
have therapeutic value in the
treatment of autoimmune and
other diseases.122
The majority of experimental
systems to date have involved a
single or a limited number of
exposures to UVR, containing the
UV-B waveband predominantly,
and in doses sufficient to cause
sunburn (erythema) followed by
application of the test antigen.
Under natural conditions, people
are exposed to solar UVR in
which the UVB represents less
than 6% of the total UV
spectrum123 and they frequently
receive suberythemal doses on a
daily basis, especially during the
summer months. Many respond
to this chronic low level exposure
by tanning and by skin thickening.
These responses, which provide
Figure 2-3. Outline of pathway leading to local immunosuppression
some protection against the
(antigen applied to the irradiated skin site) following UV irradiation.
burning effect of UVR, might lead
to photoadaptation so that protection against UV-induced immunosuppression could also
develop. This possibility has been tested recently in both mice and humans. For most immune
responses, photoadaptation did not occur so that the immunosuppression continued throughout a
period of repeated daily exposures to suberythemal solar simulated radiation.124, 125
The impact of UVR on infectious diseases and vaccination of human subjects
The 2003 UNEP report1 summarized the evidence available at that time demonstrating that solar
UVR exposure could adversely affect the pathogenesis of various infections. Information on this
topic reported since 2003 is outlined below. The two cases in which UVR exposure definitely
causes a detrimental change in the pathogenesis are herpes simplex virus (HSV) which causes
cold sores and human papillomavirus (HPV) which commonly causes warts. In both cases, UV
appears to have dual effects – both on the immune response and on the virus itself, and these
mechanisms are outlined below. The apparent inability of UVR to alter the course of other
human infections could be because the causative agents themselves do not contain any UV
responsive elements, or that the human immune system is sufficiently robust so that if one aspect
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
of it is suppressed, another can compensate. It should be noted, however, that only a limited
number of human infections have been investigated thus far in the context of solar UVR.
Herpes simplex virus (HSV). Several epidemiological and experimental studies have indicated
that exposure to solar UVR exposure is a common stimulus for the reactivation of HSV type 1
from latency in the nerve tissue. The virus then travels down the sensory nerve and replicates in
the skin to induce a recurrent lesion (cold sore) at the same site as the initial infection had
occurred. A large-scale study of 3678 infected patients, 2656 of whom suffered HSV recurrent
lesions, was undertaken recently in a Prefecture of Japan to further evaluate the role of solar
UVR exposure.126 The self-reported cause of the recurrence of cold sores was the sun in 10.4%
of individuals. In the summer months, this rose to 19.7% overall, and to 40% in subjects
younger than 30 years. One mechanism likely to be important here is the suppression of local
immune responses as a result of UV exposure: the virus arriving at the cutaneous site from the
nerve will have time to replicate and to induce the clinical symptoms before effective
immunological control is regained.127, 128 Such a scenario has been shown to operate in mice
infected cutaneously with HSV and then UV irradiated.129 New studies indicate that a second
mechanism involving a more direct interaction between HSV and UVR is probably required to
reactivate the virus, in addition to the immune effects of the UVR. For example, UV-induced
damage to nerve endings can lead to changes that result in the activation of HSV promoters, and
hence to the reactivation of the virus from latency.130
Human papillomavirus (HPV). It has been recognised for several years that, in
immunosuppressed subjects and those with epidermodysplasia verruciformis (EV; a rare genetic
disease in which the APCs are defective), infections with certain cutaneous HPV types (EVHPV) are associated with the development of SCCs but only on body sites most exposed
naturally to sunlight, such as the face and backs of the hands. New information has now
provided evidence that immunocompetent individuals can be similarly affected, i.e., UVR
exposure and infection with certain cutanous HPV types can act as co-factors in the development
of not only SCCs and but also of BCCs (reviewed in131). The interactions here are complex but,
in brief, the HPV is able to stimulate cell proliferation and inhibit UV-induced programmed cell
death (apoptosis) in the epidermis. These properties, together with the local immunosuppression
and the additional genetic changes induced by the UVR exposure, may lead to tumour
progression. Furthermore, on the basis of a lifetime-retrospective questionnaire on sun exposure,
it has been suggested that sunburn episodes in the past lead to an increase in the risk of infection
with particular HPV types in healthy subjects.132
The conjunctiva of the eye represents a further site where an association between HPV, SCC and
sun exposure is probable. Conjunctival SCCs from subjects in Uganda, where the sunlight
exposure is very high, were analysed for particular P53 mutations (CCåTT) as a molecular
signature of mutagenesis by solar UVR.133 The prevalence of CCåTT transition (56%) was the
highest observed in any of the cancer types evaluated and matched that of skin cancers in XP
patients (see section below, The impact of UVR on tumour immunity). In addition EV HPV
types were found in 86% of cases of SCCs of the conjunctiva.134 It was suggested that these
results confirm the causal role of solar UVR exposure in SCC of the conjunctiva and lead to the
conclusion that the HPV infection could act as a co-factor in the mutagenesis process.
Recently an unexpected interaction between HPV types and solar UVR exposure has been
revealed. Hrushesky and colleagues in the Netherlands observed a seasonal fluctuation in the
frequency of cervical smears that were positive for the anogenital HPV types: it was twice as
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high in the summer months with a peak in August.135, 136 There was a positive correlation
between the monthly HPV detection rate and the monthly solar UVR exposure. Hrushesky et al.
speculate that UV-induced systemic immunosuppression could be the main reason for the
increase in active HPV infections in the cervix in the summer months. This finding could be of
importance as the high-risk anogenital HPV types are recognised to be the primary cause of
carcinoma of the cervix, a tumour that is estimated to kill about 500,000 women annually
worldwide.
Vaccination. To date, only one large-scale experimental study, carried out in the Netherlands,
has evaluated whether solar UVR exposure can affect the generation of immune responses to
vaccines.137 In brief, subjects were vaccinated with recombinant hepatitis B surface antigen
following whole-body UV irradiation on five consecutive days in half of the individuals. While
natural killer cell activity and contact hypersensitivity responses were suppressed in the
irradiated subjects compared with the unirradiated subjects, there was no difference between the
two groups in the hepatitis B-specific T cell or antibody responses. However, when the subjects
were genotyped to characterise their cytokine polymorphisms (which can affect cytokine
production or activity), it was found that individuals with a particular interleukin-1β
polymorphism showed suppressed antibody responses to hepatitis B virus, if exposed to UVR
prior to the vaccination.138 Furthermore when skin samples were assessed for cis-urocanic acid
concentration (which acts as major photoreceptor for UVR in the skin and can initiate the
cascade resulting in immunosuppression), UV-irradiated subjects with higher cis-urocanic acid
levels had suppressed T cell responses to the vaccine.139 These results indicate that there are
genetic and other differences in the way in which an individual might respond to vaccination in
the context of UVR exposure. Therefore, it may not be appropriate to put all the irradiated or
unirradiated subjects into single groups in order to make valid comparisons regarding UVinduced effects on immune responses during vaccination.
Three further studies are of interest. Sharma et al.140 investigated an outbreak of measles in
children in an Indian city and found that one-third of the cases had occurred in individuals who
had been vaccinated previously against measles and who should have been protected as a result.
They suggested that the virus-specific immunity could have waned due to solar UV-induced
suppressive effects although experimental evidence is required to substantiate this idea. Snopov
et al.141 studied plasma cytokine levels following measles and poliovirus vaccination in infants in
St Petersburg, Russia, some of whom had received ten daily suberythemal whole-body exposures
to UV lamps (emitting predominantly UV-B) prior to the vaccination. This procedure was
thought to improve the general health of such children. A shift towards a Th2 cytokine response
occurred in the infants who had been UV exposed, but without the development of any clinical
symptoms; antibody titres were not measured. Finally Ghoreishi and Dutz142 demonstrated
recently that if mice were immunised with a protein applied directly to UV-irradiated skin
together with an adjuvant (the trancutaneous route), immune responses to that protein were not
generated. This outcome was mediated by Treg cells that function through the production of the
immunosuppressive cytokine, interleukin-10. In the future, the trancutaneous route may become
preferred to subcutaneous inoculation as it avoids the use of needles; thus this result is of
considerable interest.
In conclusion, there is limited evidence that UVR exposure can reduce the efficacy of
vaccination, at least in some individuals. Clearly, this issue requires further investigation,
particularly with regard to the identification of UV-susceptible groups within a population.
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
The impact of UVR on tumour immunity
There is considerable evidence that UV-induced immunosuppression contributes significantly to
the progression of both melanoma and non-melanoma skin cancers.1 Recently Jans et al.110
demonstrated that prevention of the formation of the most common UV lesion in the skin, CPDs,
also prevented the vast majority of the acute responses in UV-exposed skin and increased the
resistance to UV-induced tumour development. Furthermore, Kuchel et al.143 found that CPD
development is the initiating event for suppression of memory immune responses in human
subjects. This study looked at the effect of UVR exposure on the memory immune response in
individuals who were allergic to nickel. This means that they had already shown a cell-mediated
immune response to nickel in the past and would therefore have an immunological memory of
nickel. When irradiated with solar-simulated UVR and then challenged on the skin with nickel,
the normal cell-mediated response (seen as reddening and inflammation of the skin) was
suppressed. However, if liposomes containing a DNA repair enzyme were applied immediately
after the exposure, the cell-mediated response was not suppressed.
Subjects with the genetic disease XP, in whom there are mutations affecting DNA repair, show
enhanced UV-induced acute inflammation and a high incidence of UV-induced skin cancers, up
to 5000 times that of the general population.144 Application of liposomes containing a DNA
repair enzyme to the exposed skin leads to a decrease in the rate of newly occurring actinic
keratoses (precursors of SCC) and skin cancers compared with placebo145 Mice with different
genetic defects in nucleotide excision repair (used as animal models of XP disease) have been
investigated to determine further the effect of DNA repair on UV-induced local
immunosuppression.146 In another example, transgenic mice with a defect in one form of
nucleotide excision repair have been used to demonstrate that tumour cells, derived from a
murine UV-B-induced SCC, first develop into tumours following subcutaneous injection, and
then are subsequently rejected in exactly the same fashion as in the wild-type.147 However, if
the transgenic and wild-type mice were UV-B exposed prior to the tumour cell inoculation, the
tumours were rejected in 40% of the transgenic mice, as compared to 96% rejection in the wildtype mice. It was concluded that this immune-mediated impairment in tumour rejection, induced
by the lack of repair of the DNA damage following the UV exposure, could contribute
significantly to skin cancer development in XP patients. This work on XP represents further
compelling evidence that the immunosuppression caused by UVR can be a crucial factor in the
generation of skin cancers.
Vitamin D
Although exposure to solar UVR has many adverse health effects in human populations, one
very beneficial effect is its contribution to vitamin D status. The vitamin D status of an
individual is based on measuring the serum or plasma concentration of 25-hydroxyvitamin D
[25(OH)D]. The active form of vitamin D, 1,25-dihydroxyvitamin D [1,25(OH)2D] is
synthesised in the final step of the metabolic pathway. The levels of 1,25(OH)2D are maintained
even when 25(OH)D levels become sub-optimal. Currently the serum levels of 25(OH)D
considered excessive, sufficient, insufficient and deficient are >250, 50-250, 25-50 and <25
nmol/L respectively.148-150 These values are the topic of continuing discussion. For example, a
recent report indicates that the most advantageous serum concentration of 25(OH)D for a number
of health endpoints begins at 75 nmol/L with the optimum between 90-100 nmol/L.151 For most
people, more than 90% of their vitamin D requirement is acquired from exposure to solar UVR.
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An action spectrum for vitamin D formation in human skin indicates that synthesis occurs most
effectively following exposure to the UV-B waveband.152 As solar UV-B is reduced to almost
zero in the winter months at latitudes above 500 North or South153, vitamin D status can vary
greatly with season and location. Various surveys have provided evidence that many
individuals, even those living in countries with high solar UVR154, may have inadequate vitamin
D status.155-159 Because of its ability to absorb UV-B, melanin in the skin can also decrease
vitamin D status although, with sufficient UV-B, adequate vitamin D status can be achieved.160
As an example of the effect that skin pigmentation can have on vitamin D production, 42% of
Black American women were considered 25(OH)D-deficient compared with 4.2% of white
women in a recent survey.161
Vitamin D was identified almost one hundred years ago, and the link between sunlight exposure
and childhood rickets proposed about four hundred years ago. Vitamin D is a very important
hormone for many aspects of general health. It plays a major role in the growth, development
and maintenance of bone, with deficits leading to low bone mineral density resulting in an
increased risk of osteoporosis and fractures in adults and rickets in children. However adequate
vitamin D status is now implicated in the prevention of an increasing list of non-skeletal
disorders including several internal cancers and autoimmune diseases, and hypertension.
1,25(OH)2D most commonly acts as a factor that stimulates cell differentiation and cell death.
Immune effects
Following the discovery of vitamin D receptors (VDRs) on several populations of immune cells,
it is now known that vitamin D status can affect the immune system by suppressing T-cell
proliferation, down-regulating antigen presentation, stimulating the generation of Treg cells and
Th2 cells, and activating macrophage function (reviewed in Mathieu et al.162 Indeed, once it
became known that 1,25(OH)2D3 can be synthesised in the skin following UVR, it has been
suggested as a mediator of UV-induced immunosuppression. One illustration of this aspect is its
inhibitory effects on the ability of Langerhans cells (which form a dendritic cell network in the
outermost layers of the skin and survey the skin for any foreign challenges) to present
antigens.163
Cancer
The most persuasive evidence to date suggesting a protective role for vitamin D in human
disease relates to some internal cancers. Most information is available for colon, breast, prostate
and ovarian tumours. Recently Garland et al.164 undertook a review of relevant epidemiological
studies and concluded that 20 out of 30 studies on colon cancer, 9 out of 13 on breast cancer, 13
out of 26 on prostate cancer and 5 out of 7 on ovarian cancer reported a significant benefit of
vitamin D, its serum metabolites, sunlight exposure or another marker of vitamin D status on
cancer risk or mortality. The other studies demonstrated a favourable trend (of borderline
significance) or no association with vitamin D or its markers. A second recent review found a
significant inverse correlation between sunlight exposure and the incidence or mortality of
prostate, ovary and colon cancers with the data on non-Hodgkin lymphoma giving conflicting
results.165 Vitamin D might provide a protective effect by controlling cell proliferation, inducing
terminal differentiation of tumour cells and inhibiting angiogenesis. There are many VDR
polymorphisms, and only particular genotypes of VDR in combination with low 25(OH)D levels
may correlate with the increased risk of cancer or metastasis. Notably one large longitudinal
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
case-control study in the Nordic countries found that the risk of prostate cancer was greatest in
two groups: those men with a low serum 25(OH)D (below 19 nmol/L) and those with a high
serum 25(OH)D (above 80 nmol/L).166 In addition, the results of a very recent large randomised
double-blind placebo-controlled trial taking place in post-menopausal women showed that the
incidence of colorectal cancer in the 18,176 individuals assigned to receive calcium carbonate
plus vitamin D3 (400 IU) daily was no different from the 18,106 individuals assigned to the
placebo group.167 This finding has been criticised as the daily dose of vitamin D taken by the
subjects was lower than that recommended by some experts.168, 169 Furthermore a meta-analysis
of 44 observational studies of either prospective (cohort) or retrospective (case-control) design
concluded that individuals taking >1000 IU/day oral vitamin D or with >82 nmol/L serum
25(OH)D had 50% lower incidence of colorectal cancer compared with reference values.170 In
addition to vitamin D status, consideration of calcium status may be of crucial importance in the
prevention of internal cancers, as has been demonstrated for colorectal adenomas.171
The majority of the epidemiological studies linking low UV exposures to higher incidence of
internal cancers used latitude as a surrogate for exposure rather than measuring personal UV
dose. However, several reports have now tried to include a personal estimation of sun exposure.
In a case-control Australian survey, the risk of non-Hodgkin lymphoma fell with increasing solar
irradiation, as assessed via a self-administered questionnaire and telephone interview.172 As
already noted in a previous section, Berwick et al.45 reported that, following the diagnosis of
early stage cutaneous melanoma, sun exposure was associated with increased survival rates over
an average of a 5-year period. The irradiation was assessed by personal interview and a review
of histopathological parameters, such as solar elastosis. Rukin et al.173 assessed various
parameters regarding past sun exposure, via a questionnaire, that might affect susceptibility to
prostate cancer: in men with very low UV exposure, polymorphisms in particular subregions of
the VDR gene were associated with risk. The difficulties of accurately estimating past personal
UV exposure have already been indicated in this report. The finding of a significant protective
effect is thus of some importance. Furthermore the inclusion of objective measures of past sun
exposure such as solar elastosis provides further weight to this conclusion.
No studies in
animals have attempted to assess a protective role for solar UV exposure in internal cancer
development, although several such studies have shown that vitamin D has activity against
tumour proliferation and metastasis (reviewed in Giovannucci174).
Autoimmune diseases
As discussed above for the internal cancers, a protective role for vitamin D status is postulated
for some autoimmune diseases, namely multiple sclerosis (MS), diabetes mellitus type 1,
rheumatoid arthritis (RA) and inflammatory bowel diseases (IBDs). A brief overview of each is
given below.
MS is an autoimmune disease in which an overactive Th1 cytokine response to an unidentified
antigen stimulates an immune attack on myelin in the central nervous system. Initial
epidemiological studies in human populations using latitude as a surrogate for solar UV
exposure175 and experimental studies in a mouse model of MS (experimental allergic
encephalomyelitis, EAE)176 support the view that there is a link between poor vitamin D status,
due to low sunlight exposure, and MS incidence. New evidence has indicated that increased sun
exposure during ages 6-15 years is associated with a decreased risk of MS.177 In a prospective
cohort study of almost 20,000 nurses in the USA, Munger et al.178 revealed that vitamin D
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supplements (>400IU/day vs. nil) after the age of 25 was inversely associated with MS onset
(40% decrease in risk). Also a record linkage study of skin cancer and MS has revealed that skin
cancer incidence is significantly less common in MS patients than in those patients with other
autoimmune or neurological diseases.179 It is postulated that 1,25(OH)2D could act by
suppressing Th1 function while concurrently increasing Treg and Th2 activities, thus helping to
reduce the risk of MS development. However, in one of the few animal model studies to date in
which UVR was incorporated, UV exposure induced progressive disease in some mice that had
already developed the relapsing-remitting form of EAE.180 It was shown that systemic
immunosuppression had resulted from the UVR. These findings were explained by suggesting
that Th1 responses contribute to disease onset while Th2 responses that are promoted by UVR
may be more important in disease progression. It should be noted that in most of the mouse
studies of EAE, 1,25(OH)2D3 was added to the diet rather than vitamin D3, the metabolite formed
in the skin after UV exposure, and calcium supplementation was also provided. A recent paper
reports that dietary vitamin D3 provided protection from the development of EAE in female
mice, but not in ovariectomised female mice or in male mice.181 Thus a complex relationship
between vitamin D and female hormones may be indicated.
For type 1 diabetes, epidemiological studies show increased incidence at higher latitude, the
converse to skin cancer incidence. Added to this, convincing evidence from models of nonobese diabetic mice demonstrates that vitamin D deficiency in early life accelerates the
appearance of the disease.182 A birth-cohort study in Finland indicated that regular vitamin D
intake in early childhood reduced the risk of type 1 diabetes development in later life.183 Two
other reports show the protective effects of vitamin D or cod-liver oil (rich in vitamin D) in type
1 diabetes.184, 185 No studies have attempted to relate individual solar UVR dose with type 1
diabetes in humans or animal models thus far.
Unlike MS and type 1 diabetes, the incidence of rheumatoid arthritis (RA) does not correlate
convincingly with latitude.186 However, a prospective large-scale study has revealed an inverse
association between vitamin D intake and RA.187 As the symptoms of RA are largely due to the
overactivity of the Th1 cytokines, especially tumour necrosis factor-α, low levels of 1,25(OH)2D
may not be sufficient to suppress this imbalance.
Inflammatory bowel diseases (IBDs) have an unknown aetiology but are immune-mediated and
consist of at least two forms, ulcerative colitis and Crohn disease. A mouse model in which the
VDRs are not expressed has been used to illustrate the importance of vitamin D for the
maintenance of normal immune responses in the gastro-intestinal tract.188 In another mouse
model, 1,25(OH)2D3 prevented and ameliorated the symptoms of IBD.189 Therefore it is possible
that a vitamin D deficiency may lead to a lack of suppression of the enhanced Th1 cytokine
responses that are typical of IBDs in humans. The role of sunlight in IBD has not been examined
experimentally, although it is known that IBDs have a complex aetiology involving
environmental factors and are most prevalent in higher latitudes where exposure to solar UVR is
reduced compared with lower latitudes.
In conclusion, for the human autoimmune diseases, MS, type 1 diabetes, RA and IBDs, there is
growing, although still not definitive, evidence to associate low solar UVR exposure and/or
vitamin D with occurrence. Recent cohort studies have indicated convincingly that poor vitamin
D status can be prospectively associated with the onset of the first three of these diseases
(reviewed in Ponsonby et al.190). However, it is possible that another factor, apart from vitamin
D, which is also linked with sun exposure, may be involved in modulating immune responses.
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
Suggested factors include the UV-induced release of the neuropeptides, α-melanocyticstimulating hormone and calcitonin-gene related peptide, or the light-induced suppression of
melatonin levels.190
As a further indication of how complicated and confusing the links are between vitamin D
deficiency and an increased risk of certain autoimmune diseases, there appear to be certain
subsets of patient populations in whom the production of 1,25(OH)2D3 is increased.191-193 In
those with Crohn disease, the elevated 1,25(OH)2D3 is associated with low bone density and
active disease which Abreu et al.193 suggest may arise from inflammation occurring in the
intestinal tract. In patients with sarcoidosis, elevated vitamin D was seen more frequently in
those with extrathoracic involvement, a more serious form of the disease.192
Infectious diseases
Few studies to date have considered vitamin D in the context of infectious diseases, although
Cantorna et al.189 found that the susceptibility of mice to infection with HSV or the yeast
Candida albicans was not affected by 1,25(OH)2D3 given in the diet. However, historically
vitamin D has been used to treat tuberculosis and there is more recent evidence that 1,25(OH)2D3
can activate anti-mycobacterial activity in a murine model194 and in cattle infected with
Mycobacterium bovis.195 An explanation of how this mechanism might operate has been
provided using a mycobacterial model system. It has been shown that the activation of Toll-like
receptors on human macrophages by mycobacterial lipopeptides leads to the up-regulation of the
VDRs and vitamin D hydroxylase genes, resulting in the activation of the macrophages and the
killing of the intracellular bacteria.196 Several surveys have shown that, in temperate climates,
the incidence of tuberculosis is higher in human subjects with low serum 25(OH)D levels197, and
a recent study involving foreign-born people living in London concluded that 25(OH)D
deficiency correlated with tuberculosis amongst all ethnic groups, except white Europeans and
Chinese/South Asians.198 The lack of solar UVR exposure is likely to contribute to the low
levels of vitamin D, but poor dietary intake may be important and particular VDR
polymorphisms may provide a genetic risk factor for some ethnic groups. An interesting recent
review suggests the hypothesis that the occurrence of epidemic influenza predominantly in the
winter months might be explained by the seasonal deficiency in vitamin D, leading to a
significant reduction in several anti-viral immune mechanisms.199
Safety of response strategies
Response strategies to deal with the problems arising from ozone depletion can be divided into
those that are directed at restoring the appropriate level of ozone in the stratosphere by replacing
ozone depleting substances (ODSs) with alternative chemicals, and those that are directed at
protecting individuals from the increased solar UV-B arising from ozone depletion. Both
strategies may have unintended consequences for human health. The sections below will
summarize the safety aspects associated with the development and use of ODS replacement
chemicals and then will discuss some of the issues associated with various personal protection
strategies for the eye and the skin.
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ODS replacement chemicals
Much of the safety testing of many of the substitutes for ODSs, for example HCFC-124, HFC134a and HFC-227, continues to find low toxicity in humans and animals.200, 201 However, there
has been an increasing number of reports indicating that use or exposure to HCFC-123, in
particular in occupationally exposed populations, can be associated with liver toxicity.202-204 As
the number of chemicals being proposed as replacements for ODSs is steadily increasing (EPA
2004, available at www.epa.gov/ozone/snap), it will be important to monitor their use for
adverse events. This is particularly true for those chemicals that have seen limited use in the past
and for which exposure and toxicity information is limited.
Personal protection strategies
Many of the protective strategies against excessive exposure to sunlight have been developed
and advocated by those concerned about the effects of UVR on the skin. The first step towards
protection from any toxic agent is to be aware that the hazard exists. The general advice to seek
shade has become a keynote slogan for those involved in sun safety; this has been an effective
addendum to the popular Australian slip, slap, slop campaign (now modified by New Zealand to
be slip, slap, slop and wrap). The equivalent programme in the USA is called SunWise and it
seeks to teach the public, especially children, how to protect themselves from overexposure to
the sun (http://epa.gov.sunwise/).
Most public health pamphlets now include a reference to the need for hats and sunglasses. Wide
brimmed (>10 cm) hats are recommended for head and eye protection and can reduce ocular
exposure by up to 50%.205 Protection from side-angles of UVR is often provided by the hood of
a jacket and similar headwear. Although, as discussed above, there have been concerns that
under-exposure to UV-B may impair vitamin D status, one recommendation suggests that 10-15
minutes per day in sunlight in the summer months should be sufficient to maintain adequate
vitamin D status for most individuals.164 This dose relates to white-skinned people living in
countries such as north-west Europe and the USA, with exposure on unprotected skin. It should
be modified considerably for those living at high or low latitude, for the season of the year and
for immigrants with darker skin colour. In addition age, type of clothing, diet, whether the work
place is in- or out-doors and the social environment are all important variables in determining
how much ambient UVR exposure is optimal. One recent study illustrates the complexity of
estimating recommended UV exposure times for the Australian population, and concludes that a
single simple message for the general public is not possible.206
The skin and eye normally have some defences against oxidative and photo-induced damage.
These include pigments such as melanin, antioxidant enzymes such as superoxide dismutase and
catalase, and antioxidants such as vitamins C and E, lutein, β-carotene and other carotenoids, and
glutathione. Many of these defences begin to diminish after 40 years of age resulting in less
protection from radiation-induced damage to various structures of the eye.207 The use of
antioxidants, free radical scavengers and trace minerals, principally via the diet, appear to be
effective in reducing the immunosuppressive effects of UVR as well as UV-B induced skin
carcinogenesis208; no evidence was found of a similar effect for cataract or other UV-B-related
ocular diseases. However, recent clinical and experimental data suggest that modifying a
person’s antioxidant status via supplementation may require extreme caution as the antioxidant
defence system is complex and intricately balanced, and altering it may actually make the
carcinogenic impact of UV worse.208
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Protection specific to the eye. The eye is located in the bony orbit, and the forehead, eyebrows,
lids and eyelashes provide considerable protection from overhead solar irradiance.209 This
explains why solar exposure at levels that should produce corneal damage within minutes, if the
exposure were directly onto the cornea, does not do so. The need to protect ocular tissues from
excessive exposure to UVR using appropriate absorptive glass and plastic materials is generally
accepted and well understood.210, 211 Plastic lenses absorb up to about 350 nm and most high
refractive index plastic (including polycarbonate) and glass lenses absorb even more UV-A.
Thus, even clear spectacle lenses provide protection from UV-B. However, in the case of nonwrap around spectacles there is potential for ambient UVR to enter the eye from the side. This
effect can be exacerbated by tinted sunglass lenses, which provoke a wider opening of the eye.
This is particularly significant for the potential exposure of the crystalline lens from peripheral
rays. Dose estimate factors have been proposed for the efficacy of a wide range of forms of eye
protection, i.e., from ordinary glass spectacles to highly protective ski goggles.210
Most early contact lens materials, other than fluorosilicone acrylate, provided little protection
from UVR. As a result, rigid and soft contact lenses have now been developed which offer
various levels of protection from UVR. Consideration of the optical absorption characteristics of
a given lens and the related protection factors may be used to predict the protection afforded by a
given lens. This has been confirmed by Walsh et al.212 using modelled and measured data under
high levels of solar UVR in the summer months in Houston, Texas. Rigid contact lenses provide
no protection for the peripheral cornea or from the effects of peripheral light focussing. On the
other hand, soft contact lenses that cover the entire cornea will protect the eye from UVR
entering from the side or below. Using model eye and mannequin studies, Kwok et al.7 have
demonstrated that UVR-blocking soft contact lenses effectively shield against peripheral corneal
focussing of obliquely incident UVR in the anterior segment of the eye. They also re-emphasise
that many sunglasses do not protect against these rays and that contact lenses would provide
protection when sunglasses are not worn. Sliney210 concluded that UVR-blocking soft contact
lenses provide protection from UV-B equivalent to ski-goggles for the cornea and internal eye
structures.
Protection specific to the skin. Broad spectrum sunscreens are being used increasingly by the
general population to minimise the erythemal effect of high sun exposure. They are generally
effective for that end-point but concerns have been expressed that regular sunscreen usage may
impair cutaneous vitamin D synthesis, if the cream is applied at the correct concentration. While
some reports indicate that sunscreens significantly decrease the production of 25(OH)D and
1,25(OH)2D3 213, others found little effect on the levels of these two substances.214, 215 Farrerons
et al.216 followed two groups of elderly subjects living in Barcelona, one treated with sunscreen
and the other without treatment. The sunscreen users showed a minor decrease in serum
25(OH)D levels in both the summer and winter months compared with the controls, but this
reduction was not sufficient to induce secondary hyperparathyroidism. It should be noted that, in
practice, sunscreen application is frequently problematic with insufficient quantity being used to
achieve the sun protection factor rated, or the spreading being non-uniform resulting in some
skin sites getting little or no protection, or to some being washed or towelled off.217, 218
Efforts have been made to define sunscreens in terms of their ability to protect against UVinduced immunosuppression. The immune protection factor (IPF) has been developed in an
attempt to compare one preparation with another219 The IPF is defined as the ratio of UV doses
influencing a particular immunological end-point in the presence or in the absence of the
46
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
sunscreen. Using delayed hypersensitivity as an example, several reports indicate that
sunscreens that absorb the UV-A waveband offer the most effective immunoprotection
(reviewed in 220). Of course, protection against the immune effects of solar UVR might not be
beneficial if consideration of protection against selected internal cancers, autoimmune and
infectious diseases is taken into consideration. Apart from sunscreens, there is considerable
interest currently in identifying dietary constituents that could protect the skin’s immune system
against UV damage.221, 222
Some concerns have arisen about unintended consequences from the increased use of sunscreens
to protect against UV-B. A number of the UV-B absorbing components in sunscreens have been
shown to have weak estrogenic activity so may have adverse consequences for reproductive
function in human and animal populations in the environment, lending strength to the
recommendation that protection from UV-B should not rely solely on sunscreen use.223-230 As
discussed above, there are many protective strategies for the skin that do not have unintended
consequences for the environment. These include staying indoors, wearing clothing that covers
sun-exposed areas of the body during conditions of high ambient UVR or seeking shade during
the middle hours of the day although this will provide partial protection only.
Possible interactions between climate change and ozone depletion
If the predicted higher ambient temperatures in summer due to global warming are combined
with drier weather, people living in mid-latitudes may spend more time outdoors, thus increasing
their solar UV exposure. Indeed, it has been shown, at least in schoolchildren in the UK, that
climate and ambient temperature influence behaviour and hence sun exposure more than ambient
solar UV.217 While such behavioural adaptation may have benefits in terms of vitamin D
synthesis, the impact on skin cancer incidence and other health aspects of solar UVR are
predicted to be adverse. There is also the possibility that climate change may result in wetter
weather with more individuals staying indoors. Also, there would be regional differences in
behavioural responses to warming.
In the previous Report (UNEP 2002, published in de Gruijl et al.1) the possibility that rising
temperatures due to global warming might enhance the induction of skin cancer by solar UVR
was considered. This suggestion was based on experiments in mice performed many years
ago.231, 232 As the process of UV-carcinogenesis is similar in mice and humans, rising
temperatures could have a similar impact on skin cancers in humans, but the effect might be
quantitatively different. Data on the influence of temperature on UV-carcinogenesis in human
populations are not available but it is possible to investigate skin cancer incidence in people of
similar skin colour living at different altitudes.233 An attempt was made to find some indication
from existing results: the incidence of NMSC in fair-skinned males and females in 10 different,
well distributed regions of continental USA, collected in the Third National Cancer Survey234,
has already been compared with UV-B measurements in the same region. In the new analysis,
temperature data for these regions were added (van der Leun et al. personal communication). It
was discovered that there was a similar trend to that in the mouse experiments towards a higher
incidence of NMSC at relatively high temperatures compared with relatively lower temperatures.
These preliminary results on human skin cancer reinforce the suggestion that the interaction of
temperature and solar UV radiation may become an important health effect due to climate
change. In addition it should be noted that, following the work of Sasaki et al.235, higher ambient
The Environmental Effects Assessment Panel Report for 2006
47
Effects on human health from stratospheric ozone depletion and its interactions with climate change
temperatures as a result of global climate change may interact with UVR exposure to further
increase the risk of nuclear cataract development.
As temperatures increase, changes in the quality and quantity of pest infestations are likely to
require the increased use of pesticides. There are recent reports that exposure to certain
pesticides can result in immunosuppression, and, in the case of permethrin, that such
immunosuppression236 may be additive to that caused by exposure to UV-B.237
Conclusions and gaps in knowledge
In the four years since our last report, considerable progress has taken place regarding the impact
of ozone depletion, and hence of increased solar UV-B, on human health. The mechanisms
whereby UVR interacts with structures in the eye and causes a variety of ocular diseases are
becoming clear, as are details regarding the genetic basis of skin cancers and the pathways
leading to UV-induced immunosuppression. The suggested links between solar UVR exposure,
vitamin D and protection against a variety of internal cancers, autoimmune diseases and infection
require further confirmation. In Table 2, we indicate areas where crucial knowledge is lacking.
Despite the distinct possibility that the ozone layer will repair itself in the coming decades, the
general public will still require to maintain vigilance regarding their sunlight exposure. While it
remains fashionable, for example, to have a tanned skin, to wear minimal clothing in hot weather
and to experience holidays in the sun, the risk of overexposure of the white population is high.
The projection of a doubling in the incidence of all three types of skin cancer in the next ten
years, plus a large increase in the number of cataracts, due partly to an ageing population, mean
that health campaigns that stress the harmful effects of solar UVR are required and justified.
However, to maintain sufficient vitamin D levels, the protective measures employed by an
individual should not go to the extreme of minimal or no solar UVR exposure in the summer
months.
Table 2. Suggested current gaps in knowledge regarding solar UVR and human health
Subject
Key questions
The eye
What are the pathogenic mechanisms involved in the cataract types?
What are the wavelength dependencies for cataract development?
What are the associations between UVR and other environmental factors
that contribute to the induction of nuclear cataract in residents of developing
countries?
The skin
What is the action spectrum for induction of melanoma?
Are there any interactions between UV-A and UV-B in the induction of
non-melanoma skin cancer and melanoma?
What are the pathogenic mechanisms underlying infant vs adult UVR
exposure in skin carcinogenesis?
What is the mechanism of the interactions between UV-B and UV-A with
regard to effects on immunity?
48
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
What is the action spectrum for the synthesis of vitamin D3 in pigmented
and unpigmented skin?
How much solar UVR exposure is required, and how should it be distributed
over the year, to maintain adequate vitamin D levels in people of different
skin phototypes living at different latitudes?
Can valid estimates be given to the general public regarding optimal doses
of solar UVR for vitamin D synthesis while reducing the risk of developing
skin cancer?
What is the effect of solar UVR in animal models of auto-immunity and
internal cancers?
Protective
measures
Should the immune protection factors of topical sunscreens be measured
and publicised?
Are there factors in the diet that could give significant protection against the
harmful effects of solar UVR?
Should the UV Index be used and analysed in developing countries, and
should attempts be made to educate the general public regarding its
meaning?
Climate change
interactions
What are the combined effects of solar UVR and temperature on the skin
and the eye?
Will future changes in climate lead to people in mid-latitudes spending more
time outdoors?
References
1
2
3
4
5
6
7
8
de Gruijl FR, Longstreth J, Norval M, Cullen AP, Slaper H, Kripke ML, Takizawa Y, van
der Leun JC, Health effects from stratospheric ozone depletion and interactions with climate
change, Photochem Photobiol Sci, 2003, 2, 16-28.
Longstreth J, de Gruijl FR, Kripke ML, Abseck S, Arnold F, Slaper HI, Velders G,
Takizawa Y, van der Leun JC, Health risks, J Photochem Photobiol B, 1998, 46, 20-39.
Parisi AV, Downs N, Cloud cover and horizontal plane eye damaging solar UV exposures,
Int J Biometeorol, 2004, 49, 130-136.
Parisi AV, Downs N, Variation of the enhanced biologically damaging solar UV due to
clouds, Photochem Photobiol, 2004, 3, 643-647.
Coroneo MT, Muller-Stolzenburg NW, Ho A, Peripheral light focusing by the anterior eye
and the ophthalmohelioses, Ophthalmic Surgery, 1991, 22, 705-711.
Cullen AP, Oriowo OM, Voisin A, Anterior eye focussing of peripheral UV and visible
light albedo., Clin Expl Optom, 1997, 80, 80-86.
Kwok LS, Kuznetsov VA, Ho A, Coroneo MT, Prevention of the adverse photic effects of
peripheral light-focusing using UV-blocking contact lenses, Invest Ophthalmol Vis Sci,
2003, 44, 1501-1507.
Kolozsvari L, Nogradi A, Hopp B, Bor Z, UV absorbance of the human cornea in the 240to 400-nm range, Invest Ophthalmol Vis Sci, 2002, 43, 2165-2168.
The Environmental Effects Assessment Panel Report for 2006
49
Effects on human health from stratospheric ozone depletion and its interactions with climate change
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
50
Di Girolamo N, Coroneo M, Wakefield D, Epidermal growth factor receptor signaling is
partially responsible for the increased matrix metalloproteinase-1 expression in ocular
epithelial cells after UVB radiation, Am. J. Pathol., 2005, 167, 489-503.
Kwok LS, Coroneo MT, A model for pterygium formation, Cornea, 1994, 13, 219-224.
Al Bdour M, Al Latayfeh MM, Risk factors for pterygium in an adult Jordanian population,
Acta Ophthalmol Scand, 2004, 82, 64-67.
Taylor HR, West SK, Rosenthal FS, Munoz B, Newland HS, Emmett EA, Corneal changes
associated with chronic UV irradiation, Arch Ophthalmol, 1989, 107, 1481-1484.
McCarty CA, Fu CL, Taylor HR, Epidemiology of pterygium in Victoria, Australia, Br J
Ophthalmol, 2000, 84, 289-292.
Threlfall TJ, English DR, Sun exposure and pterygium of the eye: a dose-response curve,
Am J Ophthalmol, 1999, 128, 280-287.
Kau HC, Tsai CC, Hsu WM, Liu JH, Wei YH, Genetic polymorphism of hOGG1 and risk
of pterygium in Chinese, Eye, 2004, 18, 635-639.
Reisman D, McFadden JW, Lu G, Loss of heterozygosity and p53 expression in pterygium,
2004, 206, 77-83.
Wang L, Dai W, Lu L, Ultraviolet irradiation-induced K(+) channel activity involving p53
activation in corneal epithelial cells, Oncogene, 2005, 24, 3020-3027.
Sliney DH, Physical factors in cataractogenesis: ambient ultraviolet radiation and
temperature, Invest Ophthalmol Vis Sci, 1986, 27, 781-790.
Schein OD, West S, Munoz B, Vitale S, Maguire M, Taylor HR, Bressler NM, Cortical
lenticular opacification: Distribution and location in a longitudinal study, Invest Ophthalmol
Vis Sci, 1994, 35, 363-366.
Elliott DB, Yang KC, Dumbleton K, Cullen AP, Ultraviolet-induced lenticular fluorescence:
intraocular straylight affecting visual function, Vision Res, 1993, 33, 1827-1833.
van Best JA, Van Delft JL, Keunen JE, Long term follow-up of lenticular autofluorescence
and transmittance in healthy volunteers, Exp. Eye Res., 1998, 66, 117-123.
Oriowo OM, Robinson BE, The epidemiology associated with ultraviolet radiation. A
current review, Canadian J Optometry, 1996, 58, 26-33.
Dolin PJ, Ultraviolet radiation and cataract: a review of the epidemiological evidence, Br J
Ophthalmol, 1994, 78, 478-482.
WHO, Environmental Health Criteria 160: Ultraviolet radiation., World Health
Organization Report No., Geneva
Taylor HR, West SK, Rosenthal FS, Munoz B, Newland HS, Abbey H, Emmett EA, Effect
of ultraviolet radiation on cataract formation, N Engl J Med, 1988, 319, 1429-1433.
West SK, Longstreth JD, Munoz BE, Pitcher HM, Duncan DD, Model of risk of cortical
cataract in the US population with exposure to increased ultraviolet radiation due to
stratospheric ozone depletion, Am J Epidemiol, 2005, 162, 1080-1088.
Orr P, Barron Y, Schein OD, Rubin GS, West SK, Eye care utilization by older Americans:
the SEE Project. Salisbury Eye Evaluation, Ophthalmology, 1999, 106, 904-909.
Lucas R, McMichael AJ, Armstrong B, Smith W, Solar ultraviolet radiation. The global
burden of disease due to UVR exposure. Environmental Burden of Disease Series No 13,
World Health Organization Report No., Geneva, 2006
Hayashi LC, Hayashi S, Yamaoka K, Tamiya N, Chikuda M, Yano E, Ultraviolet B
exposure and type of lens opacity in ophthalmic patients in Japan, Sci. Tot. Environ., 2003,
302, 53-62.
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
30 Neale RE, Purdie JL, Hirst LW, Green AC, Sun exposure as a risk factor for nuclear
cataract, Epidemiology, 2003, 14, 707-712.
31 Dong X, Ayala M, Lofgren S, Soderberg PG, Ultraviolet radiation-induced cataract: age and
maximum acceptable dose, Invest Ophthalmol Vis Sci, 2003, 44, 1150-1154.
32 Hall HI, Saraiya M, Thompson T, Hartman A, Glanz K, Rimer B, Correlates of sunburn
experiences among U.S. adults: results of the 2000 National Health Interview Survey,
Public Health Rep, 2003, 118, 540-549.
33 de Vries E, van de Poll-Franse LV, Louwman WJ, de Gruijl FR, Coebergh JW, Predictions
of skin cancer incidence in the Netherlands up to 2015, Br J Dermatol, 2005, 152, 481-488.
34 Bauer J, Buttner P, Wiecker TS, Luther H, Garbe C, Risk factors of incident melanocytic
nevi: a longitudinal study in a cohort of 1,232 young German children, Int J Cancer, 2005,
115, 121-126.
35 Jhappan C, Noonan FP, Merlino G, Ultraviolet radiation and cutaneous malignant
melanoma, Oncogene, 2003, 22, 3099-3112.
36 de Gruijl FR, van Kranen HJ, van Schanke A, UV exposure, genetic targets in melanocytic
tumors and transgenic mouse models, Photochem Photobiol, 2005, 81, 52-64.
37 Marks R, The changing incidence and mortality of melanoma in Australia, Recent Results
Cancer Res, 2002, 160, 113-121.
38 Cayuela A, Rodriguez-Dominguez S, Lapetra-Peralta J, Conejo-Mir JS, Has mortality from
malignant melanoma stopped rising in Spain? Analysis of trends between 1975 and 2001,
Br J Dermatol, 2005, 152, 997-1000.
39 Stang A, Pukkala E, Sankila R, Soderman B, Hakulinen T, Time trend analysis of the skin
melanoma incidence of Finland from 1953 through 2003 including 16,414 cases, Int J
Cancer, 2006, 119, 380-384.
40 Ulmer MJ, Tonita JM, Hull PR, Trends in invasive cutaneous melanoma in Saskatchewan
1970-1999, J Cutan Med Surg, 2003, 7, 433-442.
41 de Vries E, Bray FI, Eggermont AM, Coebergh JW, Monitoring stage-specific trends in
melanoma incidence across Europe reveals the need for more complete information on
diagnostic characteristics, Eur J Cancer Prev, 2004, 13, 387-395.
42 Coory M, Baade P, Aitken J, Smithers M, McLeod GR, Ring I, Trends for in situ and
invasive melanoma in Queensland, Australia, 1982-2002, Cancer Causes Control, 2006, 17,
21-27.
43 Purdue MP, From L, Armstrong BK, Kricker A, Gallagher RP, McLaughlin JR, Klar NS,
Marrett LD, Etiologic and other factors predicting nevus-associated cutaneous malignant
melanoma, Cancer Epidemiol Biomarkers Prev, 2005, 14, 2015-2022.
44 Strouse JJ, Fears TR, Tucker MA, Wayne AS, Pediatric melanoma: risk factor and survival
analysis of the surveillance, epidemiology and end results database, J Clin Oncol, 2005, 23,
4735-4741.
45 Berwick M, Armstrong BK, Ben-Porat L, Fine J, Kricker A, Eberle C, Barnhill R, Sun
exposure and mortality from melanoma, J Natl Cancer Inst, 2005, 97, 195-199.
46 Boniol M, De Vries E, Coebergh JW, Dore JF, Seasonal variation in the occurrence of
cutaneous melanoma in Europe: influence of latitude. An analysis using the EUROCARE
group of registries, Eur J Cancer, 2005, 41, 126-132.
47 Boniol M, Armstrong BK, Dore JF, Variation in incidence and fatality of melanoma by
season of diagnosis in New South Wales, Australia, Cancer Epidemiol Biomarkers Prev,
2006, 15, 524-526.
The Environmental Effects Assessment Panel Report for 2006
51
Effects on human health from stratospheric ozone depletion and its interactions with climate change
48 Gandini S, Sera F, Cattaruzza MS, Pasquini P, Picconi O, Boyle P, Melchi CF, Metaanalysis of risk factors for cutaneous melanoma: II. Sun exposure, Eur J Cancer, 2005, 41,
45-60.
49 Agredano YZ, Chan JL, Kimball RC, Kimball AB, Accessibility to air travel correlates
strongly with increasing melanoma incidence, Melanoma Res, 2006, 16, 77-81.
50 Berwick M, Wiggins C, The current epidemiology of cutaneous malignant melanoma, Front
Biosci, 2006, 11, 1244-1254.
51 Landi MT, Kanetsky PA, Tsang S, Gold B, Munroe D, Rebbeck T, Swoyer J, TerMinassian M, Hedayati M, Grossman L, Goldstein AM, Calista D, Pfeiffer RM, MC1R,
ASIP, and DNA repair in sporadic and familial melanoma in a Mediterranean population, J
Natl Cancer Inst, 2005, 97, 998-1007.
52 Sturm RA, Skin colour and skin cancer - MC1R, the genetic link, Melanoma Res, 2002, 12,
405-416.
53 Jannot AS, Meziani R, Bertrand G, Gerard B, Descamps V, Archimbaud A, Picard C,
Ollivaud L, Basset-Seguin N, Kerob D, Lanternier G, Lebbe C, Saiag P, Crickx B, ClergetDarpoux F, Grandchamp B, Soufir N, Melan C, Allele variations in the OCA2 gene (pinkeyed-dilution locus) are associated with genetic susceptibility to melanoma, Eur J Hum
Genet, 2005, 13, 913-920.
54 Gillanders E, Juo SH, Holland EA, Jones M, Nancarrow D, Freas-Lutz D, Sood R, Park N,
Faruque M, Markey C, Kefford RF, Palmer J, Bergman W, Bishop DT, Tucker MA,
Bressac-de Paillerets B, Hansson J, Stark M, Gruis N, Bishop JN, Goldstein AM, BaileyWilson JE, Mann GJ, Hayward N, Trent J, Localization of a novel melanoma susceptibility
locus to 1p22, Am J Hum Genet, 2003, 73, 301-313.
55 Baccarelli A, Calista D, Minghetti P, Marinelli B, Albetti B, Tseng T, Hedayati M,
Grossman L, Landi G, Struewing JP, Landi MT, XPD gene polymorphism and host
characteristics in the association with cutaneous malignant melanoma risk, Br J Cancer,
2004, 90, 497-502.
56 Han J, Colditz GA, Samson LD, Hunter DJ, Polymorphisms in DNA double-strand break
repair genes and skin cancer risk, Cancer Res, 2004, 64, 3009-3013.
57 Lovatt T, Alldersea J, Lear JT, Hoban PR, Ramachandran S, Fryer AA, Smith AG, Strange
RC, Polymorphism in the nuclear excision repair gene. ERCC2/XPD: association between
an exon 6-exon 10 haplotype and susceptibility to cutaneous basal cell carcinoma, Hum
Mutat, 2005, 25, 353-359.
58 Blankenburg S, Konig IR, Moessner R, Laspe P, Thoms KM, Krueger U, Khan SG,
Westphal G, Berking C, Volkenandt M, Reich K, Neumann C, Ziegler A, Kraemer KH,
Emmert S, Assessment of 3 xeroderma pigmentosum group C gene polymorphisms and risk
of cutaneous melanoma: a case-control study, Carcinogenesis, 2005, 26, 1085-1090.
59 Blankenburg S, Konig IR, Moessner R, Laspe P, Thoms KM, Krueger U, Khan SG,
Westphal G, Volkenandt M, Neumann C, Ziegler A, Kraemer KH, Reich K, Emmert S, No
association between three xeroderma pigmentosum group C and one group G gene
polymorphisms and risk of cutaneous melanoma, Eur J Hum Genet, 2005, 13, 253-5.
60 Vogel U, Olsen A, Wallin H, Overvad K, Tjonneland A, Nexo BA, Effect of
polymorphisms in XPD, RAI, ASE-1 and ERCC1 on the risk of basal cell carcinoma among
Caucasians after age 50, Cancer Detect Prev, 2005, 29, 209-214.
61 Millikan RC, Hummer A, Begg C, Player J, de Cotret AR, Winkel S, Mohrenweiser H,
Thomas N, Armstrong B, Kricker A, Marrett LD, Gruber SB, Culver HA, Zanetti R,
52
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
Gallagher RP, Dwyer T, Rebbeck TR, Busam K, From L, Mujumdar U, Berwick M,
Polymorphisms in nucleotide excision repair genes and risk of multiple primary melanoma:
the Genes Environment and Melanoma Study, Carcinogenesis, 2006, 27, 610-618.
Nofsinger JB, Liu Y, Simon JD, Aggregation of eumelanin mitigates photogeneration of
reactive oxygen species, Free Radic Biol Med, 2002, 32, 720-730.
Maresca V, Flori E, Briganti S, Camera E, Cario-Andre M, Taieb A, Picardo M, UVAinduced modification of catalase charge properties in the epidermis is correlated with the
skin phototype, J Invest Dermatol, 2006, 126, 182-190.
Pavel S, Smit NP, van der Meulen H, Kolb RM, de Groot AJ, van der Velden PA, Gruis
NA, Bergman W, Homozygous germline mutation of CDKN2A/p16 and glucose-6phosphate dehydrogenase deficiency in a multiple melanoma case, Melanoma Res, 2003,
13, 171-178.
Sander CS, Hamm F, Elsner P, Thiele JJ, Oxidative stress in malignant melanoma and nonmelanoma skin cancer, Br J Dermatol, 2003, 148, 913-922.
Pavel S, van Nieuwpoort F, van der Meulen H, Out C, Pizinger K, Cetkovska P, Smit NP,
Koerten HK, Disturbed melanin synthesis and chronic oxidative stress in dysplastic naevi,
Eur J Cancer, 2004, 40, 1423-1430.
Li C, Liu Z, Wang LE, Strom SS, Lee JE, Gershenwald JE, Ross MI, Mansfield PF,
Cormier JN, Prieto VG, Duvic M, Grimm EA, Wei Q, Genetic variants of the ADPRT,
XRCC1, and APE1 genes and risk of cutaneous melanoma, Carcinogenesis, 2006, 27,
1894-1901.
Curtin JA, Fridlyand J, Kageshita T, Patel HN, Busam KJ, Kutzner H, Cho KH, Aiba S,
Brocker EB, LeBoit PE, Pinkel D, Bastian BC, Distinct sets of genetic alterations in
melanoma, N Engl J Med, 2005, 353, 2135-2147.
Maldonado JL, Fridlyand J, Patel H, Jain AN, Busam K, Kageshita T, Ono T, Albertson
DG, Pinkel D, Bastian BC, Determinants of BRAF mutations in primary melanomas, J Natl
Cancer Inst, 2003, 95, 1878-1890.
Pollock PM, Harper UL, Hansen KS, Yudt LM, Stark M, Robbins CM, Moses TY,
Hostetter G, Wagner U, Kakareka J, Salem G, Pohida T, Heenan P, Duray P, Kallioniemi O,
Hayward NK, Trent JM, Meltzer PS, High frequency of BRAF mutations in nevi, Nat
Genet, 2003, 33, 19-20.
Bennett DC, Human melanocyte senescence and melanoma susceptibility genes, Oncogene,
2003, 22, 3063-3069.
Michaloglou C, Vredeveld LC, Soengas MS, Denoyelle C, Kuilman T, van der Horst CM,
Majoor DM, Shay JW, Mooi WJ, Peeper DS, BRAFE600-associated senescence-like cell
cycle arrest of human naevi, Nature, 2005, 436, 720-724.
Noonan FP, Recio JA, Takayama H, Duray P, Anver MR, Rush WL, De Fabo EC, Merlino
G, Neonatal sunburn and melanoma in mice, Nature, 2001, 413, 271-272.
Hacker E, Irwin N, Muller HK, Powell MB, Kay G, Hayward N, Walker G, Neonatal
ultraviolet radiation exposure is critical for malignant melanoma induction in pigmented
Tpras transgenic mice, J Invest Dermatol, 2005, 125, 1074-1077.
De Fabo EC, Noonan FP, Fears T, Merlino G, Ultraviolet B but not ultraviolet A radiation
initiates melanoma, Cancer Res, 2004, 64, 6372-6376.
Robinson ES, Hill RH, Jr., Kripke ML, Setlow RB, The Monodelphis melanoma model:
initial report on large ultraviolet A exposures of suckling young, Photochem Photobiol,
2000, 71, 743-746.
The Environmental Effects Assessment Panel Report for 2006
53
Effects on human health from stratospheric ozone depletion and its interactions with climate change
77 Setlow RB, Grist E, Thompson K, Woodhead AD, Wavelengths effective in induction of
malignant melanoma, Proc Natl Acad Sci U S A, 1993, 90, 6666-6670.
78 Wood SR, Berwick M, Ley RD, Walter RB, Setlow RB, Timmins GS, UV causation of
melanoma in Xiphophorus is dominated by melanin photosensitized oxidant production,
Proc Natl Acad Sci U S A, 2006, 103, 4111-4115.
79 Yamazaki F, Okamoto H, Matsumura Y, Tanaka K, Kunisada T, Horio T, Development of a
new mouse model (xeroderma pigmentosum a-deficient, stem cell factor-transgenic) of
ultraviolet B-induced melanoma, J Invest Dermatol, 2005, 125, 521-525.
80 Kikuchi H, Nishida T, Kurokawa M, Setoyama M, Kisanuki A, Three cases of malignant
melanoma arising on burn scars, J Dermatol, 2003, 30, 617-624.
81 van Schanke A, van Venrooij GM, Jongsma MJ, Banus HA, Mullenders LH, van Kranen
HJ, de Gruijl FR, Induction of nevi and skin tumors in Ink4a/Arf Xpa knockout mice by
neonatal, intermittent, or chronic UVB exposures, Cancer Res, 2006, 66, 2608-2615.
82 van Schanke A, Jongsma MJ, Bisschop R, van Venrooij GM, Rebel H, de Gruijl FR, Single
UVB overexposure stimulates melanocyte proliferation in murine skin, in contrast to
fractionated or UVA-1 exposure, J Invest Dermatol, 2005, 124, 241-247.
83 Overwijk WW, Restifo NP, Autoimmunity and the immunotherapy of cancer: targeting the
"self" to destroy the "other", Crit Rev Immunol, 2000, 20, 433-50.
84 Steitz J, Buchs S, Tormo D, Ferrer A, Wenzel J, Huber C, Wolfel T, Barbacid M,
Malumbres M, Tuting T, Evaluation of genetic melanoma vaccines in cdk4-mutant mice
provides evidence for immunological tolerance against authochthonous melanomas in the
skin, Int J Cancer, 2006, 118, 373-380.
85 Grimbaldeston MA, Pearce AL, Robertson BO, Coventry BJ, Marshman G, Finlay-Jones JJ,
Hart PH, Association between melanoma and dermal mast cell prevalence in sun-unexposed
skin, Br J Dermatol, 2004, 150, 895-903.
86 Synnerstad I, Nilsson L, Fredrikson M, Rosdahl I, Fewer melanocytic nevi found in children
with active atopic dermatitis than in children without dermatitis, Arch Dermatol, 2004, 140,
1471-1475.
87 Zanetti R, Rosso S, Martinez C, Nieto A, Miranda A, Mercier M, Loria DI, Osterlind A,
Greinert R, Navarro C, Fabbrocini G, Barbera C, Sancho-Garnier H, Gafa L, Chiarugi A,
Mossotti R, Comparison of risk patterns in carcinoma and melanoma of the skin in men: a
multi-centre case-case-control study, Br J Cancer, 2006, 94, 743-51.
88 Athas WF, Hunt WC, Key CR, Changes in nonmelanoma skin cancer incidence between
1977-1978 and 1998-1999 in Northcentral New Mexico, Cancer Epidemiol Biomarkers
Prev, 2003, 12, 1105-8.
89 Demers AA, Nugent Z, Mihalcioiu C, Wiseman MC, Kliewer EV, Trends of nonmelanoma
skin cancer from 1960 through 2000 in a Canadian population, J Am Acad Dermatol, 2005,
53, 320-8.
90 Pearce MS, Parker L, Cotterill SJ, Gordon PM, Craft AW, Skin cancer in children and
young adults: 28 years' experience from the Northern Region Young Person's Malignant
Disease Registry, UK, Melanoma Res, 2003, 13, 421-6.
91 Christenson LJ, Borrowman TA, Vachon CM, Tollefson MM, Otley CC, Weaver AL,
Roenigk RK, Incidence of basal cell and squamous cell carcinomas in a population younger
than 40 years, JAMA, 2005, 294, 681-90.
54
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
92 Valery PC, Neale R, Williams G, Pandeya N, Siller G, Green A, The effect of skin
examination surveys on the incidence of basal cell carcinoma in a Queensland community
sample: a 10-year longitudinal study, J Investig Dermatol Symp Proc, 2004, 9, 148-151.
93 Estrada JG, Non-melanoma skin cancer in Catalonia. A community-based prevalence study,
Int J Dermatol, 2005, 44, 922-924.
94 Lewis KG, Weinstock MA, Nonmelanoma skin cancer mortality (1988-2000): the Rhode
Island follow-back study, Arch Dermatol, 2004, 140, 837-842.
95 Yamada M, Udono MU, Hori M, Hirose R, Sato S, Mori T, Nikaido O, Aged human skin
removes UVB-induced pyrimidine dimers from the epidermis more slowly than younger
adult skin in vivo, Arch Dermatol Res, 2006, 297, 294-302.
96 Ashton KJ, Carless MA, Griffiths LR, Cytogenetic alterations in nonmelanoma skin cancer:
a review, Genes Chromosomes Cancer, 2005, 43, 239-348.
97 Han J, Hankinson SE, Colditz GA, Hunter DJ, Genetic variation in XRCC1, sun exposure,
and risk of skin cancer, Br J Cancer, 2004, 91, 1604-9.
98 Fryer AA, Ramsay HM, Lovatt TJ, Jones PW, Hawley CM, Nicol DL, Strange RC, Harden
PN, Polymorphisms in glutathione S-transferases and non-melanoma skin cancer risk in
Australian renal transplant recipients, Carcinogenesis, 2005, 26, 185-191.
99 Besaratinia A, Synold TW, Chen HH, Chang C, Xi B, Riggs AD, Pfeifer GP, DNA lesions
induced by UV A1 and B radiation in human cells: comparative analyses in the overall
genome and in the p53 tumor suppressor gene, Proc Natl Acad Sci U S A, 2005, 102, 1005810063.
100 Kramata P, Lu YP, Lou YR, Singh RN, Kwon SM, Conney AH, Patches of mutant p53immunoreactive epidermal cells induced by chronic UVB Irradiation harbor the same p53
mutations as squamous cell carcinomas in the skin of hairless SKH-1 mice, Cancer Res,
2005, 65, 3577-3585.
101 Backvall H, Stromberg S, Gustafsson A, Asplund A, Sivertsson A, Lundeberg J, Ponten F,
Mutation spectra of epidermal p53 clones adjacent to basal cell carcinoma and squamous
cell carcinoma, Exp Dermatol, 2004, 13, 643-650.
102 Ponten F, Berg C, Ahmadian A, Ren ZP, Nister M, Lundeberg J, Uhlen M, Ponten J,
Molecular pathology in basal cell cancer with p53 as a genetic marker, Oncogene, 1997, 15,
1059-1067.
103 Brash DE, Rudolph JA, Simon JA, Lin A, McKenna GJ, Baden HP, Halperin AJ, Ponten J,
A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma,
Proc Natl Acad Sci U S A, 1991, 88, 10124-10128.
104 Ziegler A, Leffell DJ, Kunala S, Sharma HW, Gailani M, Simon JA, Halperin AJ, Baden
HP, Shapiro PE, Bale AE, et al., Mutation hotspots due to sunlight in the p53 gene of
nonmelanoma skin cancers, Proc Natl Acad Sci U S A, 1993, 90, 4216-4220.
105 Agar NS, Halliday GM, Barnetson RS, Ananthaswamy HN, Wheeler M, Jones AM, The
basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations:
a role for UVA in human skin carcinogenesis, Proc Natl Acad Sci U S A, 2004, 101, 49544959.
106 Pelisson I, Soler C, Chardonnet Y, Euvrard S, Schmitt D, A possible role for human
papillomaviruses and c-myc, c-Ha-ras, and p53 gene alterations in malignant cutaneous
lesions from renal transplant recipients, Cancer Detect Prev, 1996, 20, 20-30.
The Environmental Effects Assessment Panel Report for 2006
55
Effects on human health from stratospheric ozone depletion and its interactions with climate change
107 Reifenberger J, Wolter M, Knobbe CB, Kohler B, Schonicke A, Scharwachter C, Kumar K,
Blaschke B, Ruzicka T, Reifenberger G, Somatic mutations in the PTCH, SMOH, SUFUH
and TP53 genes in sporadic basal cell carcinomas, Br J Dermatol, 2005, 152, 43-51.
108 Strange RC, El-Genidy N, Ramachandran S, Lovatt TJ, Fryer AA, Smith AG, Lear JT,
Wong C, Jones PW, Ichii-Jones F, Hoban PR, Susceptibility to basal cell carcinoma:
associations with PTCH polymorphisms, Ann Hum Genet, 2004, 68, 536-545.
109 Brellier F, Marionnet C, Chevallier-Lagente O, Toftgard R, Mauviel A, Sarasin A,
Magnaldo T, Ultraviolet irradiation represses PATCHED gene transcription in human
epidermal keratinocytes through an activator protein-1-dependent process, Cancer Res,
2004, 64, 2699-2704.
110 Jans J, Schul W, Sert YG, Rijksen Y, Rebel H, Eker AP, Nakajima S, van Steeg H, de Gruijl
FR, Yasui A, Hoeijmakers JH, van der Horst GT, Powerful skin cancer protection by a
CPD-photolyase transgene, Curr Biol, 2005, 15, 105-115.
111 Rebel H, Kram N, Westerman A, Banus S, van Kranen HJ, de Gruijl FR, Relationship
between UV-induced mutant p53 patches and skin tumours, analysed by mutation spectra
and by induction kinetics in various DNA-repair-deficient mice, Carcinogenesis, 2005, 26,
2123-2130.
112 Garinis GA, Mitchell JR, Moorhouse MJ, Hanada K, de Waard H, Vandeputte D, Jans J,
Brand K, Smid M, van der Spek PJ, Hoeijmakers JH, Kanaar R, van der Horst GT,
Transcriptome analysis reveals cyclobutane pyrimidine dimers as a major source of UVinduced DNA breaks, Embo J, 2005, 24, 3952-3962.
113 Kelly GE, Meikle WD, Moore DE, Enhancement of UV-induced skin carcinogenesis by
azathioprine: role of photochemical sensitisation, Photochem Photobiol, 1989, 49, 59-65.
114 Yarosh DB, Pena AV, Nay SL, Canning MT, Brown DA, Calcineurin inhibitors decrease
DNA repair and apoptosis in human keratinocytes following ultraviolet B irradiation, J
Invest Dermatol, 2005, 125, 1020-1025.
115 O'Donovan P, Perrett CM, Zhang X, Montaner B, Xu YZ, Harwood CA, McGregor JM,
Walker SL, Hanaoka F, Karran P, Azathioprine and UVA light generate mutagenic
oxidative DNA damage, Science, 2005, 309, 1871-1874.
116 de Paulis A, Monfrecola G, Casula L, Prizio E, Di Gioia L, Carfora M, Russo I, de
Crescenzo G, Marone G, 8-Methoxypsoralen and long-wave ultraviolet A inhibit the release
of proinflammatory mediators and cytokines from human Fc epsilon RI+ cells: an in vitro
study, J Photochem Photobiol B, 2003, 69, 169-177.
117 Campistol JM, Eris J, Oberbauer R, Friend P, Hutchison B, Morales JM, Claesson K,
Stallone G, Russ G, Rostaing L, Kreis H, Burke JT, Brault Y, Scarola JA, Neylan JF,
Sirolimus therapy after early cyclosporine withdrawal reduces the risk for cancer in adult
renal transplantation, J Am Soc Nephrol, 2006, 17, 581-589.
118 Schade N, Esser C, Krutmann J, Ultraviolet B radiation-induced immunosuppression:
molecular mechanisms and cellular alterations, Photochem Photobiol Sci, 2005, 4, 699-708.
119 Schwarz T, Mechanisms of UV-induced immunosuppression, Keio J Med, 2005, 54, 165171.
120 Ullrich SE, Mechanisms underlying UV-induced immune suppression, Mutat Res, 2005,
571, 185-205.
121 Hanneman KK, Cooper KD, Baron ED, Ultraviolet immunosuppression: mechanisms and
consequences, Dermatol Clin, 2006, 24, 19-25.
122 Beissert S, Schwarz A, Schwarz T, Regulatory T cells, J Invest Dermatol, 2006, 126, 15-24.
56
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
123 Diffey BL, Sources and measurement of ultraviolet radiation, Methods, 2002, 28, 4-13.
124 McLoone P, Woods GM, Norval M, Decrease in Langerhans cells and increase in lymph
node dendritic cells following chronic exposure of mice to suberythemal doses of solar
simulated radiation, Photochem Photobiol, 2005, 81, 1168-1173.
125 Narbutt J, Lesiak A, Skibinska M, Wozniacka A, van Loveren H, Sysa-Jedrzejowska A,
Lewy-Trenda I, Omulecka A, Norval M, Suppression of contact hypersensitivity after
repeated exposures of humans to low doses of solar simulated radiation, Photochem
Photobiol Sci, 2005, 4, 517-522.
126 Ichihashi M, Nagai H, Matsunaga K, Sunlight is an important causative factor of recurrent
herpes simplex, Cutis, 2004, 74, 14-18.
127 Gilmour JW, Vestey JP, Norval M, The effect of UV therapy on immune function in
patients with psoriasis, Br J Dermatol, 1993, 129, 28-38.
128 van der Molen RG, Out-Luiting C, Claas FH, Norval M, Koerten HK, Mommaas AM,
Ultraviolet-B radiation induces modulation of antigen presentation of herpes simplex virus
by human epidermal cells, Hum Immunol, 2001, 62, 589-597.
129 Norval M, el-Ghorr AA, UV radiation and mouse models of herpes simplex virus infection,
Photochem Photobiol, 1996, 64, 242-245.
130 Loiacono CM, Taus NS, Mitchell WJ, The herpes simplex virus type 1 ICP0 promoter is
activated by viral reactivation stimuli in trigeminal ganglia neurons of transgenic mice, J
Neurovirol, 2003, 9, 336-345.
131 Akgul B, Cooke JC, Storey A, HPV-associated skin disease, J Pathol, 2006, 208, 165-175.
132 Termorshuizen F, Feltkamp MC, Struijk L, de Gruijl FR, Bavinck JN, van Loveren H,
Sunlight exposure and (sero)prevalence of epidermodysplasia verruciformis-associated
human papillomavirus, J Invest Dermatol, 2004, 122, 1456-1462.
133 Ateenyi-Agaba C, Dai M, Le Calvez F, Katongole-Mbidde E, Smet A, Tommasino M,
Franceschi S, Hainaut P, Weiderpass E, TP53 mutations in squamous-cell carcinomas of the
conjunctiva: evidence for UV-induced mutagenesis, Mutagenesis, 2004, 19, 399-401.
134 Ateenyi-Agaba C, Weiderpass E, Smet A, Dong W, Dai M, Kahwa B, Wabinga H,
Katongole-Mbidde E, Franceschi S, Tommasino M, Epidermodysplasia verruciformis
human papillomavirus types and carcinoma of the conjunctiva: a pilot study, Br J Cancer,
2004, 90, 1777-1779.
135 Hrushesky WJ, Sothern RB, Rietveld WJ, Du Quiton J, Boon ME, Season, sun, sex, and
cervical cancer, Cancer Epidemiol Biomarkers Prev, 2005, 14, 1940-1947.
136 Hrushesky WJ, Sothern RB, Rietveld WJ, Du-Quiton J, Boon ME, Sun exposure, sexual
behavior and uterine cervical human papilloma virus, Int J Biometeorol, 2006, 50, 167-173.
137 Sleijffers A, Garssen J, de Gruijl FR, Boland GJ, van Hattum J, van Vloten WA, van
Loveren H, Influence of ultraviolet B exposure on immune responses following hepatitis B
vaccination in human volunteers, J Invest Dermatol, 2001, 117, 1144-1150.
138 Sleijffers A, Garssen J, de Gruijl FR, Boland GJ, van Hattum J, van Vloten WA, van
Loveren H, UVB exposure impairs immune responses after hepatitis B vaccination in two
different mouse strains, Photochem Photobiol, 2002, 75, 541-546.
139 Sleijffers A, Yucesoy B, Kashon M, Garssen J, De Gruijl FR, Boland GJ, Van Hattum J,
Luster MI, Van Loveren H, Cytokine polymorphisms play a role in susceptibility to
ultraviolet B-induced modulation of immune responses after hepatitis B vaccination, J
Immunol, 2003, 170, 3423-8.
The Environmental Effects Assessment Panel Report for 2006
57
Effects on human health from stratospheric ozone depletion and its interactions with climate change
140 Sharma MK, Bhatia V, Swami HM, Outbreak of measles amongst vaccinated children in a
slum of Chandigarh, Indian J Med Sci, 2004, 58, 47-53.
141 Snopov SA, Kharit SM, Norval M, Ivanova VV, Circulating leukocyte and cytokine
responses to measles and poliovirus vaccination in children after ultraviolet radiation
exposures, Arch Virol, 2005, 150, 1729-1743.
142 Ghoreishi M, Dutz JP, Tolerance induction by transcutaneous immunization through
ultraviolet-irradiated skin is transferable through CD4+CD25+ T regulatory cells and is
dependent on host-derived IL-10, J Immunol, 2006, 176, 2635-2644.
143 Kuchel JM, Barnetson RS, Halliday GM, Cyclobutane pyrimidine dimer formation is a
molecular trigger for solar-simulated ultraviolet radiation-induced suppression of memory
immunity in humans, Photochem Photobiol Sci, 2005, 4, 577-582.
144 Kraemer KH, Lee MM, Scotto J, Xeroderma pigmentosum. Cutaneous, ocular, and
neurologic abnormalities in 830 published cases, Arch Dermatol, 1987, 123, 241-250.
145 Yarosh DB, DNA repair, immunosuppression, and skin cancer, Cutis, 2004, 74, 10-13.
146 Kolgen W, van Steeg H, van der Horst GT, Hoeijmakers JH, van Vloten WA, de Gruijl FR,
Garssen J, Association of transcription-coupled repair but not global genome repair with
ultraviolet-B-induced Langerhans cell depletion and local immunosuppression, J Invest
Dermatol, 2003, 121, 751-756.
147 Miyauchi-Hashimoto H, Sugihara A, Tanaka K, Horio T, Ultraviolet radiation-induced
impairment of tumor rejection is enhanced in xeroderma pigmentosum a gene-deficient
mice, J Invest Dermatol, 2005, 124, 1313-1317.
148 Holick MF, Sunlight and vitamin D for bone health and prevention of autoimmune diseases,
cancers, and cardiovascular disease, Am J Clin Nutr, 2004, 80, 1678S-1688S.
149 Grant WB, Holick MF, Benefits and requirements of vitamin D for optimal health: a review,
Altern Med Rev, 2005, 10, 94-111.
150 Wolpowitz D, Gilchrest BA, The vitamin D questions: how much do you need and how
should you get it?, J Am Acad Dermatol, 2006, 54, 301-317.
151 Bischoff-Ferrari HA, Giovannucci E, Willett WC, Dietrich T, Dawson-Hughes B,
Estimation of optimal serum concentrations of 25-hydroxyvitamin D for multiple health
outcomes, Am J Clin Nutr, 2006, 84, 18-28.
152 MacLaughlin JA, Anderson RR, Holick MF, Spectral character of sunlight modulates
photosynthesis of previtamin D3 and its photoisomers in human skin, Science, 1982, 216,
1001-1003.
153 Engelsen O, Brustad M, Aksnes L, Lund E, Daily duration of vitamin D synthesis in human
skin with relation to latitude, total ozone, altitude, ground cover, aerosols and cloud
thickness, Photochem Photobiol, 2005, 81, 1287-1290.
154 McGrath JJ, Kimlin MG, Saha S, Eyles DW, Parisi AV, Vitamin D insufficiency in southeast Queensland, Med J Aust, 2001, 174, 150-151.
155 Brock K, Wilkinson M, Cook R, Lee S, Bermingham M, Associations with Vitamin D
deficiency in "at risk" Australians, J Steroid Biochem Mol Biol, 2004, 89-90, 581-588.
156 MacFarlane GD, Sackrison JL, Jr., Body JJ, Ersfeld DL, Fenske JS, Miller AB,
Hypovitaminosis D in a normal, apparently healthy urban European population, J Steroid
Biochem Mol Biol, 2004, 89-90, 621-622.
157 Andersen R, Molgaard C, Skovgaard LT, Brot C, Cashman KD, Chabros E, Charzewska J,
Flynn A, Jakobsen J, Karkkainen M, Kiely M, Lamberg-Allardt C, Moreiras O, Natri AM,
58
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
158
159
160
161
162
163
164
165
166
167
168
169
170
O'Brien M, Rogalska-Niedzwiedz M, Ovesen L, Teenage girls and elderly women living in
northern Europe have low winter vitamin D status, Eur J Clin Nutr, 2005, 59, 533-541.
Atli T, Gullu S, Uysal AR, Erdogan G, The prevalence of Vitamin D deficiency and effects
of ultraviolet light on Vitamin D levels in elderly Turkish population, Arch Gerontol
Geriatr, 2005, 40, 53-60.
Rockell JE, Green TJ, Skeaff CM, Whiting SJ, Taylor RW, Williams SM, Parnell WR,
Scragg R, Wilson N, Schaaf D, Fitzgerald ED, Wohlers MW, Season and ethnicity are
determinants of serum 25-hydroxyvitamin D concentrations in New Zealand children aged
5-14 y, J Nutr, 2005, 135, 2602-2608.
Matsuoka LY, Wortsman J, Haddad JG, Kolm P, Hollis BW, Racial pigmentation and the
cutaneous synthesis of vitamin D, Arch Dermatol, 1991, 127, 536-538.
Nesby-O'Dell S, Scanlon KS, Cogswell ME, Gillespie C, Hollis BW, Looker AC, Allen C,
Doughertly C, Gunter EW, Bowman BA, Hypovitaminosis D prevalence and determinants
among African American and white women of reproductive age: third National Health and
Nutrition Examination Survey, 1988-1994, Am J Clin Nutr, 2002, 76, 187-192.
Mathieu C, van Etten E, Decallonne B, Guilietti A, Gysemans C, Bouillon R, Overbergh L,
Vitamin D and 1,25-dihydroxyvitamin D3 as modulators in the immune system, J Steroid
Biochem Mol Biol, 2004, 89-90, 449-452.
Meindl S, Rot A, Hoetzenecker W, Kato S, Cross HS, Elbe-Burger A, Vitamin D receptor
ablation alters skin architecture and homeostasis of dendritic epidermal T cells, Br J
Dermatol, 2005, 152, 231-241.
Garland CF, Garland FC, Gorham ED, Lipkin M, Newmark H, Mohr SB, Holick MF, The
role of vitamin D in cancer prevention, Am J Public Health, 2006, 96, 252-261.
van der Rhee HJ, de Vries E, Coebergh JW, Does sunlight prevent cancer? A systematic
review, Eur J Cancer, 2006, 42, 2222-2232.
Tuohimaa P, Tenkanen L, Ahonen M, Lumme S, Jellum E, Hallmans G, Stattin P, Harvei S,
Hakulinen T, Luostarinen T, Dillner J, Lehtinen M, Hakama M, Both high and low levels of
blood vitamin D are associated with a higher prostate cancer risk: a longitudinal, nested
case-control study in the Nordic countries, Int J Cancer, 2004, 108, 104-108.
Wactawski-Wende J, Kotchen JM, Anderson GL, Assaf AR, Brunner RL, O'Sullivan MJ,
Margolis KL, Ockene JK, Phillips L, Pottern L, Prentice RL, Robbins J, Rohan TE, Sarto
GE, Sharma S, Stefanick ML, Van Horn L, Wallace RB, Whitlock E, Bassford T, Beresford
SA, Black HR, Bonds DE, Brzyski RG, Caan B, Chlebowski RT, Cochrane B, Garland C,
Gass M, Hays J, Heiss G, Hendrix SL, Howard BV, Hsia J, Hubbell FA, Jackson RD,
Johnson KC, Judd H, Kooperberg CL, Kuller LH, LaCroix AZ, Lane DS, Langer RD,
Lasser NL, Lewis CE, Limacher MC, Manson JE, Calcium plus vitamin D supplementation
and the risk of colorectal cancer, N Engl J Med, 2006, 354, 684-696.
Giovannucci E, The epidemiology of vitamin D and colorectal cancer: recent findings, Curr
Opin Gastroenterol, 2006, 22, 24-29.
Holick MF, Calcium plus vitamin D and the risk of colorectal cancer, N Engl J Med, 2006,
354, 2287-2288.
Gorham ED, Garland CF, Garland FC, Grant WB, Mohr SB, Lipkin M, Newmark HL,
Giovannucci E, Wei M, Holick MF, Vitamin D and prevention of colorectal cancer, J
Steroid Biochem Mol Biol, 2005, 97, 179-194.
The Environmental Effects Assessment Panel Report for 2006
59
Effects on human health from stratospheric ozone depletion and its interactions with climate change
171 Grau MV, Baron JA, Sandler RS, Haile RW, Beach ML, Church TR, Heber D, Vitamin D,
calcium supplementation, and colorectal adenomas: results of a randomized trial, J Natl
Cancer Inst, 2003, 95, 1765-1771.
172 Hughes AM, Armstrong BK, Vajdic CM, Turner J, Grulich A, Fritschi L, Milliken S,
Kaldor J, Benke G, Kricker A, Pigmentary characteristics, sun sensitivity and non-Hodgkin
lymphoma, Int J Cancer, 2004, 110, 429-434.
173 Rukin NJ, Luscombe C, Moon S, Bodiwala D, Liu S, Saxby MF, Fryer AA, Alldersea J,
Hoban PR, Strange RC, Prostate cancer susceptibility is mediated by interactions between
exposure to ultraviolet radiation and polymorphisms in the 5' haplotype block of the vitamin
D receptor gene, Cancer Lett, 2006.
174 Giovannucci E, The epidemiology of vitamin D and cancer incidence and mortality: a
review (United States), Cancer Causes Control, 2005, 16, 83-95.
175 McMichael AJ, Hall AJ, Does immunosuppressive ultraviolet radiation explain the latitude
gradient for multiple sclerosis?, Epidemiology, 1997, 8, 642-645.
176 Hauser S, Weiner H, Che M, Shapiro M, Gilles F, Letwin N, Prevention of experimental
allergic encephalitis (EAE) in the SJL/J mouse by whole body ultraviolet irradiation, J
Immunol, 1984, 132, 1276-1281.
177 van der Mei IA, Ponsonby AL, Dwyer T, Blizzard L, Simmons R, Taylor BV, Butzkueven
H, Kilpatrick T, Past exposure to sun, skin phenotype, and risk of multiple sclerosis: casecontrol study, Bmj, 2003, 327, 316.
178 Munger KL, Zhang SM, O'Reilly E, Hernan MA, Olek MJ, Willett WC, Ascherio A,
Vitamin D intake and incidence of multiple sclerosis, Neurology, 2004, 62, 60-65.
179 Goldacre MJ, Seagroatt V, Yeates D, Acheson ED, Skin cancer in people with multiple
sclerosis: a record linkage study, J Epidemiol Community Health, 2004, 58, 142-144.
180 Tsunoda I, Kuang LQ, Igenge IZ, Fujinami RS, Converting relapsing remitting to secondary
progressive experimental allergic encephalomyelitis (EAE) by ultraviolet B irradiation, J
Neuroimmunol, 2005, 160, 122-134.
181 Spach KM, Hayes CE, Vitamin D3 confers protection from autoimmune encephalomyelitis
only in female mice, J Immunol, 2005, 175, 4119-4126.
182 Giulietti A, Gysemans C, Stoffels K, van Etten E, Decallonne B, Overbergh L, Bouillon R,
Mathieu C, Vitamin D deficiency in early life accelerates Type 1 diabetes in non-obese
diabetic mice, Diabetologia, 2004, 47, 451-462.
183 Hypponen E, Laara E, Reunanen A, Jarvelin MR, Virtanen SM, Intake of vitamin D and
risk of type 1 diabetes: a birth-cohort study, Lancet, 2001, 358, 1500-1503.
184 EURODIAB, Substudy, 2, Study, Group, Vitamin D supplement in early childhood and risk
for Type ! (insulin-dependent) diabetes mellitus, Diabetologia, 1999, 42, 51-54.
185 Stene LC, Ulriksen J, Magnus P, Joner G, Use of cod liver oil during pregnancy associated
with lower risk of Type I diabetes in the offspring, Diabetologia, 2000, 43, 1093-1098.
186 Staples JA, Ponsonby AL, Lim LL, McMichael AJ, Ecologic analysis of some immunerelated disorders, including type 1 diabetes, in Australia: latitude, regional ultraviolet
radiation, and disease prevalence, Environ Health Perspect, 2003, 111, 518-523.
187 Merlino LA, Curtis J, Mikuls TR, Cerhan JR, Criswell LA, Saag KG, Vitamin D intake is
inversely associated with rheumatoid arthritis: results from the Iowa Women's Health Study,
Arthritis Rheum, 2004, 50, 72-77.
60
The Environmental Effects Assessment Panel Report for 2006
Effects on human health from stratospheric ozone depletion and its interactions with climate change
188 Froicu M, Weaver V, Wynn TA, McDowell MA, Welsh JE, Cantorna MT, A crucial role
for the vitamin D receptor in experimental inflammatory bowel diseases, Mol Endocrinol,
2003, 17, 2386-2392.
189 Cantorna MT, Zhu Y, Froicu M, Wittke A, Vitamin D status, 1,25-dihydroxyvitamin D3,
and the immune system, Am J Clin Nutr, 2004, 80, 1717S-1720S.
190 Ponsonby AL, Lucas RM, van der Mei IA, UVR, vitamin D and three autoimmune diseases-multiple sclerosis, type 1 diabetes, rheumatoid arthritis, Photochem Photobiol, 2005, 81,
1267-75.
191 Bosch X, Hypercalcemia due to endogenous overproduction of 1,25-dihydroxyvitamin D in
Crohn's disease, Gastroenterology, 1998, 114, 1061-1065.
192 Hamada K, Nagai S, Tsutsumi T, Izumi T, Ionized calcium and 1,25-dihydroxyvitamin D
concentration in serum of patients with sarcoidosis, Eur Respir J, 1998, 11, 1015-1020.
193 Abreu MT, Kantorovich V, Vasiliauskas EA, Gruntmanis U, Matuk R, Daigle K, Chen S,
Zehnder D, Lin YC, Yang H, Hewison M, Adams JS, Measurement of vitamin D levels in
inflammatory bowel disease patients reveals a subset of Crohn's disease patients with
elevated 1,25-dihydroxyvitamin D and low bone mineral density, Gut, 2004, 53, 1129-1136.
194 Waters WR, Palmer MV, Nonnecke BJ, Whipple DL, Horst RL, Mycobacterium bovis
infection of vitamin D-deficient NOS2-/- mice, Microb Pathog, 2004, 36, 11-17.
195 Rhodes SG, Terry LA, Hope J, Hewinson RG, Vordermeier HM, 1,25-dihydroxyvitamin D3
and development of tuberculosis in cattle, Clin Diagn Lab Immunol, 2003, 10, 1129-1135.
196 Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K,
Meinken C, Kamen DL, Wagner M, Bals R, Steinmeyer A, Zugel U, Gallo RL, Eisenberg
D, Hewison M, Hollis BW, Adams JS, Bloom BR, Modlin RL, Toll-like receptor triggering
of a vitamin D-mediated human antimicrobial response, Science, 2006, 311, 1770-1773.
197 Wilkinson RJ, Llewelyn M, Toossi Z, Patel P, Pasvol G, Lalvani A, Wright D, Latif M,
Davidson RN, Influence of vitamin D deficiency and vitamin D receptor polymorphisms on
tuberculosis among Gujarati Asians in west London: a case-control study, Lancet, 2000,
355, 618-621.
198 Ustianowski A, Shaffer R, Collin S, Wilkinson RJ, Davidson RN, Prevalence and
associations of vitamin D deficiency in foreign-born persons with tuberculosis in London, J
Infect, 2005, 50, 432-437.
199 Cannell JJ, Vieth R, Umhau JC, Holick MF, Grant WB, Madronich S, Garland CF,
Giovannucci E, Epidemic influenza and vitamin D, Epidemiol Infect, 2006, 1-12.
200 Emmen HH, Hoogendijk EM, Klopping-Ketelaars WA, Muijser H, Duistermaat E,
Ravensberg JC, Alexander DJ, Borkhataria D, Rusch GM, Schmit B, Human safety and
pharmacokinetics of the CFC alternative propellants HFC 134a (1,1,1,2-tetrafluoroethane)
and HFC 227 (1,1,1,2,3,3, 3-heptafluoropropane) following whole-body exposure, Regul
Toxicol Pharmacol, 2000, 32, 22-35.
201 Hoet P, Buchet JP, Sempoux C, Haufroid V, Rahier J, Lison D, Potentiation of 2,2-dichloro1,1,1-trifluoroethane (HCFC-123)-induced liver toxicity by ethanol in guinea-pigs, Arch
Toxicol, 2002, 76, 707-14.
202 Takebayashi T, Kabe I, Endo Y, Tanaka S, Miyauchi H, Nozi K, Takahashi K, Omae K,
Acute liver dysfunction among workers exposed to 2,2-dichloro-1,1,1-tryfluoroethane
(HCFC-123): a case report, Appl Occup Environ Hyg, 1999, 14, 72-74.
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
203 Hoet P, Buchet JP, Sempoux C, Nomiyama T, Rahier J, Lison D, Investigations on the liver
toxicity of a blend of HCFC-123 (2,2-dichloro-1,1,1-trifluoroethane) and HCFC-124 (2chloro-1,1,1,2-tetrafluoroethane) in guinea-pigs, Arch Toxicol, 2001, 75, 274-283.
204 Boucher R, Hanna C, Rusch GM, Stidham D, Swan E, Vazquez M, Hepatotoxicity
associated with overexposure to 1,1-dichloro-2,2,2-trifluoroethane (HCFC-123), AIHA J
(Fairfax, Va), 2003, 64, 68-79.
205 Rosenthal FS, Phoon C, Bakalian AE, Taylor HR, The ocular dose of ultraviolet radiation to
outdoor workers, Invest Ophthalmol Vis Sci, 1988, 29, 649-656.
206 Samanek AJ, Croager EJ, Giesfor Skin Cancer Prevention P, Milne E, Prince R, McMichael
AJ, Lucas RM, Slevin T, Estimates of beneficial and harmful sun exposure times during the
year for major Australian population centres, Med J Aust, 2006, 184, 338-341.
207 Roberts JE, Ocular phototoxicity, J Photochem Photobiol B, 2001, 64, 136-143.
208 Black HS, Reassessment of a free radical theory of cancer with emphasis on ultraviolet
carcinogenesis, Integr Cancer Ther, 2004, 3, 279-293.
209 Sliney DH, Exposure geometry and spectral environment determine photobiological effects
on the human eye, Photochem Photobiol, 2005, 81, 483-489.
210 Sliney DH, Photoprotection of the eye - UV radiation and sunglasses, J Photochem
Photobiol B, 2001, 64, 166-75.
211 Dain SJ, Sunglasses and sunglass standards, Clin Expl Optom, 2003, 86, 77-90.
212 Walsh JE, Bergmanson JP, Saldana G, Jr., Gaume A, Can UV radiation-blocking soft
contact lenses attenuate UV radiation to safe levels during summer months in the southern
United States?, Eye Contact Lens, 2003, 29, S174-S179.
213 Matsuoka LY, Ide L, Wortsman J, MacLaughlin JA, Holick MF, Sunscreens suppress
cutaneous vitamin D3 synthesis, J Clin Endocrinol Metab, 1987, 64, 1165-1168.
214 Marks R, Foley PA, Jolley D, Knight KR, Harrison J, Thompson SC, The effect of regular
sunscreen use on vitamin D levels in an Australian population. Results of a randomized
controlled trial, Arch Dermatol, 1995, 131, 415-421.
215 Sollitto RB, Kraemer KH, DiGiovanna JJ, Normal vitamin D levels can be maintained
despite rigorous photoprotection: six years' experience with xeroderma pigmentosum, J Am
Acad Dermatol, 1997, 37, 942-947.
216 Farrerons J, Barnadas M, Rodriguez J, Renau A, Yoldi B, Lopez-Navidad A, Moragas J,
Clinically prescribed sunscreen (sun protection factor 15) does not decrease serum vitamin
D concentration sufficiently either to induce changes in parathyroid function or in metabolic
markers, Br J Dermatol, 1998, 139, 422-427.
217 Diffey BL, Gibson CJ, Haylock R, McKinlay AF, Outdoor ultraviolet exposure of children
and adolescents, Br J Dermatol, 1996, 134, 1030-1034.
218 Diffey B, Sunscreen isn't enough, J Photochem Photobiol B, 2001, 64, 105-108.
219 Young AR, Methods used to evaluate the immune protection factor of a sunscreen:
advantages and disadvantages of different in vivo techniques, Cutis, 2004, 74, 19-23.
220 Kripke ML, The ABCs of sunscreen protection factors, J Invest Dermatol, 2003, 121, VIIVIII.
221 Strickland FM, Kuchel JM, Halliday GM, Natural products as aids for protecting the skin's
immune system against UV damage, Cutis, 2004, 74, 24-28.
222 Kullavanijaya P, Lim HW, Photoprotection, J Am Acad Dermatol, 2005, 52, 937-58; quiz
959-62.
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Effects on human health from stratospheric ozone depletion and its interactions with climate change
223 Schlumpf M, Schmid P, Durrer S, Conscience M, Maerkel K, Henseler M, Gruetter M,
Herzog I, Reolon S, Ceccatelli R, Faass O, Stutz E, Jarry H, Wuttke W, Lichtensteiger W,
Endocrine activity and developmental toxicity of cosmetic UV filters--an update,
Toxicology, 2004, 205, 113-122.
224 Durrer S, Maerkel K, Schlumpf M, Lichtensteiger W, Estrogen target gene regulation and
coactivator expression in rat uterus after developmental exposure to the ultraviolet filter 4methylbenzylidene camphor, Endocrinology, 2005, 146, 2130-2139.
225 Gomez E, Pillon A, Fenet H, Rosain D, Duchesne MJ, Nicolas JC, Balaguer P, Casellas C,
Estrogenic activity of cosmetic components in reporter cell lines: parabens, UV screens, and
musks, J Toxicol Environ Health A, 2005, 68, 239-251.
226 Koda T, Umezu T, Kamata R, Morohoshi K, Ohta T, Morita M, Uterotrophic effects of
benzophenone derivatives and a p-hydroxybenzoate used in ultraviolet screens, Environ
Res, 2005, 98, 40-45.
227 Morohoshi K, Yamamoto H, Kamata R, Shiraishi F, Koda T, Morita M, Estrogenic activity
of 37 components of commercial sunscreen lotions evaluated by in vitro assays, Toxicol In
Vitro, 2005, 19, 457-469.
228 Suzuki T, Kitamura S, Khota R, Sugihara K, Fujimoto N, Ohta S, Estrogenic and
antiandrogenic activities of 17 benzophenone derivatives used as UV stabilizers and
sunscreens, Toxicol Appl Pharmacol, 2005, 203, 9-17.
229 Klann A, Levy G, Lutz I, Muller C, Kloas W, Hildebrandt JP, Estrogen-like effects of
ultraviolet screen 3-(4-methylbenzylidene)-camphor (Eusolex 6300) on cell proliferation
and gene induction in mammalian and amphibian cells, Environ Res, 2005, 97, 274-281.
230 Schreurs RH, Sonneveld E, Jansen JH, Seinen W, van der Burg B, Interaction of polycyclic
musks and UV filters with the estrogen receptor (ER), androgen receptor (AR), and
progesterone receptor (PR) in reporter gene bioassays, Toxicol Sci, 2005, 83, 264-272.
231 Bain J, Rusch H, Kline B, The effect of temperature upon ultraviolet carcinogenesis with
wavelengths 2800-3400 A, Cancer Res, 1943, 3, 610-612.
232 Freeman RG, Knox JM, Influence of temperature on utraviolet Injury, Arch Dermatol,
1964, 89, 858-864.
233 van der Leun JC, de Gruijl FR, Climate change and skin cancer, Photochem Photobiol Sci,
2002, 1, 324-326.
234 Scotto J, Nonmelanoma skin cancer--UV-B effects, in Stratospheric ozone. Effects of
changes in stratospheric ozone and global climate, Vol. 2 ed.: Titus JG, U.S. Environmental
Protection Agency, Washington, DC, 1986, pp. 33-61.
235 Sasaki H, Jonasson F, Shui YB, Kojima M, Ono M, Katoh N, Cheng HM, Takahashi N,
Sasaki K, High prevalence of nuclear cataract in the population of tropical and subtropical
areas, Dev Ophthalmol, 2002, 35, 60-69.
236 Punareewattana K, Smith BJ, Blaylock BL, Longstreth J, Snodgrass HL, Gogal RM, Jr.,
Prater RM, Holladay SD, Topical permethrin exposure inhibits antibody production and
macrophage function in C57Bl/6N mice, Food Chem Toxicol, 2001, 39, 133-139.
237 Prater MR, Gogal RM, Jr., Blaylock BL, Holladay SD, Cis-urocanic acid increases
immunotoxicity and lethality of dermally administered permethrin in C57BL/6N mice, Int J
Toxicol, 2003, 22, 35-42.
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63
Chapter 3. Terrestrial ecosystems, increased solar ultraviolet
radiation, and interactions with other climate change factors
M. M. Caldwella, J. F. Bornmanb C. L. Ballaréc, S. D. Flintd, G. Kulandaivelue
a
Division of Environmental Biology, National Science Foundation, 4201 Wilson Blvd, Arlington,
Virginia 22230, USA
b
Danish Institute of Agricultural Sciences, Department of Plant Biology, Research Centre
Flakkebjerg, Flakkebjerg, DK-4200 Slagelse, Denmark and International Global Change
Institute, IGCI, University of Waikato, 3200 Hamilton, New Zealand
c
IFEVA, Facultad de Agronomía, CONICET and Universidad de Buenos Aires, Avda. San
Martín 4453, C1417DSE Buenos Aires, Argentina
d
Ecology Center, Utah State University, Logan, Utah 84322-5230, USA
e
School of Biological Sciences, Madurai Kamaraj University, Madurai 625021, India
Summary
There have been significant advances in our understanding of the effects of UV-B radiation on
terrestrial ecosystems, especially in the description of mechanisms of plant response. A further
area of highly interesting research emphasizes the importance of indirect UV radiation effects on
plants, pathogens, herbivores, soil microbes and ecosystem processes below the surface.
Although photosynthesis of higher plants and mosses is seldom affected by enhanced or reduced
UV-B radiation in most field studies, effects on growth and morphology (form) of higher plants
and mosses are often manifested. This can lead to small reductions in shoot production and
changes in the competitive balance of different species. Fungi and bacteria are generally more
sensitive to damage by UV-B radiation than are higher plants. However, the species differ in
their UV-B radiation sensitivity to damage, some being affected while others may be very
tolerant. This can lead to changes in species composition of microbial communities with
subsequent influences on processes such as litter decomposition. Changes in plant chemical
composition are commonly reported due to UV-B manipulations (either enhancement or
attenuation of UV-B in sunlight) and may lead to substantial reductions in consumption of plant
tissues by insects. Although sunlight does not penetrate significantly into soils, the biomass and
morphology of plant root systems of plants can be modified to a much greater degree than plant
shoots. Root mass can exhibit sizeable declines with more UV-B. Also, UV-B-induced changes
in soil microbial communities and biomass, as well as altered populations of small invertebrates
have been reported and these changes have important implications for mineral nutrient cycling in
the soil. Many new developments in understanding the underlying mechanisms mediating plant
response to UV-B radiation have emerged. This new information is helpful in understanding
common responses of plants to UV-B radiation, such as diminished growth, acclimation
responses of plants to UV-B radiation and interactions of plants with consumer organisms such
as insects and plant pathogens. The response to UV-B radiation involves both the initial stimulus
by solar radiation and transmission of signals within the plants. Resulting changes in gene
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
expression induced by these signals may have elements in common with those elicited by other
environmental factors, and generate overlapping functional (including acclimation) responses.
Concurrent responses of terrestrial systems to the combination of enhanced UV-B radiation and
other global change factors (increased temperature, CO2, available nitrogen and altered
precipitation) are less well understood. Studies of individual plant responses to combinations of
factors indicate that plant growth can be augmented by higher CO2 levels, yet many of the effects
of UV-B radiation are usually not ameliorated by the elevated CO2. UV-B radiation often
increases both plant frost tolerance and survival under extreme high temperature conditions.
Conversely, extreme temperatures sometimes influence the UV-B radiation sensitivity of plants
directly. Plants that endure water deficit stress effectively are also likely to be tolerant of high
UV-B flux. Biologically available nitrogen is exceeding historical levels in many regions due to
human activities. Studies show that plants well supplied with nitrogen are generally more
sensitive to UV-B radiation. Technical issues concerning the use of biological spectral
weighting functions (BSWF) have been further elucidated. The BSWF, which are multiplication
factors assigned to different wavelengths giving an indication of their relative biological
effectiveness, are critical to the proper conduct and interpretation of experiments in which
organisms are exposed to UV radiation, both in the field and in controlled environment facilities.
The characteristics of BSWF vary considerably among different plant processes, such as growth,
DNA damage, oxidative damage and induction of changes in secondary chemicals. Thus, use of
a single BSWF for plant or ecosystem response is not appropriate. This brief review emphasizes
progress since the previous report toward the understanding of solar ultraviolet radiation effects
on terrestrial systems as it relates to ozone column reduction and the interaction of climate
change factors.
Introduction
Terrestrial ecosystems are undergoing transitions in our changing climate and are likely to be in
flux in the coming decades and beyond. Much of this may be attributed to direct and indirect
effects of increasing temperature and CO2. The influence of increased solar UV-B radiation is
superimposed on these important drivers of our changing terrestrial ecosystems. Much has been
learned about how plants and other organisms respond to UV radiation at the molecular and
physiological levels and several studies have focused on the implications of interactions of
vegetation with animals and microbes. Ecosystems are being confronted with several aspects of
climate change simultaneously, resulting in interactive responses to environmental factors such
as UV radiation, increasing temperature, CO2, and changing precipitation patterns. Nitrogen is
also considered, since biologically available nitrogen is increasing in more inhabited areas of the
globe due to factors such as air pollution and agricultural application of nitrogen. Experiments
have been conducted on agricultural and non-agricultural plants in various settings (Figure 3-1).
Ecosystem-level responses
Predictions of ecosystem consequences of enhanced UV-B radiation are necessarily complicated
because of species interactions and the way in which living organisms affect and are affected by
the abiotic components of the ecosystem, e.g., soils, water, mineral elements, etc. Ecosystemlevel effects can best be examined by direct, manipulative experiments conducted in the field in
intact ecosystems. Sometimes these experiments are confined to small sections of intact soil,
vegetation and associated microorganisms, termed “mesocosms”. These field studies have either
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
involved supplementation with UV-B-radiation-emitting lamps or attenuation of ambient solar
UV-B radiation using special selective filters (Figure 3-1a and 3-1c). In both cases, there are
appropriate control treatments to account for unintended side effects of the structures used to
effect the UV-B radiation manipulations.
Figure 3-1. Examples of studies of the impacts of UV-B radiation on terrestrial ecosystems. The work described in
this report is based on studies that addressed the effects of UV-B radiation manipulations on (a) intact natural
ecosystems, (b) native plants, such as Gunnera magellanica and Blechnum penna-marina, (c) field crops, such as (d)
soybean, (e) barley, (f) tomato, (g) the model plant Arabidopsis thaliana, and (h) several species of phytophagous
insects, such as Manduca sexta.
Global distribution of climate change factors
Factors of climate change are being manifested across the globe in different patterns. Elevated
CO2 is fairly evenly distributed. Significant changes in the frequency and quantity of
precipitation are also predicted at all latitudes because of climate change. With global warming
the hydrological cycle will accelerate and general increases in precipitation are likely to occur.1
However, there are large departures at regional scales, such that some areas will receive
considerably more and some much less precipitation. Nitrogen deposition is increasingly a
global issue and is particularly prominent in densely inhabited areas where agricultural nitrogen
use and air pollution are the main contributors to the biologically available nitrogen in these
ecosystems.2 The relative increases in solar UV-B radiation and temperature are decidedly more
pronounced at high latitudes and, accordingly, most of the more recent UV-B radiation
experiments conducted at the ecosystem level have been at high latitudes. These have included
locations in Antarctica and the southernmost tip of South America (Tierra del Fuego) and several
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
Arctic and sub-Arctic locations including northern Sweden, Svalbard, and Greenland. A few of
the ecosystem-level experiments have involved manipulation of other climate change factors in
addition to UV-B radiation, such as moisture.
Direct effects on organisms
Plants. Mosses, lichens, and higher plants have received most attention in assessing UV-B
radiation effects on terrestrial systems. Photosynthesis of these plant groups at high-latitude sites
is generally unaffected, although aboveground biomass is often reduced to a small extent by UVB radiation in various supplementation and attenuation experiments.3-6 Small effects on higher
plant growth at high latitudes due to UV-B radiation concur with findings of many studies on
plants at lower latitudes, e.g., Searls et al.7 Occasionally, large growth reductions have been
reported. For example, UV radiation attenuation studies with potted plants in Antarctica
indicated that ambient UV-B radiation caused sizeable growth reductions.8-11 Also, an endemic
species of moss in Antarctica was found to have reduced levels of photoprotective pigments
(compared to other widely distributed moss species), and current levels of UV radiation were
reported to cause increased frequency of leaf morphological abnormalities.12
Among growth characteristics altered by UV-B radiation, reductions in plant height are often
reported. Even subtle decreases in plant height due to UV-B radiation might be of eventual
significance if different species are affected to different degrees as was the case in ecosystem
plots of a peat bog in Tierra del Fuego.5 In this study, when compared to the attenuated UV-B
radiation treatment, higher plants were inhibited more by near-ambient solar UV-B radiation
than was the moss layer. Thus, the moss could slowly engulf the higher plants; however, this
would likely take several years to decades.
Both supplementation and attenuation of UV-B radiation in experimental studies may influence
allocation of biomass to root systems. A few recent reports indicate large changes in root
systems attributable to the UV-B radiation treatments aboveground, suggesting a systemic
response to the radiation (Figure 3- 2). Root mass increased with solar UV-B radiation
attenuation in experiments conducted in Greenland13 and Tierra del Fuego.14 In a similar vein,
Ruhland et al.11 reported substantial increases in root mass with reduced UV-B radiation in solar
UV-B radiation attenuation experiments using potted plants in Antarctica. On the other hand,
studies in Finland indicated an increase in root mass with UV-B radiation supplementation.15
The underlying mechanisms behind these seemingly contradictory responses are not known but
may be due in part to experimental differences. In all these cases, these were large relative
changes — much larger than the relative changes in shoot mass generally reported as a result of
UV-B radiation manipulations.
Animals. Most vertebrate animals and insects are assumed to be well protected by body
coverings (fur, feathers, etc.) and pigmentation. However, amphibians, such as frogs and
salamandars are much less well protected than other vertebrates and considerable controversy
exists regarding how much they might be affected by exposure to ambient UV-B radiation in
their natural habitats16-18, see Chapter 4. The UV-B radiation sensitivity of soil insects such as
the Arctic collembolan (springtail) species was investigated in laboratory tests.19 The species
varied considerably in pigmentation which corresponded to the degree to which they are
normally exposed to sunlight. These ranged from soil-living forms that lacked apparent
pigmentation to heavily pigmented surface-dwelling species often exposed to the sun. The UVB radiation sensitivity was inversely correlated with pigmentation and well pigmented species
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
were considered to be tolerant of UV-B radiation corresponding to solar UV-B radiation with
substantially depleted ozone. Nevertheless, the author speculated that solar UV-B radiation
(especially with ozone reduction) might influence the distribution of springtail species near the
soil surface in heterogeneous environments. Behavioral responses to solar UV-B radiation have
been reported for thrips, a leaf-eating insect that can cause severe damage to a variety of
commercially important crops. Field studies demonstrated that these insects can detect and avoid
exposure to the UV-B component of solar radiation, even though the natural background levels
of solar UV-A and visible radiation contain much more energy, indicating that thrips have a
sensory system with high UV-B radiation specificity.20, 21 Whether or not this sensitivity is
widespread among herbivorous insects is not known, but strong effects of UV-B radiation
manipulations on levels of insect herbivory have been documented in a variety of ecosystems22
and are described below.
Figure 3-2. Ecosystem-level manifestations of changing the UV-B flux reaching above-ground vegetation and other
surfaces. Above ground, higher plants are affected to a small degree in morphology and growth, while fungi and
other microbes exposed to sunlight are often affected to a greater extent. Many effects occur below the surface of
soils or peat where no sunlight penetrates. Root mass and mycorrhizal abundance can either increase or decrease
with more UV-B radiation and these changes can be much larger than changes in the plant shoot system. Alterations
in microbial communities, nutrient levels and fluxes as well as microinvertebrates have also resulted from UV-B
radiation changes above ground. These are probably mediated by systemic changes in higher plants and in the
Sphagnum peat.
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
Microbes. Unlike most photosynthetic plants (flowering plants, mosses and lichens), microbes
can be quite sensitive to the UV-B radiation in direct sunlight.23-26 However, this is usually not a
uniform sensitivity among different species so that species composition changes are often
observed on foliage and litter surfaces where these microbes are directly exposed to sunlight.27-32
In the studies of Moody et al.27 and Pancotto et al.30, changes in microbial species composition
were linked to differences in litter decomposition rates resulting from UV-B radiation
manipulations. Solar UV radiation can also have direct effects promoting plant litter
decomposition. This process is know as photodegradation and plays a significant role in carbon
cycling in arid ecosystems33 as discussed in Chapter 5.
Indirect effects of UV-B radiation
Though less expected, indirect effects of solar UV-B radiation are usually much more important,
intricate and, indeed, fascinating than the direct effects of solar UV radiation. In addition, there
is an increasing mechanistic understanding of these indirect effects that is developing as will be
described later. In most cases, these effects are mediated through the plants, but can be
manifested below ground as well as above ground.
Above ground
As discussed in the last report22, UV irradiation of plants affects plant disease sensitivity and
development. Although few phenomenological studies of UV radiation and plant disease have
been published since the last report, there are important new developments in understanding the
mechanisms of this action.
In the field, plants exposed to ambient UV-B radiation often suffer less herbivory by folivorous
insects than plants cultivated under filters that specifically exclude the UV-B component of solar
radiation. This effect of solar UV-B radiation on insect herbivory was reported to be very large
in a number of earlier studies.20, 34, 35 In some cases the negative influence of UV-B radiation on
insect herbivory can be partially explained by direct effects of solar UV-B radiation on insect
behavior.20, 21 In most cases, however, the anti-herbivore effect of solar UV-B radiation appears
to be indirect, i.e., mediated by UV-B-radiation-induced increases in plant defenses. Much has
been learned concerning mechanisms of this indirect influence on susceptibility to herbivory, as
discussed later.
Below ground
Sunlight scarcely penetrates the soil surface, yet manipulation of UV-B radiation has been
reported to have several consequences belowground in ecosystems (Figure 3- 2). In the soil,
specific microbial communities live in close association with roots. Relatively few field studies
have probed soil microbial changes, but recently, reports indicate several potentially important
changes. With supplemental UV-B radiation above ground36 mycorrhizae, fungi that are
associated with roots and important for plant mineral nutrition, were substantially decreased in
quantity (by ca 20%). Zaller et al.14 reported a reduction in mycorrhizae in a sedge fen with
solar UV-B radiation attenuation, even though root production had increased.
Apart from mycorrhizae, other soil fungi, bacteria, and microfauna inhabit soils and participate
in important ecosystem functions such as nutrient cycling (Chapter 5). UV-B radiation
treatments above ground can be manifested in several changes in populations of these
belowground organisms and also in some apparent changes in the soil environment. For
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
example, in Greenland, although attenuating solar UV-B radiation above ground did not affect
total microbial biomass, it did result in qualitative changes (indicated by lipid biomarkers that
reflect composition of microbial groups) in the soil microbial communities.13 In southern
Finland, UV-B radiation supplementation led to changes in exudations from roots of two heath
species growing in peatland microcosms. The two heath species reacted quite differently to the
UV-B radiation supplementation treatment. The differences in root exudations were also
reflected in the soil microbial biomass.15 Similar findings of altered root exudations were
reported from UV-B radiation supplementation experiments in a grassland in the United
Kingdom, but only if the soil had been disturbed.37 In Antarctica, solar UV-B radiation
attenuation led to an altered soil microbial community and this was thought to be due to altered
quantity and/or quality of root exudates.38 Root exudations are quite important, since these
provide significant amounts of the energy and carbon for soil microbial communities.39 Changes
in the quantity and quality of root exudations, if reflected in changes in the soil microbial
function, can have important implications for soil nutrients and carbon (Chapter 5). In northern
Sweden, UV-B radiation supplementation over a 5-year period with and without elevated CO2
treatments were used to test soil microbial responses in field experiments.40 The aboveground
sub-Arctic heath vegetation was not greatly affected by these treatments. However, there were
sizeable changes in bacterial community structure due to the supplemental UV-B radiation, such
as alterations in the nature of carbon use profiles, decreased microbial carbon and increased
microbial nitrogen. Other studies also suggest that UV-B-radiation-induced changes in plant
chemistry have the potential to affect the interactions between plants and N-fixing symbiotic
bacteria, as will be discussed later.
Convey et al.41 reported that near ambient solar UV-B radiation decreased the prevalence of a
prominent soil-dwelling microarthropod species in Antarctic soils where these field studies were
performed. This was more pronounced in the springtails than the mites. Since these soil insects
are not directly exposed to solar radiation, the effects were assumed to have been mediated by
UV-B-induced changes in the vegetation.
As with soil, sunlight penetrates no more than a few millimeters into the surface of peat42, yet
many changes in the subsurface milieu of peatbogs have been found, including changes in the
predominance of various microfauna (testate amoeba, rotifers, mites, and nematodes) and in the
abundance and species diversity of microfungi (Figure 3- 2). Testate amoebae
consistently increased with near-ambient UV-B radiation compared to the attenuated UV-B
radiation treatment, although fungal species diversity decreased only to a small degree.42-44
These changes were linked to increases in dissolved organic carbon and phosphates in the peat
subsurface environment44 (Figure 3-2). Although the significance of these changes in root mass,
apparent root exudations, microbiological and abiotic chemical changes is not known, there are
important potential implications for carbon sequestration and nutrient cycling in ecosystems
(Chapter 5).
Interactions between UV-B radiation and other climate change factors
Several environmental factors have been shown to modify UV-B-induced responses of plants,
either ameliorating or enhancing the UV-B radiation effect. Furthermore, UV-B radiation can
alter the way in which plants respond to other factors such as temperature extremes.
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
On a global scale, CO2 is clearly increasing rapidly and uniformly throughout the world. Other
environmental variables such as temperature and UV-B radiation are increasing to various
degrees at different latitudes, while water supply is changing in a less predictable manner.
Additionally, biologically available nitrogen is increasing substantially in many regions.
Tropospheric ozone is also elevated in many regions, and some of this increase is the result of
enhanced UV-B radiation resulting from stratospheric ozone reduction (Chapter 6). A few
studies of the interaction of elevated ozone and enhanced UV-B radiation have been conducted
as discussed in the 2003 report,22 but newer studies are not available.
Experiments designed to explore interactions of these factors with UV-B radiation are useful to
determine potential effects in the future. However, those experiments manipulating two or,
sometimes more factors simultaneously are necessarily more logistically difficult to conduct.
Thus, most have been carried out under conditions that can depart from those in nature and
therefore constrain how much they might represent plant responses in nature. Furthermore, most
of these experiments have been conducted with isolated plants or plots of plants rather than in
intact ecosystems, and most only analyzed direct UV-B radiation effects on plants aboveground.
Elevated CO2, temperature and UV radiation
One of the most interesting questions to be answered by interaction studies is whether increases
in CO2 and temperature can counteract negative effects of UV-B radiation, or whether
synergistic or additive negative effects might occur. In our previous report, we found these
synergistic effects to be rare.22 Several studies using sunlit controlled environment chambers to
manipulate UV-B radiation, temperature and CO2 have been reported recently. The chambers
were very useful in controlling these factors, but may have compromised the realism in relation
to field conditions due to the high UV levels employed and the removal of solar UV-A radiation
by the chamber material. Koti et al.45 reported that higher temperatures and UV-B radiation,
either singly or in combination, had detrimental effects on soybean flower and pollen
characteristics. Elevated CO2 by itself had a small beneficial effect in some soybean varieties,
but had no ameliorating effects on the decidedly detrimental effect of high temperature and high
UV-B radiation on pollen morphology, production, or germination. The results further suggest
that these combinations of environmental factors ultimately would negatively affect fruit set and
soybean yield.45
In the same type of sunlit chambers, other factor interaction studies have been conducted with
cotton.46-49 Very high fluxes of UV-B radiation detrimentally affected leaf physiological
activities such as photosynthesis and foliage development, though this did not occur with
moderate UV-B radiation levels. Elevated CO2 enhanced growth, but did not counteract the
detrimental effects of the high UV-B flux.47, 48 High temperature and UV-B radiation both
reduced cotton fruit production.49 Higher temperatures increased the fraction of leaves abscising,
while UV-B radiation only had an effect on abscission in the high temperature treatment. Both
higher temperatures and UV-B radiation increased fruit fall, especially in combination.
study involving the interaction of CO2 and UV-B radiation conducted in conventional growth
chambers, rather than sunlit chambers, tested potential ameliorating influence of elevated CO2 on
UV-B radiation effects for canola.50 Several physiological and morphological characteristics
were assessed. For some traits such as plant height, elevated CO2 did counteract the tendency of
UV-B radiation to decrease plant height. However, these studies were conducted in low-light
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conditions compared with natural sunlight so their results may be difficult to extrapolate to
nature.
While in the above example higher temperatures could be considered detrimental, there are
situations where higher temperatures facilitate physiological processes that are protective.
Tropical legumes exposed to elevated UV-B radiation were less detrimentally affected if they
were simultaneously exposed to higher temperatures. This has been attributed to the heatstimulated synthesis of “heat shock” proteins by the plants.51 In another study, UV-B radiation
increased heat tolerance considerably in cucumber plants grown in growth chambers.52
In field studies, freezing tolerance in rhododendron was increased by UV-B radiation exposure53
which corroborated earlier studies for this species.54 Freezing tolerance of jack pine was
similarly increased by UV-B radiation and this was linked to induction of secondary compounds
(phenolics) in plant tissues.55 This latter study was also conducted in growth chambers. The
effect of UV-B radiation on frost hardiness in seedlings of several conifer species from
southwestern Canada was investigated under greenhouse conditions.56 Frost tolerance of four
species decreased and the tolerance increased for another three species. Heat tolerance of two
conifer species increased. These changes in frost and heat tolerance were only apparent if very
high UV-B fluxes were employed so the applicability of these findings for conifer seedlings in
nature may be limited.
Drought and UV radiation
In a controlled environment study, several clover varieties were compared under combined
treatments of drought and high UV-B fluxes.57 Drought and UV-B radiation interacted
synergistically resulting in a substantial increase of UV-B radiation- absorbing compounds,
including phenolics (flavonol glycosides), in drought-stressed plants. These changes were linked
with somewhat improved water status of the plants. The authors suggested that clover varieties
that are slow growing and adapted to other stresses such as drought are more likely to be UV-B
radiation tolerant. In contrast to the interactions reported by this study with clover, Turtola et
al.58 conducted a greenhouse study with willows and found few significant interactions between
water stress and UV-B radiation for various stress indicators. However, the visible light levels
were exceedingly low in the greenhouse and may have compromised the realism of these results.
Yang et al.59 conducted a greenhouse study using UV-B radiation supplementation and water
stress on two populations of an important shrub from the Tibetan Plateau of China used in land
restoration efforts. The low elevation population of this shrub was more sensitive to UV-B
radiation than to drought and the high elevation populations more sensitive to drought than UVB radiation supplementation. There were also significant interactions between these two stress
factors. For example, in the high elevation population, enhanced levels of UV-B radiation
tended to somewhat alleviate the effects of drought on decreased plant dry mass, and increased
the levels of a plant hormone (abscisic acid) that is known to mediate plant responses to water
stress.
In a field study60 in which solar UV radiation was manipulated by filters, productivity was
decreased and forage quality (including nitrogen content and digestibility) increased with nearambient UV radiation for the dominant grass species in a dry, but not in a wet year. Since
foliage with higher forage quality decomposes more readily, solar UV radiation and drought
could reduce both grass biomass and soil organic matter for this dominant species. In another
grass species, productivity decreased due to near ambient UV radiation, but only in wet years.
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Forage quality of this species did not change. The variable responses observed among species
grown under changing conditions of soil moisture availability and UV radiation suggest that with
current solar UV radiation, as drought becomes more prevalent with global change in the
shortgrass-steppe ecosystem, the structure and function of this ecosystem may change
substantially.60 This is one of the few studies of climate change factors involving UV radiation
that has been conducted in the field in an intact ecosystem. However, the UV radiation
manipulations included a sizeable amount of UV-A as well as UV-B radiation removal, so the
relevance for ozone depletion is limited. Current levels of solar UV radiation is playing an
important role in this system, but it is not clear if an increase in the UV-B component due to
ozone depletion would enhance the UV radiation effects on grass growth and foliage quality.
Nitrogen and UV-B radiation
Increasing nitrogen supply to plants may result in additional sensitivity to UV-B radiation. The
interaction of nitrogen and UV-B radiation is relevant to areas of nitrogen deposition from
pollution and in agricultural areas where nitrogen is intentionally applied.2 In field experiments,
supplemental UV-B radiation simulating ozone depletion caused reduced total biomass, nitrogen
content and specific pigment concentrations for a South African legume species (Cyclopia
maculata), but the UV-B radiation effect was much more pronounced when the plants were
supplied with supplemental nitrate.61 In another field study with enhanced UV-B radiation in
Portugal, net photosynthesis of maize was less affected by UV-B radiation at low nitrogen
supply than at high nitrogen levels. Furthermore, with elevated UV-B radiation, the
responsiveness to plant nitrogen nutrition was decreased.62 However, shoot length of a
freshwater higher plant species was reduced by high fluxes of UV-B radiation and this radiation
effect was exacerbated by low nitrogen levels in the plant.63 A study with potted tree seedlings
of two birch species conducted outdoors64 showed effects of different levels of UV-B radiation
and nitrogen. There was no apparent growth response to supplemented UV-B radiation, but a
positive growth response to greater nitrogen supply. Supplemental UV-B radiation did affect the
phenolic constituents of the birch species, but not in a uniform manner for the two species tested.
The different levels of nitrogen supply yielded a diversity of responses in the two birch species
for both phenolics and tannins. However, there were no interactions between UV-B radiation
and nitrogen levels in these responses.
Symbiotic nitrogen fixation by micro-organisms in specialized nodules on plant roots is an
important source of nitrogen for plants and also for neighboring plants that do not have the
capacity to form nodules. Nodulation of bean plant roots was found to be stimulated
substantially by UV-B radiation in outdoor experiments.65 This positive effect of UV-B
radiation on nodulation was accompanied by a large increase in UV-B-absorbing compounds in
the root system. In contrast to the study of Pinto et al., elevated levels of UV-B radiation
decreased nodulation in some species of grain legumes in a study by Rajendiran et al..66
Additional studies by Chimphango et al.61, 67 did not find an effect of elevated UV-B radiation on
nodulation; however, they speculated that very high UV-B flux might inhibit nodulation. In
summary, the available information suggests that increases in nitrogen supply can increase UV-B
radiation sensitivity, at least in those species where higher nitrogen levels result in a reduced
synthesis of protective UV-absorbing compounds.61 On the other hand, moderate increases in
UV-B radiation are likely to have only modest consequences on nitrogen fixation by symbiotic
bacteria.
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Where interactions between UV-B radiation and nitrogen supply occur, these can also modulate
plant responses to other organisms. In a recent outdoor study using potted grapevines,
application of high levels of nitrogen together with below-ambient UV radiation modified the
susceptibility of some grapevines to powdery mildew disease. This was evident in a high
incidence of infection when UV-B radiation was attenuated that was related, among other plant
physiological and anatomical features, to low concentrations of specific phenolic compounds
(flavonol glycosides and hydroxycinnamic acid derivatives) and less leaf wax.68
Mechanisms of plant responses to solar UV-B radiation
Since our last report,22 there has been a substantial increase in understanding the mechanisms
that mediate the responses of terrestrial plants to solar UV-B radiation. This progress is
important because it improves our ability to understand the effects of UV-B radiation on
organisms and their ecological interactions and to devise strategies for improving plant tolerance
to UV-B radiation in species of economic interest. In addition, it also serves to highlight the
importance of climate change interactions.
Three generalizations about ecophysiological impacts of UV-B radiation have emerged from
work carried out under field conditions mostly using natural or moderately-enhanced levels of
UV-B radiation.3, 22 Firstly, solar UV-B radiation frequently has an inhibitory effect on plant
growth, although this effect is generally small (<20%) and is more pronounced among
herbaceous species than in woody perennials. Secondly, solar UV-B radiation elicits a variety of
acclimation responses, which typically include increased activity of antioxidant enzymes,
increased DNA repair capacity, and accumulation of phenolic compounds that serve as
“sunscreens” or UV filters. Thirdly, plant exposure to solar UV-B radiation frequently has large
effects on the interactions between plants and consumer organisms. In this section we will
briefly describe some of the most recent advances in our understanding of the mechanisms
underlying some of these plant responses.
Growth inhibition
Growth inhibition at the whole-plant level often correlates with reduced leaf expansion, which
appears to be more sensitive to UV-B radiation than photosynthesis per unit leaf area.34, 69, 70
CO2 assimilation (net photosynthesis) per unit leaf area is largely unaffected by solar UV-B
radiation,7, 34, 70 and detailed studies have demonstrated that the integrity of part of the
photosynthetic system (photosystem II) is not affected by ambient or moderately enhanced levels
of UV-B radiation under field conditions.10, 71 In a model system, using the primary leaf of
wheat to study growth reduction, Hopkins et al.72 found that leaves responded to UV-B radiation
with changes in the rate and extent of cell division and elongation. This resulted in a decreased
and retarded elongation leading to the reduced growth observed.
Reactive oxygen species. The inhibition of leaf growth by solar UV-B radiation may result
from accumulation of UV-B-induced damage to key macromolecules and cellular structures. In
living tissues, molecular oxygen may react to form reactive oxygen species (ROS), which
include superoxide radicals, hydroxyl radicals, hydrogen peroxide, singlet oxygen and reactive
nitrogen. All these molecules are potentially highly destructive, since they participate in many
chemical reactions with lipids, proteins and nucleic acids resulting, for example, in damage to
cell membrances due to lipid peroxidation.73-75 However, recent evidence has indicated that in
low concentrations they also function as signaling molecules (c.f. 75, 76, 77) implicated in
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modulating normal plant development, including senescence (ageing) and many other
physiological processes.78 To date, much research has focused on these oxidant signals as well
as their interrelationship with several key hormones and stress-induced proteins. Disease and
climate change factors such as increased levels of UV-B radiation, temperature extremes,
drought, and ozone can stimulate elevated amounts of ROS.79-83
UV-B radiation enhances the expression of several genes involved in natural senescence
phenomena84 where ROS are implicated.85, 86 Apart from their role in accelerated ageing and
other developmental processes, ROS, including nitric oxide,87 also function in triggering defense
mechanisms against a range of stress factors including UV-B radiation, temperature, drought,
herbivore attack and disease.88-91 The increased ROS levels are thought to activate intricate
signaling networks that eventually result in internal regulation and plant acclimation to the
altered environmental conditions. In addition to ROS, the defense-related growth regulators
salicylic acid, jasmonic acid and ethylene have been implicated in the mediation of plant stress to
changes in UV-B radiation.92, 93
DNA damage. It is also possible that solar UV-B radiation generates DNA damage at a rate that
overburdens DNA repair mechanisms, leading to transient accumulation of toxic DNA
photoproducts. Two basic photoproducts result from the absorption of UV-B photons by DNA:
the cyclobutane pyrimidine dimer (CPD), which is thought to be quantitatively the most
important (about 75% of the lesions), and the pyrimidine (6–4)-pyrimidone photoproduct (6–4
PP). Both of these lesions can have toxic and mutagenic effects and can impair DNA
transcription and replication.94 Mutants that are deficient in DNA repair mechanisms are more
sensitive to UV-B radiation than wild-type plants.95-97
The relative importance of DNA photodamage in UV-B-induced growth inhibition has been
tested recently in developing plants. A native herb from southern Patagonia, Gunnera
magellanica, was exposed to a gradient of UV-B radiation from zero to moderate UV-B fluxes in
a greenhouse study. Leaf expansion was measured as an indicator of plant growth and other
techniques were used to detect damage to DNA (in the form of CPDs) and lipid peroxidation.
Leaf expansion decreased and the CPD density increased with increasing UV-B radiation,
although the degree of lipid peroxidation remained unaffected. The highest UV-B flux induced
only a transient oxidative stress. These results suggested that at UV-B fluxes within the range
that G. magellanica plants experience in their natural environment, DNA damage may be a
factor in growth inhibition.98 Field work in southern Patagonia has shown that the rates of CPD
repair in G. magellanica plants were modest in comparison with other species and, under
equivalent conditions, were about 50% lower than the repair rates of the model plant Arabidopsis
thaliana.99 This low DNA repair capacity may be one of the reasons why the midday CPD load
in naturally occurring plants of G. magellanica was linearly correlated with UV-B fluxes in the
hours before midday.100
Using relatively high UV-B radiation, studies in rice add further support to the idea that DNA
damage in the form of CPDs may be one of the main determinants of UV-B-induced growth
inhibition in plants grown under physiologically meaningful conditions.101 This work
demonstrated that there is natural variation among rice cultivars in DNA repair capacity, and that
slight variations in photolyase (the enzyme involved in CPD repair) activity have consequences
for the ability of rice plants to tolerate the growth-inhibitory effects of UV-B radiation.
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Growth-inhibitory effects of ambient UV-B radiation have been detected in herbaceous species
of the Tierra del Fuego National Park,3 and also in the two species of vascular plants that occur
in the Antarctic peninsula.9 Low DNA repair capacity may be a general feature of these species
of this high-latitude region, which have evolved under low levels of ambient UV-B radiation.
Repair mechanisms may also be affected by other prevailing conditions when plants are exposed
to UV-B radiation, for example by water availability and temperature. This was demonstrated in
a lichen species (Cladonia arbuscula), where exposure to UV-B radiation in a dried state
resulted in deficient repair of DNA damage, evidenced by accumulation of CPDs. At low
temperatures (2 oC) DNA damage was also not repaired even though the lichens were in a
hydrated state.102
Acclimation response
Under field conditions, plants generally adapt to changes in UV-B radiation by activating an
array of protective responses that include morphological changes,34, 103 increased DNA repair
capacity,97 induction of protective compounds (sunscreens)7, 104-107 and increased levels of
antioxidants.108
Of all the acclimation responses, the best characterized is the accumulation of UV-absorbing
sunscreens. These sunscreens include phenolic compounds derived from phenylalanine
(flavonoids and other phenylpropanoid derivatives, such as sinapate esters) that accumulate in
large quantities in the vacuoles of epidermal cells and effectively attenuate the UV component of
sunlight with minimal change in the visible region of the spectrum. Various studies have
suggested that certain flavonoid compounds serve not only a UV-screening/filtering function, but
also an antioxidant function.109-111 This has been further supported by recent work.57, 112
Furthermore, those flavonoids with potential antioxidant properties have also been reported to
increase differentially in response to drought stress.113
UV-B perception and signaling in UV-B radiation acclimation. A considerable body of work
has continued to reveal details of how these protective responses are activated when plants are
exposed to UV-B radiation (Figure 3- 3). However, our understanding of the mechanisms of
UV-B response in higher plants is still fragmentary.
Potential pathways of UV-B perception and signaling have been partially characterized, largely
under laboratory conditions.85, 93, 114-120 UV-B-induced patterns of gene expression have been
characterized under controlled environment conditions,121, 122 and also in field and greenhouse
experiments.123-126 Changes in gene expression have been observed in tissues not directly
exposed to UV-B, implying transmission of a signal from irradiated to non-irradiated tissues.125
One of the major gaps in our understanding of UV-B perception is that the nature of the primary
UV-B photoreceptors is still not well defined. Data derived from the large number of research
reports cited in this chapter, as well as work done in animal models, would indicate that DNA
damage may act directly as a major trigger of molecular UV-B radiation response (Figure 3- 3).
However, it has been known for some time that the action spectra for the induction of several
UV-B responses do not match the action spectrum for DNA damage.127 In addition, several
responses to UV-B radiation cannot be mitigated by treatments that ameliorate DNA damage117
and they are not exacerbated in mutant plants deficient in DNA damage repair.128 In a study
where plants were pre-acclimated to UV-B radiation during growth,129 it was reported that the
expression of a gene involved in UV screening pigment induction (chalcone synthase) did not
occur, although high levels of DNA damage were observed. However, without the acclimation
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treatment, the chalcone synthase gene was strongly activated with only low levels of DNA
damage occurring. Therefore, in these cases, additional mechanisms of UV-B radiation
perception and signaling have to be considered.
There are several lines
of evidence suggesting
that plants have specific
UV-B photoreceptors,
analogous to the
photoreceptors involved
in the perception of
visible light and far-red
radiation (phytochromes, cryptochromes, and phototropins) (Figure 3- 3,
for a review, see Ulm
and Nagy130). However, attempts to
identify these receptors
using photophysiological techniques and,
more recently, genetic
approaches with the
model plant
Arabidopsis thaliana,
have met with little
success.
Figure 3-3. Mechanisms of plant response to solar UV-B radiation. Three general
effects of solar UV-B on plants have been documented in field experiments: Growth
inhibition (e.g., reduced leaf area expansion), acclimation (e.g. increased
accumulation of UV-absorbing sunscreens), and alteration of plant interactions with
organisms at other trophic levels (e.g., increased plant resistance to leaf-eating
insects). Some of these responses can be directly linked to effects of solar UV-B on
key cellular components (e.g., DNA lesions caused by UV-B photons may have
inhibitory effects on plant growth). Other responses are triggered by the activation
of intricate signaling networks that involve a number of signaling elements, in some
instances including a UV-B-specific regulatory protein (UVR8), and in others, ROS
and defense-related hormones, such as salicylic acid and jasmonic acid. Some of the
signaling components appear to be shared by response circuits that are activated by a
diverse group of environmental stressors (e.g., UV-B, drought, herbivory, etc.).
Activation of overlapping signaling cascades by different stressors results in
overlapping gene expression patterns and convergent physiological responses.
Elucidation of these mechanisms will facilitate the understanding of the interactive
effects of solar UV-B radiation and other environmental factors on plant growth and
ecological relationships.
A recent study119 led to
the characterization of
the first UV-B-specific
signaling pathway,
which is regulated by
the protein UVR8 and
controls the expression
of numerous genes
involved in UV-B
protection and
acclimation. The list of
genes regulated by UVR8 includes most of the genes involved in the biosynthesis of flavonoids
(protective pigments), the gene encoding CPD photolyase, PHR1 (which is essential for repair of
UV-B-induced DNA damage), and genes concerned with protection against oxidative stress and
photooxidative damage. A combination of molecular and genetic approaches has established
that the transcription factor, HY5, is a key downstream effector of the UVR8 pathway. UVR8
regulates transcript levels of HY5 specifically in response to UV-B, and HY5 in turn regulates
the expression of a substantial number of genes involved in UV protection. Previous work122 has
demonstrated that the effects of low levels of UV-B on the expression of a subset of genes
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required HY5, but was independent of previously described photoreceptors. At present there is
growing consensus that UVR8 and HY5 orchestrate specific acclimation responses to UV-B
radiation; however, the photoreceptor and early signaling components that are activated by UVB radiation and eventually engage the UVR8 pathway remain to be elucidated.
For some effects of UV-B radiation on plants, a significant overlap has been documented
between cellular responses activated by UV-B radiation and other environmental stress factors,
such as tropospheric ozone, pathogen, and herbivore attack. This overlap has been evidenced by
the occurrence of convergent patterns of gene expression (e.g.(Izaguirre, 2003 #68;Sävenstrand,
2002 #139}) activating of common signaling components (e.g., Holley et al.131, reviewed in
Stratmann115), and induction of similar defense molecules and secondary metabolites.132 A
possible explanation for this overlap is based on the activation of common signaling
intermediates, such as ROS and defense-related growth regulators, as indicated in Figure 3-3.
Another possibility, at least in the case of overlaps between responses elicited by UV-B radiation
and attack by herbivorous insects, could be the activation of common cell surface receptors by
UV-B radiation and insect elicitors, as hypothesized by Stratmann115(Figure 3-3). Current
experiments directed to testing this hypothesis will improve our understanding of the
mechanisms of UV-B radiation effects on plants, and provide novel insights into the problem of
increasing UV-radiation tolerance and resistance to insect pests in cultivated species. The
existence of overlapping signaling components leading to a response may have important
functional implications, because environmental stresses are seldom experienced by the plant in
isolation.
Plant interactions with consumer organisms
UV-B radiation and plant-animal interactions. Plant exposure to solar UV-B radiation
frequently results in a reduction in the level of insect herbivory (Figure 3-4 and reviewed in22, 133,
134
). Recent studies show that this anti-herbivore effect induced by UV-B radiation correlates
with a significant overlap between gene expression patterns induced by UV-B radiation and
wounding under controlled environmental conditions.121, 123 Components of signaling cascades
that are activated by wounding and herbivory are also activated by UV-B radiation.131
Furthermore, a number of plant products typically associated with anti-herbivore defenses, such
as defense-related proteins (e.g., proteinase inhibitors), and phenolic compounds (e.g.,
chlorogenic acid), accumulate in larger quantities in plants exposed to UV-B radiation than in
plants receiving no UV-B radiation.118, 135 The increases in defense-related compounds in plants
exposed to UV-B radiation correlate with a lower forage quality in tissues from these plants, as
evaluated using insect growth bioassays (e.g.,123, 136). Behavioral bioassays have also shown that
exposure to solar UV-B radiation can induce changes in the plants that reduce the attractiveness
of the plants to female adults at the time of oviposition.137 This effect of solar UV-B radiation
may have important effects on insect herbivory under field conditions by controlling the
distribution of plant-feeding larvae within the canopy.
UV-B radiation and pathogens. Severity of pathogen attack plays a determining role in plant
productivity in the field and greenhouses, and studies have shown that many environmental
factors modify both pathogen and plant response. Apart from precipitation patterns, temperature,
and time of day, UV radiation can also be a modifying factor. Recent work from a field study
indicated that species diversity was affected by solar UV-B radiation because of species-specific
sensitivity to the radiation.31 Besides the potential damaging effects of UV radiation, it also may
play a role as a light signal for many processes of plant pathogen development (see 134). UVThe Environmental Effects Assessment Panel Report for 2006
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radiation effects may influence pathogen development either directly or indirectly, the latter as a
consequence of UV-induced biochemical changes, which are reflected in interactions between
pathogen and host (for reviews see 138, 139). The initial events and signaling mechanisms
underlying these interactions are complex, and will be briefly discussed below.
There have been several reports
showing that UV radiation may
either decrease or increase fungal
attack (see 138). These attacks
depend on many interacting factors
such as temperature, light, time of
day and humidity as well as on plant
morphology and genetic
background.31, 68, 134, 138
UV-B radiation and pathogen
infection trigger both specifically
targeted defense responses as well as
initiating crosstalk between signaling
pathways.140, 141 For example, the
pathogen defense may result in
repression of the UV protective
Figure 3-4. An example of effects of solar UV-B radiation on insect
flavonoid biosynthetic pathway.140
In the latter study it was shown that herbivory in the field. The graph shows the effect of attenuating the
UV-B component of solar radiation on the intensity of insect
specific genes were activated by UV- herbivory by thrips (a piercing-sucking insect) in soybean crops, and
B radiation and subsequently
leaf beetles (chewing insects) in plants of the common annual weed
repressed by the pathogen elicitor,
Datura ferox (original data in21, 36). The marked effects of solar UVB radiation on leaf damage and insect population density are
demonstrating interaction between
proportionally much larger than any reported effects of solar UV-B
two specific signaling cascades,
radiation on plant growth and morphology.
whereby the pathogen signal was
perceived as the more important in plant defense and survival.140 Thus, overlap between abiotic
and biotic signaling suggests mutual interactions and response to different external pressures.
Induction of the so-called pathogenesis-related proteins (PR proteins) is another example of the
complexity of plant response to UV-B radiation and other environmental factors. These proteins
are found in many plants, not only in response to UV-B radiation117, 142, 143, but also after fungal,
bacterial, or viral attack as well as after exposure to certain organic chemicals or heavy metals.144
The signal transduction pathway for the synthesis of these PR proteins induced by UV-B
radiation is not yet fully elucidated and there appears to be crosstalk among different
communication pathways when the plant is exposed to multiple stresses such as pathogens and
UV-B radiation. A recent example of a PR protein induced by UV-B radiation is the enzyme, β1,3-glucanase I (ßGlu I)117, a protein widely found in seed plants, involved also in developmental
plant processes.145 A laboratory study conducted with beans (Phaseolus vulgaris) indicated that
the induction of the PR protein, βGlu I, was correlated with photoreversible DNA damage, which
has not been reported for other PR protein families. In addition, the results implicate the DNA
damage (seen as CPD formation) as a key player in the signaling pathway resulting in the
induction of βGlu I by UV-B radiation (Figure 3- 3). The plant response to UV-B radiation and
subsequent induction of the PR protein, βGlu I, were found to be local rather than systemic (the
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latter where the whole plant rather than a localized area would be affected by a stress). Studies
concerned with unraveling the complex internal plant pathways of communication are important
for our understanding of the consequences of interactions between UV-B radiation and other
stress factors, especially those related to climate change and modern agricultural practices.
Technical issues in conducting and evaluating UV-B radiation research
Biologically effective UV radiation
Biological spectral weighting functions (BSWFs) are factors assigned to different wavelengths
indicating their relative biological effectiveness and these functions have been developed for a
number of different plant processes. BSWFs have played a prominent role in the ozone
reduction issue. Their uses have included predicting the relative increment of “biologically
effective” UV radiation for a given increment in ozone depletion, evaluating latitudinal and
elevational gradients of solar UV radiation, and calculating how much supplemental UV
radiation to supply in experiments with UV-B-emitting lamps.
A single BSWF cannot be expected to apply to multiple plant responses or to be necessarily
appropriate for all plant species, much less to generalize to other trophic level effects. In our
report four years ago22 we introduced new work showing a BSWF for plant growth / mass
allocation effects which extended into the UV-A wavelengths with substantial effectiveness.
This weighting function was developed in the laboratory with seedlings of cultivated oat146 and
was subsequently validated in the field for this species.147 The importance of UV-A radiation in
causing plant responses has been confirmed by other recent studies.82, 148-150 For example, the
production of singlet oxygen, one of the two major representatives of damaging ROS, is
produced more effectively by UV-A than by UV-B radiation.82 Specifically, UV-A wavelengths
were twice as effective as UV-B wavelengths for inducing singlet oxygen. This is unique as
BSWFs for damage to other plant processes typically show a marked decline toward longer
wavelengths.
Evaluating weighting functions
There have been only a few attempts during the 1980's and 1990's to evaluate alternative BSWFs
under polychromatic radiation conditions.151 Many difficulties exist in evaluating BSWFs. In
many locations, filtered-sunlight experiments produce insufficient effects to yield consistently
measurable differences between different wavelength treatments. For example, even with the
high UV fluxes of Arizona, USA (33 N), a dose of >70% of ambient UV-B radiation was
typically needed before consistent statistically significant effects were seen in cotton and
sorghum.152 However, in most cases, it is likely that experiments combining modulated UV
lamp supplementation with different treatments of UV-filtered sunlight will be necessary to
continue testing BSWFs in the field. The total UV radiant flux removed in UV radiationattenuation studies is considerably greater than the added UV radiation in lamp-supplementation
studies. However, when treatments are weighted using BSWFs, the changes in biologically
effective radiation in the lamp-supplementation studies may be greater or equal to that removed
by the UV-B exclusion treatment. The relationship between filter and lamp treatments depends
on the BSWF employed. Rousseaux et al.106 compared treatments using filters and lamps for
lettuce and oat in a field experiment where particular care was taken to insure similar
microenvironmental conditions among all treatments. Overall, when comparing the two
treatment methods, plant growth and allocation changes followed a pattern similar to a plant
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DNA damage spectrum,153 emphasizing the importance of radiation in the UV-B to UV-A
transition zone. Responses of UV-absorbing compounds suggested less of an effect of these
longer wavelengths, approaching instead a response predicted by the generalized plant response
function.154
The spectral dependence for induction of UV-absorbing pigments was also examined in the
cultivated oat in a lamp/filter experiment and sorghum, pepper and kochia in a UV-attenuation
experiment.155 Despite the very different experimental UV fluxes, a BSWF extending into the
UV-A waveband with moderate effectiveness was most representative of the observed results for
the four species. The plant DNA damage spectra153 and a new flavonol induction BSWF with
similar spectral response148 were the most appropriate of the five BSWFs evaluated.155
Implications of using different BSWFs
This increasing evidence that plant BSWFs include significant UV-A radiation responses has
substantial implications for the design and interpretation of experiments investigating plant
response to ozone depletion. Best known among the uses of BSWFs is the calculation of
radiation amplification factors (RAFs). They have been used to compare the effects of current
levels of UV radiation with scenarios of ozone depletion. For small changes in ozone the RAF is
the increment of effect (biological or chemical) resulting from a 1% ozone depletion increment.
Thus a RAF of 1 would indicate a 1% increase in response. (Note in Chapter 1, only the
erythemal spectrum is used as a weighting function. This spectrum has a RAF of 1.2 at high sun
elevations. Erythema is the sunburn response of human skin.) The original generalized plant
response function154 has a RAF calculated at 1.6, while the RAF of the new growth / mass
allocation BSWF is 0.2 for the same conditions.156 This means that, if we accept the new plant
growth BSWF in place of the generalized plant response, the effects anticipated under a given
level of ozone reduction will be smaller than with the BSWF based on the generalized plant
response. Spectra such as those of Quaite et al.153 and Ibdah et al.148 would be intermediate, as
they have greater RAFs than the new plant growth / mass allocation BSWF but a lower RAF
than the generalized plant response.
Choice of BSWF will also have a bearing on experimental simulation of ozone depletion using
UV emitting lamps. This stems from several factors, but is primarily due to the substantial effect
of short wavelengths from the lamps in providing biologically effective irradiance when the
original generalized plant response154 is used. The new BSWF weights these short-wavelength
supplements proportionately less, and the lamps commonly used produce very little of the longer
wavelengths in this BSWF. In fact, when simulating ozone depletion in the field, the racks of
lamps may result in more shading of these longer wavelengths from the sun than they
generate.157 If we accept the new BSWF as appropriate, we have simulated a much lower level
of ozone depletion in past experiments than was intended. These implications extend to
controlled environments and greenhouses (or sunlit field chambers that do not transmit UV
radiation). “Controls” in these situations, rather than receiving ambient UV radiation, often
receive little UV, especially at shorter wavelengths. If the new BSWF is correct, these "controls"
are even further removed from ambient UV radiation levels than had been previously assumed.
In fact, even "treatment" UV levels, when weighted with this new BSWF in greenhouses or
controlled environments, may be below ambient UV radiation levels! This issue is worthy of
further quantitative evaluation.
82
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Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
The uncertainties in plant BSWFs remain significant, but may be addressed by new experimental
approaches. Values of RAF are sensitive to the range of wavelengths considered in their
calculation, especially the longest wavelength where the weighting function terminates, which is
usually in the UV-A region.158 It is often difficult to determine biological response to longer
wavelengths, thus adding additional uncertainty. Equipment such as the free electron laser
(FEL), has considerable potential to enhance our ability to resolve weighting functions in the
UV-A waveband.159
In the field, plant characteristics that are influenced by UV-B radiation would be expected to
change along latitudinal or elevation gradients in parallel with changes in biologically weighted
irradiance. Theoretically, this would provide an opportunity to test different spectral weighting
functions. An elevation gradient of UV-absorbing compound concentration in beech was
described by Neitzke and Therburg.160 There were higher concentrations with increasing
elevation, and these concentrations correlated significantly with erythemally weighted UV
radiation. However, they did not compare the relative increase in pigments with UV radiation
weighted with other BSWFs. Also, for a discriminating test of BSWFs, it would be useful if the
spectral distribution along the gradient changed appreciably.
These techniques provide routes to resolving plant BSWFs further. However, in the meantime,
reporting of UV doses calculated from several different BSWFs is recommended.161 This
permits retrospective evaluation of experiments as more understanding of organism spectral
responses develops.
UV dose-response relationships above and below ambient solar flux
A comparison of UV radiation-attenuation and supplementation approaches also begs the
question of the nature of the plant response pattern to increasing UV-B radiation, i.e., the doseresponse relationship. If biological responses exhibit an apparent saturation, the same increment
of biologically effective UV radiation will exert less effect at higher UV fluxes, such as in
supplementation experiments. Coleman and Day152 tested the dose-response relationship in their
UV radiation-attenuation experiments and did not see evidence of saturation as the UV radiation
approached ambient levels. Newsham et al.162 also did not find a saturation near ambient UV
radiation in their Antarctic experiments. However, neither study combined the graded UV
attenuation treatments with UV supplementation to test the dose-response relationship above
ambient UV radiation. Thus, this issue remains to be resolved.
Concluding remarks and gaps in knowledge
Since our last report22, there have been substantial advances in our understanding of the effects
of UV-B radiation on terrestrial ecosystems, especially in the elucidation of mechanisms of plant
response. A further area of highly interesting research emphasizes the importance of indirect UV
radiation effects on plants, pathogens, herbivores, soil microbes and ecosystem processes below
the surface. What was once considered the essence of understanding terrestrial ecosystem
responses to ozone column reduction, namely reductions in plant photosynthesis and production,
is now superseded by a much more complex picture of indirect UV radiation effects, trophic
level interplay, and microbial participation in ecosystem function.
Enticing questions remain regarding the extent to which systemic chemical and physical changes
in vegetation induced by UV-B radiation affect belowground systems. This includes roots and
closely associated microoranisms and microbial communities beyond the immediate root
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83
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
microenvironment with ramifications for soil processes such as nutrient cycling. These changes
in the belowground system are apparently mediated by the vegetation. It is recognized that well
replicated field studies are highly important to realistically evaluate effects altered UV radiation.
There is a particular paucity of field studies investigating the interactions of altered UV radiation
combined with changes in other climate change factors, at least in part owing to the technical
difficulties in conducting such studies.
Much has been learned about mechanisms of UV-B radiation action in plants and how resultant
changes interact with ecologically important processes such acclimation, growth inhibition,
plant-animal and plant-microbe interactions. A more detailed understanding of how UV-B
radiation modifies gene expression and resultant systemic changes in plant characteristics is
needed and will be useful in elucidating ecosystem-level changes. Research on the intricate and
sometimes overlapping network of signaling pathways induced by UV radiation and other
stimuli, such as pathogen attack, is important to understand why these sometimes overlap and
sometimes counteract one another.
Seemingly arcane technical issues, such as which are the most relevant biological spectral
weighting functions, count heavily in the conduct and evaluation of experiments designed to
assess plant and ecosystem response to UV radiation changes. Thus, further refinement and
testing of BSWF are of considerable priority.
References
1
2
3
4
5
6
7
8
84
IPCC, Climate Change 2001: The scientific basis Contribution of Working Group I to the
Third Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge
University Press, Cambridge, U.K., 2001.
Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger
WH, Tilman DG, Technical report: Human alteration of the global nitrogen cycle: Sources
and consequences, Ecol. Appl., 1997, 7, 737-750.
Ballaré CL, Rousseaux MC, Searles PS, Zaller JG, Giordano CV, Robson TM, Caldwell
MM, Sala OE, Scopel AL, Impacts of solar ultraviolet-B radiation on terrestrial ecosystems
of Tierra del Fuego (southern Argentina). An overview of recent progress, J. Photochem.
Photobiol. B., 2001, 62, 67-77.
Phoenix GK, Gwynn-Jones D, Lee JA, Callaghan TV, Ecological importance of ambient
solar ultraviolet radiation to a sub-arctic heath community, Plant. Ecol., 2002, 165, 263273.
Robson TM, Pancotto VA, Flint SD, Ballaré CL, Sala OE, Scopel AL, Caldwell MM, Six
years of solar UV-B manipulations affect growth of Sphagnum and vascular plants in a
Tierra del Fuego peatland, New. Phytol., 2003, 160.
Rozema J, Boelen P, Blokker P, Depletion of stratospheric ozone over the Antarctic and
Arctic: Responses of plants of polar terrestrial ecosystems to enhanced UV-B, an
overview, Environ. Pollut., 2005, 137, 428-442.
Searles PS, Flint SD, Caldwell MM, A meta-analysis of plant field studies simulating
stratospheric ozone depletion, Oecologia, 2001, 127, 1-10.
Day TA, Ruhland CT, Grobe CW, Xiong F, Growth and reproduction of Antarctic vascular
plants in response to warming and UV radiation reductions in the field, Oecologia, 1999,
119, 24-35.
The Environmental Effects Assessment Panel Report for 2006
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
Day TA, Ruhland CT, Xiong FS, Influence of solar ultraviolet-B radiation on Antarctic
terrestrial plants: Results from a four year field study, J. Photochem. Photobiol. B., 2001,
62, 78-87.
Xiong FS, Day TA, Effect of solar ultraviolet-B radiation during springtime ozone
depletion on photosynthesis and biomass production of Antarctic vascular plants, Plant.
Physiol., 2001, 125, 738-751.
Ruhland CT, Xiong FS, Clark WD, Day TA, The influence of ultraviolet-B radiation on
growth, hydroxycinnamic acids and flavonoids of Deschampsia antarctica during
springtime ozone depletion in Antarctica, Photochem. Photobiol., 2005, 81, 1086-1093.
Robinson SA, Turnbull JD, Lovelock CE, Impact of changes in natural ultraviolet radiation
on pigment composition, physiological and morphological characteristics of the Antarctic
moss, Grimmia antarctici, Glob. Change Biol., 2005, 11, 476-489.
Rinnan R, Keinänen MM, Kasurinen A, Asikainen J, Kekki TK, Holopainen T, Ro-Poulsen
H, Mikkelsen TN, Michelsen A, Ambient ultraviolet radiation in the Arctic reduces root
biomass and alters microbial community composition but has no effects on microbial
biomass, Glob. Change Biol., 2005, 11, 564-574.
Zaller JG, Caldwell MM, Flint SD, Scopel AL, Sala OE, Ballaré CL, Solar UV-B radiation
affects below-ground parameters in a fen ecosystem in Tierra del Fuego, Argentina:
Implications of stratospheric ozone depletion, Glob. Change Biol., 2002, 8, 867-871.
Rinnan R, Gehrke C, Michelsen A, Two mire species respond differently to enhanced
ultraviolet-B radiation: Effects on biomass allocation and root exudation, New. Phytol.,
2006, 169, 809-818.
Heyer WR, Ultraviolet-B and amphibia, Bioscience., 2003, 53, 540-541.
Blaustein AR, Kats LB, Amphibians in a very bad light, Bioscience., 2003, 53, 1028-1029.
Licht LE, Shedding light on ultraviolet radiation and amphibian embryos, Bioscience.,
2003, 53, 551-561.
Leinaas HP, UV tolerance, pirmentation and life forms in high Arctic Collembola, in UV
radiation and Arctic ecosystems ed.: Hessen DO, Springer-Verlag, Berlin, 2002, pp. 123134.
Mazza CA, Zavala J, Scopel AL, Ballaré CL, Perception of solar UVB radiation by
phytophagous insects: Behavioral responses and ecosystem implications, Proc. Nat. Acad.
Sci. USA., 1999, 96, 980-985.
Mazza CA, Izaguirre MM, Zavala J, Scopel AL, Ballaré CL, Insect perception of ambient
ultraviolet-B radiation, Ecol. Lett., 2002, 5, 722-726.
Caldwell MM, Ballaré CL, Bornman JF, Flint SD, Björn LO, Teramura AH, Kulandaivelu
G, Tevini M, Terrestrial ecosystems, increased solar ultraviolet radiation and interactions
with other climatic change factors, Photochem. Photobiol. Sci., 2003, 2, 29-38.
Braga GUL, Flint SD, Miller CD, Anderson AJ, Roberts DW, Both solar UVA and UVB
radiation impair conidial culturability and delay germination in the entomopathogenic
fungus Metarhizium anisopliae, Photochem. Photobiol., 2001, 74, 734-739.
Kadivar H, Stapleton AE, Ultraviolet radiation alters maize phyllosphere bacterial
diversity, Micro. Ecol., 2003, 45, 353-361.
Rangel DEN, Bragaa GUL, Flint SD, Anderson AJ, Roberts DW, Variations in UV-B
tolerance and germination speed of Metarhizium anisopliae conidia produced on insects
and artificial substrates, J. Invertebr. Pathol., 2004, 87, 77-83.
The Environmental Effects Assessment Panel Report for 2006
85
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
86
Mühlenberg E, Stadler B, Effects of altitude on aphid-mediated processes in the canopy of
Norway spruce, Agric. Forest Entomol., 2005, 7, 133-143.
Moody SA, Paul ND, Björn LO, Callaghan TV, Lee JA, Manetas Y, Rozema J, GwynnJones D, Johanson U, Kyparissis A, Oudejans AMC, The direct effects UV-B radiation on
Betula pubescens litter decomposing at four European field sites, Plant. Ecol., 2001, 154,
29-36.
Zucconi L, Ripa C, Selbmann L, Onofri S, Effects of UV on the spores of the fungal
species Arthrobotrys oligospora and A. ferox, Polar Biol., 2002, 25, 500-505.
Hughes KA, Lawley B, Newsham KK, Solar UV-B radiation inhibits the growth of
Antarctic terrestrial fungi, Appl. Environ. Microbiol., 2003, 69, 1488-1491.
Pancotto VA, Sala OE, Cabello M, Lopez NI, Robson TM, Ballaré CL, Caldwell MM,
Scopel AL, Solar UV-B decreases decomposition in herbaceous plant litter in Tierra del
Fuego, Argentina: Potential role of an altered decomposer community, Glob. Change Biol.,
2003, 9, 1465-1474.
Ulevicius V, Peciulyte D, Lugauskas A, Andriejauskiene J, Field study on changes in
viability of airborne fungal propagules exposed to UV radiation, Environ. Toxicol., 2004,
19, 437-441.
Jacobs JL, Carroll TL, Sundin GW, The role of pigmentation, ultraviolet radiation
tolerance, and leaf colonization strategies in the epiphytic survival of phyllosphere bacteria,
Micro. Ecol., 2005, 49, 104-113.
Austin AT, Vivanco L, Plant litter decomposition in a semi-arid ecosystem controlled by
photodegradation, Nature, 2006, 442, 555-558.
Ballaré CL, Scopel AL, Stapleton AE, Yanovsky MJ, Solar ultraviolet-B radiation affects
seeding emergence, DNA integrity, plant morphology, growth rate, and attractiveness to
herbivore insects in Datura ferox, Plant. Physiol., 1996, 112, 161-170.
Zavala JA, Scopel AL, Ballaré CL, Effects of ambient UV-B radiation on soybean crops:
Impact on leaf herbivory by Anticarsia gemmatalis, Plant. Ecol., 2001, 156, 121-130.
van de Staaij JWM, Rozema J, van Beem A, Aerts R, Increased solar UV-B radiation may
reduce infection by arbuscular mycorrhizal fungi (AMF) in dune grassland plants:
Evidence from five years of field exposure, Plant. Ecol., 2001, 154, 171-177.
Avery LM, Thorpe PC, Thompson K, Paul ND, Grime JP, West HM, Physical disturbance
of an upland grassland influences the impact of elevated UV-B radiation on metabolic
profiles of below-ground micro-organisms, Glob. Change Biol., 2004, 10, 1146-1154.
Avery LM, Lewis Smith RI, West HM, Response of rhizosphere microbial communities
associated with Antarctic hairgrass ( Deschampsia antarctica) to UV radiation, Polar Biol.,
2003, 26, 525-529.
Toal ME, Yeomans C, Killham K, Meharg AA, A review of rhizosphere carbon flow
modelling, Plant and Soil, 2000, 222, 263-281.
Johnson D, Campbell CD, Lee JA, Callaghan TV, Gwynn-Jones D, Arctic microorganisms
respond more to elevated UV-B radiation than CO2, Nature, 2002, 416, 82-83.
Convey P, Pugh PJA, Jackson C, Murray AW, Ruhland CT, Xiong FS, Day TA, Response
of Antarctic terrestrial microarthropods to long-term climate manipulations, Ecol., 2002,
83, 3130-3140.
Searles PS, Kropp BR, Flint SD, Caldwell MM, Influence of solar UV-B radiation on
peatland microbial communities of sourthern Argentina, New. Phytol., 2001, 152, 213-221.
The Environmental Effects Assessment Panel Report for 2006
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
Robson TM, Pancotto VA, Ballare CL, Sala OE, Scopel AL, Caldwell MM, Reduction of
solar UV-B mediates changes in the Sphagnum capitulum microenvironment and the
peatland microfungal community, Oecologia, 2004, 140, 480-490.
Robson TM, Pancotto VA, Scopel AL, Flint SD, Caldwell MM, Solar UV-B influences
microfaunal community composition in a Tierra del Fuego peatland, Soil. Biol. Biochem.,
2005, 37, 2205-2215.
Koti S, Reddy KR, Reddy VR, Kakani VG, Zhao D, Interactive effects of carbon dioxide,
temperature, and ultraviolet-B radiation on soybean (Glycine max L) flower and pollen
morphology, pollen production, germination, and tube lengths, J. Exp. Bot., 2005, 56, 725736.
Kakani VG, Reddy KR, Zhao D, Mohammed AR, Effects of ultraviolet-B radiation on
cotton (Gossypium hirsutum L) morphology and anatomy, Ann. Bot., 2003, 91, 817-826.
Zhao D, Reddy KR, Kakani VG, Read JJ, Sullivan JH, Growth and physiological responses
of cotton (Gossypium hirsutum L) to elevated carbon dioxide and ultraviolet-B radiation
under controlled environmental conditions, Plant. Cell. Environ., 2003, 26, 771-782.
Zhao D, Reddy KR, Kakani VG, Mohammed AR, Read JJ, Gao W, Leaf and canopy
photosynthetic characteristics of cotton (Gossypium hirsutum) under elevated CO2
concentration and UV-B radiation, J. Plant. Physiol., 2004, 161, 581-590.
Zhao D, Reddy KR, Kakani VG, Koti S, Gao W, Physiological causes of cotton fruit
abscission under conditions of high temperature and enhanced ultraviolet-B radiation,
Physiol. Plant., 2005, 124, 189-199.
Qaderi MM, Reid DM, Growth and physiological responses of canola (Brassica napus) to
UV-B and CO2 under controlled environment conditions, Physiol. Plant., 2005, 125, 247259.
Nedunchezhian N, Kulandaivelu G, Effects of ultraviolet-B enhanced radiation and
temperature on growth and photochemical activities in Vigna unguiculata, Biologia
Planta., 1996, 38, 205-214.
Teklemariam T, Blake TJ, Effects of UVB preconditioning on heat tolerance of cucumber
(Cucumis sativus L), Environ. Exp. Bot., 2003, 50, 169-182.
Chalker-Scott L, Scott JD, Elevated ultraviolet-B radiation induces cross-protection to cold
in leaves of Rhododendron under field conditions, Photochem. Photobiol., 2004, 79, 199204.
Dunning CA, Chalker-Scott L, Scott JD, Exposure to ultraviolet-B radiation increases cold
hardiness in Rhododendron, Physiol. Plant., 1994, 92, 516-520.
Teklemariam T, Blake TJ, Phenylalanine ammonia-lyase-induced freezing tolerance in jack
pine (Pinus banksiana) seedlings treated with low, ambient levels of ultraviolet-B
radiation, Physiol. Plant., 2004, 122, 244-253.
L’Hirondell S, Binder WD, Temperature stress tolerance of conifer seedlings after
exposure to UV-B radiation, Photochem. Photobiol., 2005, 81, 1094-1100.
Hofmann RW, Campbell BD, Bloor SJ, Swinny EE, Markham KR, Ryan KG, Fountain
DW, Responses to UV-B radiation in Trifolium repens L – physiological links to plant
productivity and water availability, Plant Cell Environ., 2003, 26, 603-612.
Turtola S, Rousi M, Pusenius J, Yamaji K, Heiska S, Tirkkonen V, Meier B, JulkunenTiitto R, Clone-specific responses in leaf phenolics of willows exposed to enhanced UVB
radiation and drought stress, Glob. Change Biol., 2005, 11, 1655-1663.
The Environmental Effects Assessment Panel Report for 2006
87
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
88
Yang Y, Yao Y, Xu G, Li C, Growth and physiological responses to drought and elevated
ultraviolet-B in two contrasting populations of Hippophae rhamnoides, Physiol. Plant.,
2005, 124, 431-440.
Milchunas DG, King JY, Mosier AR, Moore JC, Morgan JA, Quirk MH, Slusser JR, UV
radiation effects on plant growth and forage quality in a shortgrass steppe ecosystem,
Photochem. Photobiol., 2004, 79, 404-410.
Chimphango SB, Musil CF, Dakora FD, Responses to ultraviolet-B radiation by purely
symbiotic and NO3-fed nodulated tree and shrub legumes indigenous to southern Africa,
Tree. Physiol., 2004, 24, 181-192.
Correia CM, Moutinho Pereira JM, Countinho JF, Björn LO, Torres-Pereira JMG,
Ultraviolet-B radiation and nitrogen affect the photosynthesis of maize: A Mediterranean
field study, Europ. J. Agronom., 2005, 22, 337-347.
Li Y, Yu D, Huang Y, Effects of UV-B, nutrient, and light availability on shoot length and
phenolic content of Myriophyllum spicatum (L), J. Freshw. Ecol., 2005, 20, 59-63.
Keski-Saari S, Pusenius J, Julkunen-Tiitto R, Phenolic compounds in seedlings of Betula
pubescens and B pendula are affected by enhanced UVB radiation and different nitrogen
regimens during early ontogeny, Glob. Change Biol., 2005, 11, 1180-1194.
Pinto M, Edwards GE, Riquelme AA, Ku M, S.B., Enhancement of nodulation in bean
(Phaseolus vulgaris) by UV-B irradiation, Functional Plant Biology, 2002, 29, 1189-1196.
Rajendiran K, Ramanujam MP, Interactive effects of UV-B irradiation and triadimefon on
nodulation and nitrogen metabolism in Vigna radiata plants, Biologia Planta., 2006, 50,
709-712.
Chimphango SB, Musil CF, Dakora FD, Response of purely symbiotic and NO3-fed
nodulated plants of Lupinus luteus and Vicia atropurpurea to ultraviolet-B radiation, J.
Exp. Bot., 2003, 54, 1771-1784.
Keller M, Rogiers SY, Schultz HR, Nitrogen and ultraviolet radiation modify grapevines'
susceptibility to powdery mildew, Vitis, 2003, 42, 87-94.
Gonzalez R, Mepsted R, Wellburn AR, Paul ND, Non-photosynthetic mechanisms of
growth reduction in pea (Pisum sativum L) exposed to UV-B radiation, Plant. Cell.
Environ., 1998, 21, 23-32.
Nogués S, Allen D, Morison J, Baker N, Ultraviolet-B radiation effects on water relations,
leaf development, and photosynthesis in droughted pea, Plant. Physiol., 1998, 117, 173181.
Kolb CA, Käser MA, Kopecký J, Zotz G, Riederer M, Pfündel EE, Effects of natural
intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and
photosynthesis in grape leaves, Plant. Physiol., 2001, 127, 863-875.
Hopkins L, Bond MA, Tobin AK, Ultraviolet-B radiation reduces the rates of cell division
and elongation in the primary leaf of wheat (Triticum aestivum L cv Maris Huntsman),
Plant. Cell. Environ., 2002, 25, 617-624.
Foyer CH, Lelandais M, Kunert KJ, Photooxidative stress in plants, Physiol. Plant., 1994,
92, 696-717.
Apel K, Hirt H, Reactive oxygen species: Metabolism, oxidative stress, and signal
transduction, Annu. Rev. Plant Biol., 2004, 55, 373-399.
Foyer CH, Noctor G, Oxidant and antioxidant signalling in plants: A re-evaluation of the
concept of oxidative stress in a physiological context, Plant Cell Environ., 2005, 28, 10561071.
The Environmental Effects Assessment Panel Report for 2006
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
91
92
93
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F, Reactive oxygen gene network
of plants, Trends Plant Sci., 2004, 9, 490-498.
Noctor G, Metabolic signalling in defence and stress: The central roles of soluble redox
couples, Plant. Cell. Environ., 2006, 29, 409-425.
Kwak JM, Mori IC, Pei ZM, N. L, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones J, D,,
Schroeder JI, NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent
ABA signaling in Arabidopsis, EMBO Journal, 2003, 22, 2623-2633.
Pastori GM, Foyer CH, Common components, networks and pathways of cross-tolerance to
stress The central role of 'redox' and abscisic acid-mediated controls, Plant. Physiol., 2002,
129, 460-468.
Tamot BK, Pauls KP, Glick BR, Regulation of expression of the prb-1b / ACC deaminase
gene byUV-B in transgenic tomatoes, J. Plant Biochem. Biotech., 2003, 12, 25-29.
Wendehenne D, Durner J, Klessig DF, Nitric oxide: A new player in plant signalling and
defence responses, Cur. Opin. Plant Biol., 2004, 7, 449-455.
Barta C, Kalai T, Hedig K, Vass I, Hedig E, Differences in the ROS-generating efficacy of
various ultraviolet wavelengths in detached spinach leaves, Functional Plant Biology,
2004, 31, 23-28.
Hideg É, Rosenqvist E, Váradi G, Bornman JF, Vincze É, A comparison of UV-B induced
stress responses in three barley cultivars, Plant Funct. Biol., 2006, 33, 77-90.
John CF, Morris K, Jordan BRT, B., A.-H.-Mackerness S, Ultraviolet-B exposure leads to
upregulation of senescence associated genes in Arabidopsis thaliana, J. Exp. Bot., 2001,
52, 1367-1373.
Jansen MAK, Gaba V, Greenberg BM, Higher plants and UV-B radiation: Balancing
damage, repair and acclimation, Trends Plant Sci., 1998, 3, 131-135.
Navabpour S, Morris K, Allen R, Harrison E, A.-H.-Mackerness S, Buchanan-Wollaston
V, Expression of senescence-enhanced genes in response to oxidative stress, J. Exp. Bot.,
2003, 54, 2285-2292.
Zhang M, An L, Feng H, Chen T, Chen K, Liu Y, Tang H, Chang J, Wang X, The cascade
mechanisms of nitric oxide as a second messenger of ultraviolet B in inhibiting mesocotyl
elongations, Photochem. Photobiol., 2003, 77, 219-225.
Beligni MV, Lamattina L, Nitric oxide counteracts cytotoxic processes mediated by
reactive oxygen species in plant tissues, Planta, 1999, 208, 337-344.
Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL, Nitric oxide acts as an antioxidant
and delays programmed cell death in barley aleurone layers, Plant. Physiol., 2002, 129,
1642-1650.
Grün S, Lindermayr C, Sell S, Durner J, Nitric oxide and gene regulation in plants, J. Exp.
Bot., 2006, 57, 507-516.
Shi S, Wang G, Wang Y, Zhang L, Protective effect of nitric oxide against oxidative stress
under ultraviolet-B radiation, Nitric Oxide, 2005, 13, 1-9.
A.-H-Mackerness S, Surplus SL, Blake P, John CF, Buchanan-Wollaston V, Jordan BR,
Thomas B, Ultraviolet-B-induced stress and changes in gene expression in Arabidopsis
thaliana: Role of signalling pathways controlled by jasmonic acid, ethylene and reactive
oxygen species, Plant Cell Environ., 1999, 22, 1413-1423.
A.-H-Mackerness S, Plant responses to ultraviolet-B (UV-B: 280-320 nm) stress: What are
the key regulators?, Plant. Grow. Regul., 2000, 37, 27-39.
The Environmental Effects Assessment Panel Report for 2006
89
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
94
95
96
97
98
99
100
101
102
103
104
105
106
107
108
109
90
Britt AB, Molecular genetics of DNA repair in higher plants, Trends Plant Sci., 1999, 4,
20-25.
Jiang M, Zhang J, Water stress-induced abscisic acid accumulation triggers the increased
generation of reactive oxygen species and up-regulates the activities of antioxidant
enzymes in maize leaves, J. Exp. Bot., 2002, 53, 2401-2410.
Landry L, Stapleton A, Lim J, Hoffman P, Hays J, Walbot V, Last R, An Arabidopsis
photolyase mutant is hypersensitive to ultraviolet-B radiation, Proc. Nat. Acad. Sci. USA.,
1997, 94, 328-332.
Britt AB, Fiscus EL, Growth responses of Arabidopsis DNA repair mutants to solar
irradiation, Physiol. Plant., 2003, 118, 183-192.
Giordano CV, Galatro A, Puntarulo S, Ballare CL, The inhibitory effects of UV-B radiation
(280–315 nm) on Gunnera magellanica growth correlate with increased DNA damage but
not with oxidative damage to lipids, Plant Cell Environ., 2004, 27, 1415-1423.
Giordano CV, Mori T, Sala OE, Scopel AL, Caldwell MM, Ballaré CL, Functional
acclimation to solar UV-B radiation in Gunnera magellanica, a native plant species of
southernmost Patagonia, Plant. Cell. Environ., 2003, 26, 2027-2036.
Rousseaux MC, Ballaré CL, Giordano CV, Scopel AL, Zima AM, Szwarcberg-Bracchitta
M, Searles PS, Caldwell MM, Diaz SB, Ozone depletion and UVB radiation: Impact on
plant DNA damage in southern South America, Proc. Nat. Acad. Sci. USA., 1999, 96,
15310-15315.
Teranishi M, Iwamatsu Y, Hidema J, Kumagai T, Ultraviolet-B sensitivity in Japanese
lowland rice cultivars: Cyclobutane pyrimidine dimer photolyase activity and gene
mutation, Plant. Cell. Physiol., 2004, 45, 1848-1856.
Buffoni Hall RS, Paulsson M, Duncan K, Tobin AK, Widell S, Bornman JF, Water- and
temperature-dependence of DNA damage and repair in the fruticose lichen Cladonia
arbuscula ssp mitis exposed to UV-B radiation, Physiol. Plant., 2003, 118, 371-379.
Furness NH, Jolliffe PA, Upadhyaya MK, Ultraviolet-B radiation and plant competition:
Experimental approaches and underlying mechanisms, Photochem. Photobiol., 2005, 81,
1026-1037.
Mazza CA, Boccalandro H, Giordano CV, Battista D, Scopel AL, Ballaré CL, Functional
significance and induction by solar radiation of UV-absorbing sunscreens in field-grown
soybean crops, Plant. Physiol., 2000, 122, 117-126.
Jordan BR, Molecular response of plant cells to UV-B stress, Functional Plant Biology,
2002, 29, 909-916.
Rousseaux MC, Flint SD, Searles PS, Caldwell MM, Plant responses to current solar
ultraviolet-B radiation and to supplemented solar ultraviolet-B radiation simulating ozone
depletion: An experimental comparison, Photochem. Photobiol., 2004, 80, 224-230.
Lafontaine M, Schultz HR, Lopes C, Bálo B, Varadi G, Leaf and fruit responses of
´Riesling´ grapevines to UV-radiation in the field, ISHS Acta Horticulturae, 2005, 689,
125-132.
Mazza CA, Battista D, Zima AM, Szwarcberg-Bracchitta M, Giordano C, Acevedo A,
Scopel AL, Ballare CL, The effects of solar UV-B radiation on the growth and yield of
barley are accompanied by increased DNA damage and antioxidant responses, Plant. Cell.
Environ., 1999, 22, 61-70.
Markham KR, Ryan KG, Bloor SJ, Mitchell KA, An increase in luteolin : Apigenin ratio in
Marchantia polymorpha on UV-B enhancement, Phytochem., 1998, 48, 791-794.
The Environmental Effects Assessment Panel Report for 2006
Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with climate change
110 Olsson LC, Veit M, Weissenböck G, Bornman JF, Differential flavonoid response to
enhanced UV-B radiation in Brassica napus, Phytochem., 1998, 49, 1021-1028.
111 Ryan K, Markham K, Bloor S, Bradley J, Mitchell K, Jordan B, UVB-radiation induced
increase in quercetin: Kaempferol ratio in wild-type and transgeneic lines of petunia,
Photochem. Photobiol., 1998, 68, 323-330.
112 Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G, On the role of flavonoids
in the integrated mechanisms of response of Ligustrum vulgare and Phillyrea latifolia to
high solar radiation, New. Phytol., 2005, 167, 457-470.
113 Tattini M, Guidi L, Morassi-Bonzi L, Pinelli P, Remorini D, Degl'Innocenti E, Giordano C,
Massai R, Agati G, Differential accumulation of flavonoids and hydroxycinnamates in
leaves of Ligustrum vulgare under excess light and drought stress, New. Phytol., 2004, 163,
547-561.
114 Jordan BR, The effects of ultraviolet-B radiation on plants: A molecular perspective, Adv.
Bot. Res., 1996, 22, 97-162.
115 Stratmann J, Ultraviolet-B radiation co-opts defense signaling pathways, Trends Plant Sci.,
2003, 8, 526-533.
116 Brosché M, Strid A, Molecular events following perception of ultraviolet-B radiation by
plants, Physiol. Plant., 2003, 117, 1-10.
117 Kucera B, Leubner-Metzger G, Wellmann E, Distinct ultraviolet-signaling pathways in
bean leaves DNA damage is associated with ß-1,3-glucanase gene induction, but not with
flavonoid formation, Plant. Physiol., 2003, 133, 1445-1452.
118 Stratmann JW, Stelmach BA, Weiler EW, Ryan CA, UVB/UVA radiation activates a 48
kDa myelin basic protein kinase and potentiates wound signaling in tomato leaves,
Photochem. Photobiol., 2000, 71, 116-123.
119 Brown BA, Cloix C, Jiang GH, Kaiserli E, Herzyk P, Kliebenstein DJ, Jenkins GI, A UVB-specific signaling component orchestrates plant UV protection, Proc. Nat. Acad. Sci.
USA., 2005, 102, 18225-18230.
120 Sävenstrand H, Brosché M, Strid Å, Regulation of gene expression by low levels of
ultraviolet-B radiation in Pisum sativum: Isolation of novel genes by suppression
subtractive hybridisation, Plant. Cell. Physiol., 2002, 43, 402-410.
121 Brosché M, Schuler MA, Kalbina I, Connor L, Strid A, Gene regulation by low level UV-B
radiation: Identification by DNA array analysis, Photochem. Photobiol. Sci., 2002, 1, 656664.
122 Ulm R, Baumann A, Oravecz A, Mate Z, Adam E, Oakeley EJ, Schaefer E, Nagy F,
Genome-wide analysis of gene expression reveals function of the bZIP transcription factor
HY5 in the UV-B response of Arabidopsis, Proc. Nat. Acad. Sci. USA., 2004, 101, 13971402.
123 Izaguirre MM, Scopel AL, Baldwin IT, Ballare CL, Convergent responses to stress. Solar
ultraviolet-B radiation and Manduca sexta herbivory elicit overlapping transcriptional
responses in field-grown plants of Nicotiana longiflora, Plant. Physiol., 2003, 132, 17551767.
124 Casati P, Walbot V, Gene expression profiling in response to ultraviolet radiation in maize
genotypes with varying flavonoid content, Plant. Physiol., 2003, 132, 1739-1754.
125 Casati P, Walbot V, Rapid transcriptome responses of maize (Zea mays) to UV-B in
irradiated and shielded tissues, Genome Biol., 2004, 5, R16.
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126 Casati P, Stapleton AE, Blum JE, Walbot V, Genome-wide analysis of high-altitude maize
and gene knockdown stocks implicates chromatin remodeling proteins in response to UVB, Plant J., 2006, 46, 613-627.
127 Ensminger PA, Control of development in plants and fungi by far-UV radiation, Physiol.
Plant., 1993, 88, 501-508.
128 Boccalandro H, Mazza CA, Mazella A, Casel JJ, Ballare CL, Ultraviolet-B radiation
enhances a phytochrome-B-mediated photomorphogenetic response in Arabidopsis, Plant.
Physiol., 2001, 125, 780-788.
129 Kalbin G, Hidema J, Brosché M, Kumagai T, Bornman JF, Strid Å, UV-B-induced DNA
damage and expression of defence genes under UV-B stress: Tissue-specific molecular
marker analysis in leaves, Plant Cell Environ., 2001, 24, 983-990.
130 Ulm R, Nagy F, Signalling and gene regulation in response to ultraviolet light, Cur. Opin.
Plant Biol., 2005, 8, 477-482.
131 Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW, Convergence of
signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B
radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum
suspension-cultured cells, Plant. Physiol., 2003, 132, 1728-1738.
132 Izaguirre MM, Mazza CA, Svatos A, Baldwin IT, Ballare CL, Solar ultraviolet-B radiation
and insect herbivory trigger partially overlapping responses in Nicotiana longiflora and
Nicotiana longiflora, Ann. Bot., 2006, in press.
133 Ballaré CL, Stress under the sun. Spotlight on ultraviolet-B responses, Plant. Physiol.,
2003, 132, 1725-1727.
134 Roberts MR, Paul ND, Seduced by the dark side: Integrating molecular and ecological
perspectives on the influence of light on plant defence against pests and pathogens, New.
Phytol., 2006, 170, 677-699.
135 Tegelberg R, Julkunen-Tiitto R, Aphalo P, Red:far-red light ratio and UV-B radiation:
Their effects on leaf phenolics and growth of silver birch seedlings, Plant. Cell. Environ.,
2004, 27, 1005-1013.
136 Izaguirre MM, Mazza CA, Biondini M, Baldwin IT, Ballare CL, Remote detection of
future competitors: Impacts on plant defenses, Proc. Nat. Acad. Sci. USA., 2006, 103,
7170-7174.
137 Caputo C, Rutitzky M, Ballaré CL, Solar UV-B radiation alters the attractiveness of
Arabidopsis plants to diamondback moths (Plutella xylostella L) Impacts on oviposition
and involvement of the jasmonic acid pathway, Oecologia, 2006, 149, 81-90.
138 Raviv M, Antignus Y, UV radiation effects on pathogens and insect pests of greenhousegrown crops, Photochem. Photobiol., 2004, 79, 219-229.
139 Bassman JH, Ecosystem consequences of enhanced solar ultraviolet radiation: Secondary
plant metabolites as mediators of multiple trophic interactions in terrestrial plant
communities, Photochem. Photobiol., 2004, 79, 382-398.
140 Logemann E, Hahlbrock K, Crosstalk among stress responses in plants: Pathogen defense
overrides UV protection through an inversely regulated ACE/ACE type of light-responsive
gene promoter unit, Proc. Nat. Acad. Sci. USA., 2002, 99, 2428-2432.
141 Glombitza S, Dubuis P-H, Thulke O, Welzl G, Bovet L, Götz M, Affenzeller M, Geist B,
Hehn A, Asnaghi C, Ernst D, Seidlitz HK, Gundlach H, Mayer KF, Martinoia E, WerckReichhart D, Mauch F, Schäffner AR, Crosstalk and differential response to abiotic and
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142
143
144
145
146
147
148
149
150
151
152
153
154
155
156
157
158
biotic stressors reflected at the transcriptional level of effector genes from secondary
metabolism, Plant Mol. Biol., 2004, 54, 817-835.
Chappell J, Hahlbrock K, Transcription of plant defence genes in response to UV light or
fungal elicitor, Nature, 1984, 311, 76-78.
Surplus S, Jordan B, Murphy A, Carr J, Thomas B, Mackerness S, Ultraviolet-B-induced
responses in Arabidopsis thaliana: Role of salicylic acid and reactive oxygen species in the
regulation of transcripts encoding photosynthetic and acidic pathogenesis-related proteins,
Plant Cell Environ., 1998, 21, 685-694.
Linthorst HJM, Pathogenesis-related proteins of plants, Crit. Rev. Plant Sci., 1991, 10, 123150.
Leubner-Metzger G, Functions and regulation of beta-1,3-glucanases during seed
germination, dormancy release and after-ripening, Seed Sci. Res., 2003, 13, 17-34.
Flint SD, Caldwell MM, A biological spectral weighting function for ozone depletion
research with higher plants, Physiol. Plant., 2003, 117, 145-153.
Flint SD, Caldwell MM, Field testing of UV biological spectral weighting functions for
higher plants, Physiol. Plant., 2003, 117, 137-144.
Ibdah M, Krins A, Seidlitz HK, Heller W, Strack D, Vogt T, Spectral dependence of
flavonol and betacyanin accumulation in Mesembryanthemum crystallinum under enhanced
ultraviolet radiation, Plant. Cell. Environ., 2002, 25, 1145-1154.
Solhaug KA, Gauslaa Y, Nybakken L, Bilger W, UV-induction of sun-screening pigments
in lichens, New. Phytol., 2003, 158, 91-100.
Yao Y, Yang Y, Ren J, Li C, UV-spectra dependence of seedling injury and photosynthetic
pigment change in Cucumis sativus and Glycine max, Environ. Exp. Bot., 2006, 57, 160167.
Caldwell MM, Flint SD, Use and evaluation of biological spectral UV weighting functions
for the ozone reduction issue, in Environmental UV radiation: Impact on ecosystems and
human health and predictive models. eds.: Ghetti F, Checcucci G, Bornman JF, SpringerVerlag, Dordrecht, The Netherlands, 2006, pp. 71-84.
Coleman RS, Day TA, Response of cotton and sorghum to several levels of subambient
solar UV-B radiation: A test of the saturation hypothesis, Physiol. Plant., 2004, 122, 362372.
Quaite FE, Sutherland BM, Sutherland JC, Action spectrum for DNA damage in alfalfa
lowers predicted impact of ozone depletion, Nature, 1992, 358, 576-578.
Caldwell MM, Solar ultraviolet radiation and the growth and development of higher plants,
in Photophysiology, Vol. 6 ed.: Giese AC, Academic Press, New York, 1971, pp. 131-177.
Flint SD, Searles PS, Caldwell MM, Field testing of biological spectral weighting functions
for induction of UV-absorbing compounds in higher plants, Photochem. Photobiol., 2004,
79, 399-403.
McKenzie R, Smale D, Kotkamp M, Relationship between UVB and erythemally weighted
radiation, Photochem. Photobiol. Sci., 2004, 3, 252-256.
Flint SD, Ryel RJ, Caldwell MM, Ecosystem UV-B experiments in terrestrial communities:
A review of recent findings and methodologies, Agric. Forest Meteorol., 2003, 120, 177189.
Micheletti MI, Piacentini RD, Madronich S, Sensitivity of biologically active UV radiation
to stratospheric ozone changes: Effects of action spectrum shape and wavelength range,
Photochem. Photobiol., 2003, 78, 456-461.
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159 Sutherland JC, Biological effects of polychromatic light, Photochem. Photobiol., 2002, 7,
164-170.
160 Neitzke M, Therburg A, Seasonal changes in UV-B absorption in beech leaves (Fagus
sylvatica L) along an elevation gradient, Forstwissenschaftliches Centralblatt, 2003, 122,
1-21.
161 Cullen J, Neale P, Biological weighting functions for describing the effects of ultraviolet
radiation on aquatic systems, in The effects of ozone depletion on aquatic ecosystems ed.:
Häder D, RG Landes Company, 1997, pp. 97-118.
162 Newsham KK, Geissler PA, Nicolson MJ, Peat HJ, Lewis-Smith RI, Sequential reduction
of UV-B radiation in the field alters the pigmentation of an Antarctic leafy liverwort,
Environ. Exp. Bot., 2005, 54, 22-32.
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Chapter 4. Effects of solar UV radiation on aquatic ecosystems and
interactions with climate change
D-P. Hädera, H. D. Kumarb, R. C. Smithc and R. C. Worrestd
a
Institut für Botanik und Pharmazeutische Biologie, Friedrich-Alexander-Universität, Staudtstr.
5, D-91058 Erlangen, Germany
b
Mrigtrishna B32/605 Plot 214, Varanasi 221005, India
c
Institute for Computational Earth System Science (ICESS) and Department of Geography,
University of California, Santa Barbara, California 93106, USA
d
CIESIN, Columbia University, 12201 Sunrise Valley Drive (MS-302), Reston, VA, 20192-0002
USA
Summary
Recent results continue to show the general consensus that ozone-related increases in
UV-B radiation can negatively influence many aquatic species and aquatic ecosystems (e.g.,
lakes, rivers, marshes, oceans). Solar UV radiation penetrates to ecological significant depths in
aquatic systems and can affect both marine and freshwater systems from major biomass
producers (phytoplankton) to consumers (e.g., zooplankton, fish, etc.) higher in the food web.
Many factors influence the depth of penetration of radiation into natural waters including
dissolved organic compounds whose concentration and chemical composition are likely to be
influenced by future climate and UV radiation variability. There is also considerable evidence
that aquatic species utilize many mechanisms for photoprotection against excessive radiation.
Often, these protective mechanisms pose conflicting selection pressures on species making UV
radiation an additional stressor on the organism. It is at the ecosystem level where assessments
of anthropogenic climate change and UV-related effects are interrelated and where much recent
research as has been directed. Several studies suggest that the influence of UV-B at the
ecosystem level may be more pronounced on community and trophic level structure, and hence
on subsequent biogeochemical cycles, than on biomass levels per se.
Introduction
Aquatic ecosystems are key components of the Earth’s biosphere.1 They produce more than 50
% of the biomass on our planet (Figure 4-1) and incorporate at least the same amount of
atmospheric carbon dioxide as terrestrial ecosystems (cf. Chapter 5). The primary producers in
freshwater and marine ecosystems constitute the basis of the intricate food webs, providing
energy for the primary and secondary consumers and are thus important contributors for the
production of the human staple diet in the form of crustaceans, fish, and mammals derived from
the sea. Solar UV can negatively affect aquatic organisms.2-4 The massive loss of stratospheric
ozone over Antarctica over the past two decades as well as ozone depletion over the Arctic and
high to mid latitudes have aroused concern about the effects of increased solar UV-B radiation
on marine and freshwater ecosystems.5 Clear lakes and oceans in alpine and polar regions,
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
where UV penetrates deep into the water column, may be particularly vulnerable. The biological
organisms in polar waters are even more at risk because of the limited repair capabilities under
the inhibitory effects of low temperatures.6
Figure 4-1. This false-color map represents the Earth’s carbon “metabolism”— the rate at which plants absorbed
carbon out of the atmosphere during the years 2001 and 2002. The map shows the global, annual average of the net
productivity of vegetation on on land and in the ocean. The yellow and red areas show the highest rates, ranging
from 2 to 3 kilograms of carbon taken in per square kilometer per year. The green areas are intermediate rates,
while blue and purple shades show progressively lower productivity. In any given year, tropical rainforests are
generally the most productive places on Earth. Still, the ongoing productivity near the sea’s surface, over such a
widespread area of the globe, makes the ocean more productive than the land. (Image courtesy of NASA, 2003).
Solar UV Radiation and Penetration in Aquatic Ecosystems
A growing number of stations and networks have shown that there has been an increase in solar
UV-B radiation at the surface of and within aquatic systems7-10 which corresponds with
stratospheric ozone depletion.11 Comparative measurements indicate continued increases in
solar UV-B, which are masked by much larger seasonal changes and geographic differences (cf.
Chapter 1).12 Instrument accuracy has been improved in recent years and measurement
deviations have been quantified.13 In addition, biological and chemical actinometers have been
developed to determine UV-B doses on site during experiments and exposure.14-17
Aquatic environments vary tremendously in their UV attenuation. Coastal areas and shallow
continental shelf waters have a lower transparency than open ocean waters due to the runoff of
silt and dissolved organic carbon (DOC) from shores. In open oceans the optical properties are
largely determined by plankton and their degradation products,18-20 with zooplankton being an
additional source of DOC.21 Owing to the high input of inorganic and decaying organic material,
freshwater ecosystems usually have a high UV absorption which also depends on their level of
eutrophication.22
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
Ozone and aerosols provide the primary filter in the atmosphere that reduces damaging UV
radiation before it reaches the Earth’s surface. While stratospheric ozone depletion has now
stabilized and is beginning to return to pre-Montreal Protocol levels (see Chapter 1), the UV
transparency of inland aquatic ecosystems remains highly variable and subject to increased UV
exposure due to climate change.23 Climate change alters the DOC concentration and hence the
UV transparency of inland waters. Warmer, drier climates in particular will reduce the
inundation and water saturation of soils within watersheds and hence reduce the inputs of DOC
to adjacent lakes and streams.23 In some cases a combination of acidification and climate change
has led to dramatic increases in underwater UV penetration23 (see Chapter 5). The impact of
climate change may be particularly pronounced in freshwater ecosystems with low DOC
concentrations due to the exponential increase in UV penetration at DOC concentrations below
2 mg L-1 (Figure 4-2). Such variable levels of DOC and hence UV exposure may be important
factors in determining the distribution and abundance of planktonic and shallow benthic
organisms as well as influence the spawning depth of vertebrates such as amphibians and fish
that lay their eggs in shallow surface waters.
Depth of 1% UV-B (m) .
Climate warming has been found to
DOC (mg/l)
increase eutrophication in boreal
0
5
10
15
lakes.24 In addition, the export of
0
DOC from boreal peatlands
increases with temperature. Since
2
these areas cover about 15 % of the
4
boreal and subarctic regions and
6
climate warming is forecast to be
8
most severe at high latitudes, the
increasing temperatures are
10
expected to have significant effects
12
in boreal areas.25 Phytoplankton
14
abundance may vary by orders of
16
magnitude driven by future climate26
DOM-UV radiation interactions.
Figure 4-2. Relationship between the depth to which 1% of surface
Other aquatic ecosystems also show 320-nm UV radiation penetrates and concentration of dissolved
organic carbon (DOC) in temperature lakes. Note that at low DOC
that CDOM (colored dissolved
concentrations (1 -2 mg L-1) very small changes in the amount of
organic material) is a mediator of
DOC can cause large changes in the depth to which UV penetrates.
climate-UV interactions.26 Global
Modified from.23
warming has not only the potential
to affect lake species compositions,27 but also to increase the invasion potential by imported
species.28
Besides inorganic particulate matter, dissolved and particulate organic carbon (DOC and POC)
are the main attenuating substances in freshwater and coastal marine waters.29 DOC
concentrations often show large spatial and temporal variability.30 Recent models analyzing the
absorption of the components show that DOC mainly attenuates UV-B radiation while POC
mainly decreases the UV-A radiation in the water column.31 The optical effects of zooplankton
and phytoplankton on UV attenuation in freshwater ecosystems are usually low,32 but
bacterioplankton plays a major role (cf. Chapter 5). While DOC is only slowly degraded in the
water column, it is readily fragmented by solar UV to smaller subunits,33 which are consumed by
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
bacterioplankton.34 This increases the UV transparency of the water column35 where the
resulting deeper UV-B penetration affects bacteria and other organisms.36 In addition,
photobleaching increases UV transparency. Increasing temperatures associated with global
climate change are generally expected to decrease DOM concentrations and thus increase the
penetration of UV-B radiation into the water.37
DOC is a source of dissolved CO2 in the water,38, 39 and pCO2 is closely related to the DOC
concentration in Swedish boreal lakes.40 Acidification also decreases DOC concentrations.41, 42
Depending on its concentration, DOC can have positive or negative effects on phytoplankton
growth. Low concentrations contribute to nutrient recycling (N and P)43 and availability, while
higher concentrations negatively affect phytoplankton growth by shading.44 Bacteria are the
main agents for the mineralization of N and P from DOC. In addition to biomineralization,
phototransformation alters biodegradation to a variable degree, depending on the source of
DOC.45
Arctic and Antarctic marine and freshwater ecosystems are additionally affected by snow and ice
cover. Even thin layers of snow or ice significantly decrease the penetration of solar UV.46
Earlier ice melting due to increased temperature will expose phytoplankton blooms to higher
solar UV radiation. The seasonal change in sea-ice cover is a major determinant of the Antarctic
aquatic ecosystem. In addition, glacial meltwater plumes play a critical role near the ice edge
and their influence extends more than 100 km into the open ocean and influences the biota by
water column stratification, changes in turbidity, salinity and temperature.47 Global warming at
higher latitudes may lead to shallower mixed-layer depth, more intense seasonal stratification
with shallower mixed layers and subsequent influence on UV impact on aquatic ecosystems.
Plankton
Plankton can be subdivided, based on physiological or taxonomic criteria into major groups of
bacterioplankton, phytoplankton (including cyanobacteria and eukaryotes) and zooplankton.48 In
aquatic ecology, size (on a logarithmic scale) is used as a subdivision criterion: femtoplankton
(0.02 – 0.2 µm), picoplankton (0.2 – 2 µm), nanoplankton (2 – 20 µm), microplankton (20 – 200
µm) and macroplankton (200 – 2000 µm). Even though the smallest organisms contribute a
significant share to aquatic biomass productivity, these taxa have not yet been studied
extensively in terms of UV sensitivity.
Bacterioplankton and Viruses
Although the bacteria are small in size, they contribute a significant biomass component in
aquatic ecosystems and play a key role in biogeochemical processes.49 Predation is the major
mortality factor for planktonic bacteria.50 Most bacterioplankton do not produce screening
pigments but overcome solar radiation stress by fast cell division and effective repair
mechanisms.51 As long as the repair keeps up with the damage, the population is not threatened;
but when CPDs (cyclobutane pyrimidine dimers) accumulate under high solar radiation, the
population decreases. CPDs constitute by far the most frequent DNA damage induced by UV-B,
followed by single- and double-strand breaks.52, 53
DNA damage correlates strongly with the penetration of UV radiation into the water column, and
UV-B has a stronger effect than UV-A. When bacterioplankton was exposed in UV-transparent
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bags in tropical coastal waters, DNA damage was detectable down to 5 m. However, inhibition
of leucine and thymidine incorporation, as markers for protein and DNA synthesis, respectively,
occurred to a depth of 10 m.54 Photorepair by the enzyme photolyase, using UV-A/blue light as
an energy source,55 is a major mechanism to reduce the CPD load.4 Alternatively CPDs can be
repaired by nucleotide excision repair.56 Because of the path length of penetration, size seems to
be a decisive factor for UV sensitivity: bacterioplankton from several boreal lakes in Canada
were more sensitive to solar UV than the larger phytoplankton.57
Phytoplankton density significantly influences the depth distribution of bacterioplankton in the
water column. During the summer, dense diatom phytoplankton populations develop in the
Antarctic waters off the British Rothera Station, causing strong UV attenuation in the top
layers.58 At the surface, bacterioplankton incurred large UV-B-induced DNA damage
(exceeding 100 CPDs per megabase pairs, Mbp), but it was protected from solar UV-B below the
diatom population. This phenomenon was particularly prominent during January and February,
when sea ice melting cause pronounced stabilization of the water column. Later in the season,
this effect weakened and DNA damage was homogeneously distributed throughout the top 10 m
in well-mixed waters.
Solar UV has a decisive role in bacterioplankton community structure in marine surface waters.59
Large differences in sensitivity were found between different samples from the northern Adriatic
Sea. When exposed to UV-B radiation, inhibition of amino acid incorporation varied
substantially and there were even larger differences in the efficiency of recovery between
species. In Antarctic marine bacteria UV-B and UV-A had similar negative effects on survival.60
In contrast, in a high mountain lake (Spain) UV-A exerted the main effect.61 In the upwelling
zones of the Humboldt Current System, PAR induced a significant inhibition of bacterial
productivity followed by UV-A and UV-B.62
Both in the Arctic and Antarctic, spores of Bacillus subtilis were inactivated by solar radiation
within hours. However, a covering of ca. 500 µm of soil or dust or a retreat of ~1 mm into
endolithic habitats prevented inactivation of the spores.63 Snow covers of 5 – 15 cm thickness
attenuated UV penetration by a factor of 10 and protected the spores from inactivation. Crust
formation and biofilms are additional protective measures against environmental factors
including desiccation, temperature changes and solar UV.64 Halobacteria, being Archaea, show
a much higher resistance to solar UV radiation than bacteria and even tolerate UV-C radiation,65
reflecting the tolerance of shorter wavelengths penetrating through the atmosphere during early
evolution of these organisms. At present UV-C does not reach the Earth surface - except high
mountain locations - due to complete absorption in the atmosphere.
Another decisive factor for bacterial communities is the concentration of viruses.66 Virus-tobacteria ratios were found to be lowest in freshwater lakes and highest in saline lakes. The viral
abundance was closely correlated with the concentration of DOC. Viruses have neither effective
sunscreens nor photorepair capabilities67 and are prone to solar UV damage.68 This is supported
by their seasonal abundance in central European lakes.69 However, while being sensitive to solar
UV, it is surprising that the presence of viruses can provide some protection from solar UV to
their phytoplankton hosts such as Phaeocystis; the reason for this unexpected phenomenon is not
known.70 Anthropogenic pollutants such as cosmetic sun screens increase the abundance of viral
particles in the water.71
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
Picoplankton
Unicellular picophytoplankton such as Synechococcus and Prochlorococcus are recognized as
ubiquitous organisms of oceanic microbial loops and as the most abundant marine primary
producers.72 The effects of ambient levels of solar radiation on oceanic picoplankton were
studied in the water column73 using the range from unattenuated radiation to 23 % of the surface
level. The radiation significantly increased cell death in Prochlorococcus, while the
cyanobacterium Synechococcus had ten times the survival rate. Removal of UV radiation
strongly reduced the cell death rate in the first species and eliminated it completely in
Synechococcus. Natural solar radiation decreased the half-life times of the cells to a little over a
day. A similar differential sensitivity of the two groups was found for Mediterranean ecotypes.74
This generally high sensitivity of picoplankton to ambient solar radiation may act as a primary
driver of species composition and population structure and govern the dynamics of the microbial
food web in clear oceanic waters.73
Natural levels of solar UV-B have been determined in the Red Sea using a DNA biodosimeter.75
In parallel, depth profiles of DNA damage were analyzed in plankton samples that had been
collected from the water column down to 50 m. While the dosimeter did not show any response
below 15 m, CPD DNA damage could be found in all plankton samples. CPD concentrations
increased during the day and decreased over night, indicating DNA repair, but the dark repair
processes did not remove all CPDs during the night. Exposure to UV-B increases the membrane
permeability as shown in Nannochloropsis, which decreases the nitrogen uptake capability.76
Cyanobacteria
During the early Precambrian era, fluxes of solar UV-B and UV-C at the surface of the Earth
were several-fold higher than today due to the lack of oxygen in the atmosphere and the
consequent absence of ozone in the stratosphere (cf. Chapter 1). Early evolution was therefore
limited to UV-protected aquatic habitats. Nonetheless, there was a strong selection for
protective and mitigating strategies of early organisms against solar UV radiation.77, 78 The early
UV screens in aqueous environments may have been simple aromatic organic molecules, which
later developed into specialized UV absorbers still found in cyanobacteria as well as in some
eukaryotic photosynthetic organisms.77
Cyanobacteria are major biomass producers both in aquatic and terrestrial ecosystems and
represent more than 50 % of the biomass in many aquatic ecosystems.77 Because of their
nitrogen-fixing capacity they serve as important fertilizers both in the sea and in terrestrial plant
habitats such as tropical rice fields. Some cyanobacteria produce highly toxic substances,
including neurotoxins and peptide hepatotoxins, which cause animal poisoning in many parts of
the world79 and pose considerable risks for human health by polluting drinking water reservoirs
and recreational areas.80 In the Baltic Sea the filamentous Nodularia forms extended blooms in
late summer during calm weather.81 These organisms are tolerant of ambient solar UV-B levels
and outcompete more sensitive organisms even though solar UV-B has increased by 6 – 14 %
over the last 20 years in this area.82
Recent studies show that UV-B radiation treatment results in a wide range of responses at the
cellular level, including motility, protein biosynthesis, photosynthesis, nitrogen fixation and
survival in cyanobacteria.83, 84 The molecular targets include DNA and the photosynthetic
apparatus.85, 86 The phycobiliproteins, which serve as solar energy harvesting antennae, are
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specifically bleached by UV radiation.87, 88 However, several studies have demonstrated an
adaptation to UV stress and an increased resistance.89, 90 Long-term exclusion of solar UV
decreased the photosynthetic competence.91 Adaptive mutagenesis, which has been found in
cyanobacteria, increases their resistance to UV-B.92 Additional stress by exposure to heavy
metal ion pollutants adds to the UV-B effect.93, 94
Recent studies show that UV-B radiation treatment results in a wide range of responses at the
level of the cell. On the molecular level UV exposure causes a wide range of responses. It
induces an increased Ca2+ influx via L-type calcium channels.95 The stress signal is
subsequently amplified and transmitted using cyclic nucleotides as secondary messengers96
followed by the production of shock proteins. UV-B treatment increased the concentration of
493 proteins out of 1350 at least threefold in the terrestrial species, Nostoc commune.97 In
addition to direct UV-B-induced damage to the DNA, oxidative stress (singlet oxygen and
superoxide radicals) and damage were reported, causing lipid peroxidation and DNA strand
breakage.98 After prolonged UV-B exposures an adaptation to the reactive oxygen species
(ROS) stress has been observed.98 Typical ROS quenchers such as ascorbic acid, N-acetyl-Lcysteine or sodium pyruvate have protective effects.99, 100
Protective and mitigating strategies of cyanobacteria include mat or crust formation,101 vertical
migration of individuals within the mat, or shelf shading due to changes in morphology as
observed in Arthrospira platensis.102 In microbial mats the surface layer often serves as a
protector for the organisms underneath. A mat in a high Arctic lake showed high concentrations
of photosynthetic pigments in the lower part of the mat, while the black top layer was rich in
scytonemins and MAAs.103 By producing UV-absorbing substances including MAAs and/or
scytonemins, many cyanobacteria are able to withstand excessive solar UV radiation.104-106
MAAs are water-soluble compounds and have absorption maxima in the range from 310 to 360
nm.77 Upon absorption of UV radiation MAAs form triplet states which thermally relax and thus
render the radiation energy harmless.107 MAAs are either constitutive elements within the cells
or are induced by solar radiation.108 In many cases action spectroscopy has shown that solar
UV-B (which peaks around 300 nm) induces MAA synthesis in algae and phytoplankton, while
visible radiation has no effect.109 Biosynthesis of scytonemin is induced by exposure to UV-A
radiation and can be enhanced by elevated temperatures and photooxidative conditions.104
Scytonemins are exclusively synthesized by cyanobacteria and are chemically very stable. They
can accumulate in sediments; their abundance in sediment cores has been utilized to reconstruct
variations in the light regime over time.110 Natural populations of the same species may vary in
their concentration, indicating genetic differences.111
Phytoplankton
Phytoplankton are by far the major biomass producers in the oceans, and form the basis of the
aquatic food webs. Their productivity rivals that of all combined terrestrial ecosystems.
Another key ecological factor is that phytoplankton contribute significantly to the biological
pump: atmospheric carbon dioxide is taken up by primary producers in the sea and is cycled
through primary and secondary consumers. Most of this carbon dioxide returns to the
atmosphere, but part of this sinks to the ocean floor as zooplankton fecal pellets and, to a larger
extent, as dead phytoplankton.112 In effect the biological pump removes about 3 – 4 Gt of carbon
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per year from the atmosphere and partially offsets anthropogenic input of carbon from fossil fuel
burning and tropical deforestation.113
Phytoplankton are not evenly distributed in the oceans but dominate in the circumpolar regions
and the upwelling waters over the continental shelves, as seen by satellite imaging.114 Estimated
cell density differences are in reasonable agreement with measurements in the field.115 Marine
phytoplankton are dominated by small-sized cells of <2 µm diameter.116 A large number of
recent studies points to a considerable sensitivity of phytoplankton communities to solar UV,
ranging from polar to tropical habitats.117
Besides limitations in nutrients, light availability, pH and non-permissive temperatures, degree
of adaptation and grazing pressure, high levels of solar radiation inhibits photosynthesis in
species of different taxonomic groups.118-121 The UV component adds more to photoinhibition
than its energy share in solar radiation.122 This inhibition can be monitored in terms of oxygen
exchange,123 carbon acquisition124 or by measuring the quantum yield using pulse amplitude
modulated (PAM) fluorescence.125 Nutrient (mainly nitrogen and phosphorus) starvation often
augments the UV effects on photosynthetic performance,126 but may affect various species to a
different degree causing changes in community structure.127 This effect of nutrient deficiency
may be caused by less efficient repair processes.121 In addition, nutrient uptake, such as
phosphorus, may be impaired by solar UV radiation.128 Pollutants such as tributyltin, a
constituent of antifouling paints, have a synergistic negative effect.129, 130
Photorepair is limited at low temperatures. While at 6° C solar UV radiation significantly
inhibited growth in natural phytoplankton samples from a mountain lake in the U.S.A.; no such
inhibition was observed at 14°C, indicating that the repair processes compensate the UV
inhibition at the elevated temperature.131
Experimentally, ozone depletion has been mimicked by adding supplementary UV radiation
from lamps to ambient solar radiation. This approach was tested at three locations in Southern
Brazil, Canada and Patagonia.132, 133
Photoinhibition in terms of photosynthetic quantum yield is linked to the same mechanism as in
other eukaryotic photosynthetic organisms from algae to higher plants: the photosynthetic
electron transport chain is disrupted by photodegradation of the D1 protein in Photosystem II.134,
135
Low visible radiation enhances the repair efficiency while high PAR enhances the damage.136
Inhibition of protein synthesis results in retarded recovery. Nutrient starvation limits recovery
also.136 In contrast to photosynthesis, respiration is less affected by ambient levels of solar UV
radiation.137
Exposure of natural Antarctic marine plankton to UV at depths from 1 m to less than 20 m
showed that some phytoplankton species died, some flourished and others showed no effect.138
These and other results suggest that ozone-related enhanced UV-B may change food web
structure and function which in turn may affect biogeochemical cycles.139 In Canadian Rocky
Mountain lakes solar UV-A and UV-B were found to decrease algal density and alter community
composition.140 However, some studies indicated that after long-term exposure to solar UV,
phytoplankton can adapt to the radiation.141 UV-A had a higher impact than UV-B on hardbottom shallow marine communities, but the effects on diversity and biomass disappeared during
species succession within a few months.5, 142 Also, in Patagonian oceanic plankton assemblages,
UV-A had a stronger effect on photosynthesis during bloom periods than UV-B.143 However,
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the relative sensitivity of phytoplankton to UV-A and UV-B may depend on the species
composition and the nutrient state.144 Mixing is an important factor in plankton survival. In
contrast to marine habitats with high mixing, lakes often show stable thermal stratification.
Consequently, lake plankton communities show vertical distribution145 and populate certain
horizontal bands of optimal light conditions146 using buoyancy and active motility for niche
selection. In the subtropical lake Tanganyika, phytoplankton were affected by solar UV
radiation only in the top half-meter, reducing photosynthetic rates, damaging DNA (CPD
formation) and inducing UV-absorbing compounds, indicating that vertical mixing decreases
solar UV effects by transporting the cells to depth where active repair can take place. Fast
vertical mixing within the upper mixing layer of tropical marine environments can enhance
photosynthesis. Under cloudy conditions UV-A can be used as a source of energy, while under
slow mixing and cloudless skies UV-A is inhibitory.147 Other targets of UV-B damage are
changes in ultrastructure and pigment concentration and composition.148, 149 Besides direct
effects on cellular targets, UV-B also operates via the production of ROS.150 Phytoplankton
defend themselves by activating antioxidant systems. However, UV-B decreases the activity of
antioxidant enzymes and ROS scavengers.151
One mechanism of photoprotection against high solar radiation in many algal species (except red
algae) is the xanthophyll cycle, which relies on the thermal dissipation of excess excitation
energy thereby reducing the formation of singlet oxygen in the chloroplasts.152 Zeaxanthin
formation is also involved in increased non-photochemical quenching based on the migration of
electronic excitation energy from Photosystem II chlorophyll to nearby carotenoids. UV
exposure can enhance this process.153
MAAs are effective UV screens that protect phytoplankton from high solar UV radiation.154 In
the English channel MAAs are present on a year round basis with concentrations increasing
rapidly during spring often coinciding with the appearance of algal blooms.155 The action
spectrum for MAA synthesis induction shows a clear maximum in the UV-B range.156 In the
dinoflagellate Scrippsiella, daily vertical migrations have been found to be related to circadian
MAA biosynthesis.157, 158 In dinoflagellates, MAAs seem to be packaged in certain organelles
probably increasing the protective efficiency for specific cellular targets.159 MAAs can operate
both as UV absorbers and as quenchers for oxidative stressors.160, 161 While MAAs are very
stable molecules with respect to extreme temperatures, pH and UV radiation, they are easily
destroyed in water in the presence of photosensitizers.162
Some freshwater yeasts represent a small group of planktonic organisms showing both a
constitutive and a UV-inducible synthesis of photoprotective carotenoids and mycosporines.163165
The specific MAA is a compound linked to a glutaminol-glucoside,74 which is also
accumulated by copepods and ciliates from their diet.165 Some green algae in extreme UV
environments (snow algae) use sporopollenin as a UV-absorbing substance.166 Others rely on
massive accumulations of carotenoids such as astaxanthin167 or β-carotene,168 which provide
protection against oxidative stress by scavenging singlet oxygen or peroxyl radicals.159
Some phytoplankton taxa including dinoflagellates and diatoms produce toxic substances, such
as neurotoxins and domoic acid, and are a severe threat to animals and humans when they form
blooms. Recent blooms of the toxic Pseudo-nitzschia have caused mass mortality among
dolphins, sea lions and birds along the Californian coast.169 These blooms seem to be increasing
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in frequency and geographical range. The organisms have a low sensitivity to solar UV radiation
and escape damage of their photosynthetic apparatus by switching to heterotrophic growth.
Several taxa of marine phytoplankton such as Prymnesiophyceae and some dinoflagellates
produce dimethylsulfoniopropionate (DMSP) which is converted into dimethylsulfide (DMS)(cf.
Chapter 5). The latter is emitted into the atmosphere and forms cloud condensation nuclei,
thereby affecting local climate over the ocean.170 Cleavage of DMSP is induced by mechanical
or dark stress, by grazing or viral attack.171 This indicates that DMSP is involved in coping with
oxidative stress.172, 173 Because of the pronounced vertical migrations of the dinoflagellates,
diurnal patterns were recorded in DMS production in the St. Lawrence Estuary. Recently, lakes
and estuaries have also been found to be important sources of DMS.174 A model has been
developed to simulate the seasonal patterns of DMS production and validated against nutrient
concentrations, biological standing stock and other parameters.175 Marine biogenic iodocarbon
emissions are also significant for marine aerosol formation and have a key effect on global
radiative forcing.176 Besides changes in stratospheric ozone, cloud cover is a major factor
controlling the exposure of organisms to solar UV.177
The sea-ice ecosystems in the circumpolar oceans and water bodies of the Baltic and Caspian
Seas constitute some of the largest biomes on Earth.178 The semisolid ice matrix provides niches
in which bacteria, phytoplankton algae, protists and invertebrates thrive.179 Those organisms are
strongly affected by temperature, salinity, nutrients, visible and ultraviolet solar radiation.180
Sea-ice phytoplankton provide the fundamental energy and nutritional source for invertebrates
such as krill in their early developmental stages which amount to about a quarter of the biomass
production in ice-covered waters. The extreme conditions of their habitat force the organisms to
adapt physiologically. The production of large concentrations of MAAs is also essential for the
survival of primary consumers which ingest and incorporate the MAAs for their own protection.
The expected loss of about 25 % of the sea ice due to global warming over the current century
will certainly affect the productivity of the polar oceans.180
Anthropogenic acidification of boreal lakes decreases resistance of organisms to UV radiation
and affects species composition with increasing trophic level. Therefore it is assumed that loss
in species diversity will increase the susceptibility of acidified lakes to other stress factors.
Ecosystem stability in boreal lakes is thus likely to decline as global change proceeds.181
Experiments in large (volume >1 m3) outdoor enclosures, called mesocosms, are useful for the
study of complex impacts on food-web structure and dynamics.182-184 Mesocosms permit wellcontrolled experiments with natural phytoplankton communities in physical, chemical and light
conditions mimicking those of the natural environment. In addition, UV radiation within
mesocosms can be manipulated to simulate various levels of ozone depletion. Belzil and
coworkers182 find that while UV radiation increases can have subtle effects on bulk biomass
(carbon and chlorophyll), changes in community structure may be a more significant ecological
effect, because of differential sensitivity to UV radiation among planktonic organisms. These
workers note that “planktonic communities do not suffer from the catastrophic negative impacts
that might have been inferred from some laboratory experiments on individual components of
the marine food web”. They note, in agreement with previous observations, that ambient levels
of UV radiation already have significant effects. Mesocosm experiments, including both
plankton and their grazers, also suggest that changes in community structure are potentially more
important than effects on overall algal biomass.184 Other workers found that phytoplankton
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growth was inhibited by UV radiation in fixed-depth experiments but not in mesocosms where
vertical mixing exposed planktonic organisms to variable radiation regimes.185 A synthesis
model simulating mesocosm experiments suggests that enhanced UV-B could cause “a shift from
primary producers to bacteria at the community level”.186 Such a shift in community structure
could have important consequences for CO2 levels in oceanic surface waters. A mathematical
model based on a predator-prey scheme considers sedimentation of phytoplankton, vertical
mixing, and attenuation of PAR as well as UV radiation in the water column. Surprisingly,
higher inhibition by UV radiation and longer mixing periods can induce strong fluctuations in
the system and enhance plankton productivity due to the stronger effects on the predators.187, 188
Macroalgae and Aquatic Plants
Macroalgae are major biomass producers on rocky shores and continental shelves. The
macroalgae canopies form habitats for larval fish, crustaceans, and other animals. Macroalgae
are of commercial importance and are harvested on a large scale from natural vegetation and
aquaculture for human consumption and industrial use.
Even without ozone depletion, UV-B radiation constitutes a significant stressor for macroalgae.
Exposure to solar UV-B results in a host of biological effects on the molecular, cellular,
individual and community levels.189 Macroalgae are stressed by solar UV radiation to an extent
which is genetically determined and results in a pronounced vertical stratification.190 Even
closely related species of the same genus may have significantly different UV sensitivity,
causing them to grow in different habitats.191 UV-tolerant species populate the tidal zone, while
more sensitive species are found in deeper waters.192 Seasonal changes in UV and visible
radiation also result in a pronounced succession of species over the year in marine macrobenthic
communities.193 Besides changing salinity, temperature and desiccation in their habitats,194
macroalgae are exposed to extreme variations in light intensity due to daily, seasonal and tidal
cycles as well as changing turbidity in the water column.195 Intertidal macroalgae of all major
taxa can rapidly adapt to fast changes in radiation.196, 197 Environmental conditions can be
extreme in macroalgal habitats where, at polar growth sites, species have to survive in total
darkness during several winter months.198
Young specimens were more prone to UV inhibition of photosynthesis, and species collected
shortly after the winter were found to be affected more than those harvested later in the year,
indicating an adaptive strategy to increasing natural short-wavelength radiation.199 Both Arctic
and Antarctic species showed pronounced effects of solar UV-B on photosynthesis, morphology
and growth rates.200, 201 Unfiltered solar radiation proved lethal to several Antarctic deep water
algae. While tropical macroalgae are better adapted to higher solar UV and visible radiation than
higher-latitude species, they are also affected by ambient solar UV.202 Both UV-A and UV-B
decrease growth rate, quantum yield of photosynthesis and cause accumulation of DNA damage.
Since different species show different sensitivities, increases in solar UV-B radiation could
influence species recruitment in the upper intertidal zone.203
Excessive solar radiation causes photoinhibition of photosynthesis;204 elimination of total UV or
UV-B alone reduces the severity of photoinhibition and shortens recovery time in many
species.152, 205, 206 Electron microscopy revealed pronounced damage of the thylakoid
structure.207 Enzymes involved in the photosynthetic CO2 fixation and sugar formation are
affected by UV radiation and the concentration of chlorophyll a decreases.208, 209 The
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photosynthetic accessory phycobiliproteins operating as antenna pigments in red algae are even
more sensitive to solar UV radiation.210 UV-B is more effective than UV-A in decreasing
growth rate.203 In a laboratory study exposure to UV resulted in significant release of
organohalogens from several polar macroalgae. These substances have ozone-depleting
characteristics and so potentially enhance the incidence of solar UV.203
Most macroalgae have an efficient photorepair system of UV-induced CPDs.211 Besides DNA
repair mechanisms, efficient ROS scavenging enzymes were found in many macroalgae.212 In
several Arctic algae these enzymes vary significantly in activity over the growing season when
algae have been collected before, during and after break-up of sea ice.213 UV sensitivity
decreases with age and developmental stage of macroalgae. The germination capacity of
zoospores from five Laminariales species were found to decrease sharply after 16 h of exposure
to visible and UV radiation.214 Both zygotes and young germlings of brown algae show massive
inhibition; UV-B radiation is more effective than UV-A.215 Also juvenile stages of red and green
algae showed a pronounced UV sensitivity.216 Both UV-A and blue radiation reactivate spore
germination after UV-B inhibition, indicating photolyase activity.217 Motile gametes of brown
algae use light-directed movement (phototaxis) to accumulate at the water surface improving the
chances of finding a mating partner, but that phototactic response is drastically inhibited by solar
UV. Enhanced levels of solar UV-B may affect this vital strategy and thus impair development
of kelps.218
Many macroalgae of the tidal zone produce UV-absorbing compounds while subtidal species
usually do not have this protection. However, deep-water algae are rarely exposed to significant
levels of solar UV radiation.219 Red algae have the highest percentage of species that synthesize
MAAs,220 followed by brown and green algae. The protective effect of MAAs was shown in the
red alga Porphyra, commercially sold as Nori, where they block thymine dimer production. 221
MAAs are very stable against elevated temperatures and UV exposure.222 The presence of
ammonium increases the accumulation of MAAs. The blue component of visible radiation has
the highest effect in inducing MAA biosynthesis in Porphyra.223 Polychromatic action spectra
of induction reveal the efficiency of short wavelength radiation in several species.224, 225
Recently a new group of MAAs absorbing at 322 nm has been identified in green algae.226 The
common sea lettuce, Ulva, was found to produce a UV-B absorbing compound with a maximum
at 292 nm.227 In brown algae a novel group of UV absorbing pigments, phlorotannins, has been
found.228 Macroalgae can be classified according to their MAA production. Most deep water
algae never produce MAAs even when transplanted to surface waters. Algae from the intertidal
zone often show induction of MAAs, while species growing near the water surface normally
have a high concentration of MAAs, which cannot be further induced.229 Other defense
mechanisms against photooxidative stress involve the induction of a wide range of antioxidant
enzymes in brown, green and red algae230 as well as biosynthesis of several carotenoids.224
Aquatic mosses and liverworts show UV-B-related responses similar to those of many
macroalgae, including inhibition of photosynthesis, growth and pigmentation.231, 232 PAM
measurements show a pronounced photoinhibition during noon, from which the thalli recover
when the UV stress decreases.107 When exposed to high levels of solar UV-B radiation they
produce UV-absorbing compounds, which seem to be hydroxycinnamic acid derivatives.233
Aquatic flowering plants are also affected by solar UV. Sea grass meadows cover large areas of
sandy bottom in shallow water234 and contribute substantially to the aquatic biomass
productivity.235 Photosynthetic quantum yield dramatically decreases under unfiltered solar
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radiation. Removal of UV-B or total UV improves the photosynthetic activity.236 Transfer
experiments on plants growing at 15 m to 2.5 m water depth indicate an efficient adaptation of
sea grasses to higher solar UV. Epiphytes growing on sea grass leaves has been considered
detrimental since it reduces the photosynthetically available radiation, but as they strongly
absorb UV-B radiation they exert a beneficial effect.237 In a submersed aquatic angiosperm, UVB exposure over 7 – 16 days caused an increase in several photosynthetic enzymes. Water
transparency to visible and UV governs the distribution and abundance of submerged
macrophytes in lakes in the Canadian Arctic.238 Antioxidant enzymes were also activated by
UV.239 The common freshwater duckweed, Lemna, shows strong responses to simulated solar
radiation, with a pronounced increase in ROS responses. This UV-induced stress response was
augmented by exposure to copper, which alone also activates the ROS pathway.240 Related
species differ considerably in their UV-B sensitivity.241
Consumers
Consumers form the next
higher level in the aquatic
food webs after producers
(Figure 4-3). In most cases
several trophic levels follow
each other, usually starting
with zooplankton being the
primary consumers. It is
evident that a UV-related
decrease in primary producer
biomass has an effect on
growth and survival of the
consumers. In addition,
specific UV effects have been
identified in almost all
consumers.242
Figure 4-3. Schematic diagram of classic and microbial marine food webs
illustrating the flow of carbon and energy through the systems. Adapted
from DeLong and Karl, courtesy of the National Biological Information
Infrastructure (NBII).243
Zooplankton
Zooplankton includes
unicellular and multicellular
life forms and can be classified in several size classes. It is also comprised of larval forms of
fish, crustaceans, echinoderms, mollusks and other phyla. These forms will be discussed below.
Zooplankton community structure in freshwater ecosystems is controlled by multiple factors,
including DOC content and distribution throughout the water column, which regulates UV
penetration (see Chapter 1). UV radiation is a potential driving force for zooplankton
community structure in some lakes.244 In shallow ponds of Finnish Lapland Daphnia only
occurs when sufficient amounts of DOC are present.245 Depending on the terrestrial succession
in the watersheds of several Alaskan lakes, the UV attenuation depths (1% of surface irradiance
at 320 nm) vary from 0.6 m to more than 14 m. This UV regime strongly controls the species
composition of major macrozooplankton. When zooplankton from a UV-opaque lake was
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transplanted into the surface water (0.5 m depth) of a UV-transparent lake, it perished within
only a few days, suggesting a strong link between early succession of zooplankton communities
and terrestrial plant communities (a source of DOC) within the watershed. Large variations in
UV sensitivity were also found in a study involving lakes of different UV transparencies.246, 247
In response to high solar UV, Daphnia shows a pronounced avoidance response when observed
in UV transmitting acrylic columns suspended in the surface waters. In contrast, when UV-B
and short-wavelength UV-A are blocked, the animals prefer moving to the surface. In a low-UV
lake, no such preferential behavior was seen. These results and those from a follow-up, openlake experiment indicate that UV radiation may influence the vertical distribution and habitat
partitioning of certain zooplankton in high-UV lakes, while predation, food availability and other
factors may be more important in low-UV lakes.248 Studies of sublethal effects of UV on the
freshwater cladoceran Daphnia show increases in respiration rates at low levels of UV exposure
and decreases at high levels.249
In their natural habitat, zooplankton face conflicting selection pressures. While invertebrate
predators induce an upward movement during daylight hours, this exposes zooplankton to strong
surface UV exposure.250 Even though Daphnia and other zooplankton try to escape from surface
UV radiation by vertical migration, the organisms cannot avoid excessive exposure. The
copepod Boeckella, living in Lake Titicaca with very high solar UV levels, counters the
detrimental effect by incorporating photoprotective MAAs.251 Copepods cannot synthesize these
substances but acquire them from their algal diet (e.g., dinoflagellates).158
In a study of Antarctic copepods, MAA concentration was strongly correlated with UV
tolerance.252 In an alpine lake there was a strong seasonality in MAA concentrations in
phytoplankton and copepods with more than three times higher concentrations in the summer
than in the winter.253 Besides vertical migration and UV screening, copepods rely on photorepair
of UV-B-induced DNA damage254 as shown in species from Patagonia, Argentina.255
Photoenzymatic repair contributes significantly towards UV-B tolerance in many cladocerans.256
Some Antarctic copepods possess a less efficient photorepair mechanism, which has been
attributed to the low temperatures typical of Antarctic lakes.252 The implication is that at
elevated temperatures (due to global warming) the enzymatic photorepair of UV-induced
damage should be more efficient.257 This hypothesis was tested in living Daphnia by extracting
DNA at various temperatures. UV-induced DNA damage increased with temperature, but the
light-dependent enzymatic repair more than offset the effect and the net DNA damage
significantly decreased with increasing temperature.258 This result was supported by a study of
planktonic rotifers and crustaceans in Northern temperate lakes where UV had less detrimental
effects on abundance and reproduction at higher temperatures.259 However, one study found that
mortality and DNA damage were as high as at low temperatures in freshwater ciliates, indicating
that photolyase has an optimal temperature for its activity.260 It is interesting to note that though
elevated levels of solar UV induce mutations, there does not seem to be evolutionary selection
toward UV protection in halophilic crustaceans.261 Feeding experiments indicate that UV-B
pretreated phytoplankton species negatively affect the life history of Daphnia.262 Adults were
smaller, and a smaller number of juveniles with lower fitness were produced under these
conditions than in the controls, indicating that UV-B had a significant effect on food quality and
impaired energy transfer to the next trophic level.263, 264 The effect of climate warming on macrozooplankton is subtle: Copepod populations were reduced in size but those of ostracods
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increased.265 In contrast predation by fish has a major effect on population composition and
density.
Several workers have reported results consistent with the hypothesis that UV influences
zooplankton community structure and succession during early lake ontogeny. Engstrom and coworkers266 studied the chemical and biological trends during lake evolution in recently
deglaciated terrain near Glacier Bay, Alaska. They demonstrated that dissolved organic carbon
(DOC) concentrations increased with lake age. Williamson et al.,267 investigating changes in UV
attenuation and macrozooplankton community structure in these same lakes, showed a strong
dependence of UV radiation transparency on terrestrially derived DOC. They suggest a link
between the development of terrestrial plant communities within these lake watersheds, changes
in lake hydrology, and the early succession of zooplankton communities following deglaciation.
These results suggest that UV radiation may be a more important factor than previously
recognized in determining the distribution and abundance of zooplankton in lake ecosystems.
Corals and Sea Anemones
Recent accelerated catastrophic coral mortality has been linked with several environmental
factors including bacterial and cyanobacterial infections,268 increasing temperatures, 269-272
marine pollution273 and human destruction of coral reefs. Many corals rely on the photosynthetic
activity of dinoflagellates (zooxanthellae).274 At temperatures exceeding a thermal threshold,
corals are bleached. The underlying mechanism could be photoinhibition of photosynthesis in
the zooxanthellae induced by the production of reactive oxygen species.275, 276 However, recent
results indicate that corals and their symbionts may be capable of adapting to higher
temperatures.277 Like corals, giant clams harbor symbiotic zooxanthellae. Clams also suffered
mass bleaching on several reefs of the Great Barrier Reef.278 Virus-like particles could also be
associated with coral mortality.279
When symbiotic algae are exposed to solar radiation the host is also subjected to damaging solar
UV radiation. Some stony corals expand their tentacles upon exposure to photosynthetically
active radiation and contract them when encountering excessive radiation.280 As a countermeasure to enhanced solar UV the algae produce MAAs, some of which are also transferred to
the host.274 Moreover, the host develops antioxidant defenses to protect itself from the
photosynthetically produced oxygen. Herbicides also affect corals by impairing the
photosynthetic symbiotic zooxanthellae.281 Laboratory-kept colonies of the coral Stylophora
maintained minimal amounts of MAAs, but the concentration of the UV-absorbing pigments
increased rapidly upon exposure to broadband UV.282 Four MAAs, produced by the
zooxanthella Symbiodinium, increased first, followed by six additional ones which were
synthesized at the expense of the primary MAAs.
Sea anemones occur in several color phenotypes. At the coast of Discovery Bay, Jamaica, pink
morphs are more abundant in the lagoon and in deeper areas, while green individuals are found
in the forereef (seaward and downward from the reef crest) and in shallower areas. Genetic
analysis revealed two distinct variants with different UV absorbance and UV acclimatization
capacities.283 A comparison of sea anemones with dinoflagellates or green algae as symbionts or
asymbiotic species showed that the MAAs mainly reflect phylogenetic differences among the
anemones rather than the presence or kind of symbiont.284
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Sea Urchins
Exposure to UV radiation causes apoptosis (cell self-destruction) in developing sea urchin
embryos.285 Embryos of three sea urchin species from different habitats ranging from the Gulf of
Maine to the Antarctic indicated significant amounts of accumulated DNA damage in the form of
cyclobutane pyrimidine dimers (CPD). Biological weighting functions for DNA damage
indicated a high sensitivity for UV-A radiation, but the most sensitive species show an increased
susceptibility to UV-B correlated with the lowest concentration of UV-absorbing compounds.286
Larvae and embryos of these species dwell within 5 m of the ocean surface. UV-induced
damage in the different larval stages was clearly correlated with the absence of MAAs. The
absence of UV-screening substances strongly decreased survival.287 Further, the observed delays
in early cleavage and following development were closely related with UV-induced DNA
damage. Reproduction in the circumpolar sea urchin Sterechinus occurs during austral spring
when ozone concentrations during the past 25 years have declined by more than 50%. When the
planktonic embryos were exposed in the top 1 m of the water column, nearly all exhibited DNA
damage and 100% showed abnormal development.288 UV-B removal prevented DNA damage.
At depths below 3 m hardly any abnormal development or DNA damage occurred. The
threshold for DNA damage from ambient solar UV-B was ≤25 kJm-2 (inducing ~17 CPDs mb-1)
and levels >80 kJm-2 precluded normal development.
The Antarctic sea ice has been thought to protect the benthic invertebrate fauna from solar UV-B
radiation. However, recent investigations showed that short-wavelength UV-B (down to 304
nm) is transmitted through the austral spring annual ice of McMurdo Sound where it causes
DNA damage and mortality during the early development in sea urchin embryos.289 The degree
of damage and mortality varies from year to year and depends on the thickness of the sea ice and
on the total column ozone.
Amphibians
During the last decade amphibian populations have suffered widespread declines and even
extinctions on a global scale.290, 291 Many different factors, including habitat destruction292, 293
and fragmentation,294-297 global climate change,298, 299 acid precipitation,300, 301 environmental
pollution,302-305 including anthropogenic pesticides304, 306 and fertilizers,307 parasites,308
introduction of exotic competitors and predators,309-314 fungal diseases,315, 316 and other pathogen
outbreaks,317-319 interannual variability in precipitation, as well as climate change-induced
reductions in water depth at oviposition sites, have been suggested as responsible for those
global declines.320, 321 Since the 1990s, malformations have been noted in many parts of the
United States321 and in many other countries all over the globe.322, 323
Among other factors, solar UV-B radiation has been variously implicated as a possible
contributing factor324 involved in malformation and mortality, especially during the embryonic
development. However, there are two conflicting views on the involvement of UV-B in
amphibian declines.325, 326 In a controlled laboratory study, leopard frogs (Rana pipiens) were
exposed to unfiltered solar radiation or radiation without UV-B or total UV.327 Unlike natural
conditions, the larvae in the laboratory could not avoid exposure. Full sunlight caused ca. 50%
mortality in early larval development, while filtered solar radiation had no effect. There was a
clear correlation between solar UV doses and hindlimb malformation. In situ studies in the
natural amphibian habitat showed a considerable protection from solar UV radiation by DOC
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
and vegetation shading, especially during the sensitive development during spring.328 When
exposed to ambient solar radiation under controlled conditions and when natural shade and
refuge were eliminated, embryos and larvae of several anuran species died.329 A subsequent
quantification of the outdoor UV exposure in Northern Minnesota and Wisconsin wetlands
indicated that the risks for UV-induced malformations and mortality are low for both Northern
leopard and mink frogs. The exposure of amphibian eggs and larvae to solar UV radiation
strongly depends on the concentration of DOC in the water column.330 One important factor is
oviposition behavior: species which lay the eggs in UV-protected sites may be more sensitive to
solar UV exposure than those which deposit their eggs at the water surface.331 Amphibian
species with the highest physiological sensitivity to UV-B are those with the lowest field
exposures as a function of the location of embryos and the UV-B attenuations properties of water
at each site. These results also suggest that conclusions made about vulnerability of species to
UV-B in the absence of information on field exposures may often be misleading.331
Red-legged frog embryos (Rana aurora) appear to be tolerant to current ambient levels of UV-B,
but radiation even slightly exceeding the ambient levels is lethal.332 Although embryonic size is
a complicated issue and small size at hatching can change very quickly after feeding, even at
ambient levels, larvae exposed to UV-B as embryos tend to be smaller and less developed than
non-exposed organisms. Amphibians use behavioral, physiological and molecular defenses
against solar UV-B damage, but species-specific sensitivities may cause changes in community
structure due to persistent UV-B level increases,333 but because some species may be more
successful than others, changes in species composition can result.333
Fishes
Although humans use about 8% of the productivity of the oceans, that fraction increases to more
than 25% for upwelling areas and to 35% for temperate continental shelf systems. For about
one-sixth of the world’s population (primarily developing nations), the oceans provide at least
20% of their animal protein. Many of the fisheries that depend upon the oceanic primary
productivity are unsustainable. Although the primary causes for a decline in fish populations are
predation and poor food supply for larvae, overfishing, increased water temperature, pollution
and disease, and/or exposure to increased UV-B radiation may contribute to that decline. The
eggs and larvae of many fish are sensitive to UV-B exposure (Figure 4-4). However,
imprecisely defined habitat characteristics and the unknown effect of small increases in UV-B
exposure on the naturally high mortality rates of fish larvae are major barriers to a more accurate
assessment of effects of ozone depletion on marine fish populations.
Visual predators, including most fish, are necessarily exposed to damaging levels of solar UV
radiation. Skin and ocular components can be damaged by UV,334 but large differences are
found between different species.335 Coral reef fishes can adapt to the UV stress by incorporating
UV-absorbing substances, which they acquire through their diet, into their eyes and epidermal
slime.336 Exposure to solar radiation induced “suntanning” in red seabream. Histological,
colorimetric and chemical assays showed that the sun-exposed fish had an up to five times higher
concentration of melanin.337 In addition to direct effects, including damage to biological
molecules such as DNA and proteins and the generation of reactive oxygen species,
photoactivation of organic pollutants and photosensitization may be detrimental. The damaging
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111
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
effects on eggs and larval stages may be enhanced by polycyclic aromatic hydrocarbons (PAHs)
such as retene, which is a pollutant from pulp and paper mills.338
In goldfish, embryos are prone to UV effects during
early development339 and produce CPDs under UV
radiation. These are more efficiently repaired in the
presence of light.340 Solar UV radiation has been shown
to induce DNA damage in the eggs and larvae of the
Atlantic cod,294 where larvae were more sensitive than
eggs. Artificial UV causes massive apoptosis in larval
embryos of Japanese flounders.341 Studies addressing
biological weighting functions indicated a strong
sensitivity towards solar UV-B. CPD loads as low as 10
per megabase DNA resulted in approximately 10%
mortality. Use of video taping and measurement of
oxygen consumption showed sublethal effects of UV
radiation in juvenile rainbow trout342. Under worst-case
scenarios (60% ozone loss, sunny weather and low
water turbulence), solar UV-B eliminated buoyancy and
caused mortality within 1 or 2 days.
Fish spawning depth strongly correlates with UV
exposure. In-situ incubation experiments have shown
that in a highly UV transparent lake 100% of yellow
Figure 4-4. Fish eggs and larvae are
perch eggs (Perca flavescens) are killed before hatching specifically prone to UV-B radiation. Salmon
Alevin larva has grown around the remains of
when exposed to full solar UV.343 In this same lake
the yolk sac. In about 24 h it will be a fry
92% of eggs are spawned at depths greater than 3 m,
without yolk sac (courtesy Uwe Kils)
while in a nearby lake with low UV transparency 76%
of eggs were spawned at depths shallower than 1 m. It is not known whether the fish are able to
detect and avoid the high UV at shallower depths in the high UV lake or whether this spawning
pattern is due simply to differential survival. In either case, the deeper spawning depths place
the eggs in colder water where it takes them much longer to hatch compared to eggs spawned in
the warm surface waters. A similar phenomenon has been observed in bluegill larvae (Lepomis
macrochirus) in a UV-transparent lake where in 19 % of nests the estimated UV-induced
mortality of larvae exceeds 25 %. Most nests are exposed to relatively low UV levels because
they are either located at deeper depths or under overhanging branches.344 In fish aquaculture,
specific measures are introduced, such as installing UV sunscreens to avoid UV damage to larval
fish in the usually shallow habitats.345
Other Aquatic Animals
Early life stages of marine organisms, particularly eggs and larvae, are vulnerable to solar UV-B
radiation. Rocky shore mollusks show an increased mortality and retarded development upon
UV exposure. These detrimental effects are synergistically enhanced in the presence of other
stress factors such as high temperatures or salinity, pointing to strong underestimation of the
ecological impacts of climate change by not accounting for the complex interactions among such
environmental variables as temperature, salinity and oxygen availability.346 Desiccation
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
enhances mortality and negatively affects development in encapsulated embryos of rocky shore
gastropods.347
The amphipod Amphitoe valida has high concentrations of MAAs and consequently low
mortality while the isopod Idothea baltica has low MAA concentrations and shows high
mortality. However, the latter species deposits all available MAAs into the eggs and embryos
conferring protection to the progeny.348
Conclusions and Consequences
With the recognition of the importance of UV radiation effects on aquatic ecosystems, there has
been a plethora of publications show that solar UV can adversely affects aquatic organisms.
These studies document substantial impact on individual species yet considerable uncertainty
remains with respect to assessing effects on ecosystems. Several studies indicate that the impact
of increased UV radiation would be relatively low when considering overall biomass response
while often, in contrast, the response is quite marked when the abundance, distribution and
effects on individual species are considered. Ecosystem response to climate variability involves
both synergistic and antagonistic influences with respect to UV radiation-related effects on
aquatic ecosystems and these influences significantly complicate comprehension and prediction
at the ecosystem level. With respect to assessing UV radiation-related effects, the influence of
climate variability is often more important via indirect effects such as reduction in sea ice,
changes in water column bio-optical characteristics and shifts in oceanographic biogeochemical
provinces than through direct effects. Decreases in primary production would result in reduced
sink capacity for atmospheric carbon dioxide, with its related effects on climate change.
The global decline of amphibian populations seems to be related to several complex, interacting
causes. While one review clearly rejected any link between solar UV-B radiation and amphibian
decline326 evidence from more than 50 peer-reviewed publications from around the world shows
that dozens of amphibian species are affected by UV-B.325
A number of new studies have both confirmed and strengthened evidence that UV-B has an
important influence on community structure of various aquatic ecosystems. In lakes,
phytoplankton abundance may vary by orders of magnitude depending upon future climateDOM-UV interactions.26 Also, lakes often show thermal stratification and as a consequence
plankton communities show vertical distributions where the UV regime can strongly control
species composition.235 Other evidence supports the hypothesis that UV influences zooplankton
and community structure and succession during early lake ontogeny.267 Mesocosm studies,
including both phytoplankton and their grazers, suggest that species composition and population
structure may be more influenced by UV-B than overall algal biomass.184 These results suggest
that UV radiation may be a more important factor than previously recognized in determining
community structure in aquatic systems.349
References
1
Häder D-P, Kumar HD, Smith RC, Worrest RC, Aquatic ecosystems: effects of solar
ultraviolet radiation and interactions with other climatic change factors, Photochem.
Photobiol. Sci., 2003, 2, 39-50.
The Environmental Effects Assessment Panel Report for 2006
113
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
114
Häder D-P, Effects of solar ultraviolet radiation on aquatic primary producers, in
Handbook of Photochemistry and Photobiology: Photobiology, Vol. 4 ed.: Nalwa HS, Am.
Sci. Publ., California, USA, 2003, pp. 329-352.
Häder D-P, UV-B impact on the life of aquatic plants, in Modern Trends in Applied
Aquatic Ecology eds.: Ambasht RS, Ambasht NK, Kluwer Acad./Plenum Publ., New York,
Boston, Dordrecht, London, Moscow, 2003, pp. 149-172.
Sinha RP, Häder D-P, UV-induced DNA damage and repair: A review, Photochem.
Photobiol. Sci., 2002, 1, 225-236.
Helbling EW, Zagarese HE, UV Effects in Aquatic Organisms and Ecosystems, Royal
Society of Chemistry, Cambridge, UK, 2003.
Vincent WF, Rautio M, Pienitz R, Climate control of biological UV exposure in polar and
alpine aquatic ecosystems, in Environmental Challenges in Arctic-Alpine Regions, Vol. in
press eds.: Orbaek JB, Kallenborn R, Tombre IM, Springer-Verlag, Berlin, Heidelberg,
New York, 2006.
Gies P, Roy C, Javorniczky J, Henderson S, Lemus-Deschamps L, Driscoll C, Global solar
UV index: Australian measurements, forecasts and comparison with the UK, Photochem.
Photobiol., 2004, 79, 32-39.
Lebert M, Schuster M, Häder D-P, The European Light Dosimeter Network: four years of
measurements, J. Photochem. Photobiol. B., 2002, 66, 81-87.
Martinez-Lozano JA, Marin MJ, Tena F, Utrillas MP, Sanchez-Muniosguren L, GonzalesFrias C, Cuevas E, Redondas A, Lorente J, de Cabo X, Cachorro V, Vergaz R, de Frutos A,
Diaz JP, Exposito FJ, de la Morena B, Vilaplana JM, UV index experimental values during
the years 2000 and 2001 from the Spanish broadband UV-B radiometric network,
Photochem. Photobiol., 2002, 76, 181-187.
McKenzie RL, Björn LO, Bais A, Ilyas M, Changes in biologically active ultraviolet
radiation reaching the Earth's surface, Photochem. Photobiol. Sci., 2003, 2, 5-15.
Solomon S, The hole truth. What's news (and what's not) about the ozone hole, Nature,
2004, 427, 289-291.
Bérces A, Chernouss S, Lammer H, Belisheva NK, Kovacs G, Rontó G, Lichtenegger
HIM, A comparison of solar UV induced DNA-damaging effects between southern and
central Europe and Arctic high latitudes, European Geosciences Union Report No.,
Vienna, Austria, 24-29 April, 2005, p. 1
Cancillo ML, Serrano A, Antón M, García JA, Vilaplana JM, de la Morena B, An
improved outdoor calibration procedure for broadband ultraviolet radiometers, Photochem.
Photobiol., 2005, 81, 860-865.
Kollias N, Baqer A, Sadiq I, Gillies R, Ou-Yang H, Measurement of solar UVB variations
by polysulphone film, Photochem. Photobiol., 2003, 78, 220-224.
Lester RA, Parisi AV, Kimlin MG, Sabburg J, Optical properties of poly(2,6-dimethyl-1,4phenylene oxide) film and its potential for a long-term solar ultraviolet dosimeter, Phys.
Med. Biol., 2003, 48, 3685-3698.
Munakata N, Kazadzis S, Bais AF, Hieda K, Ronto G, Rettberg P, Horneck G,
Comparisons of spore dosimetry and spectral photometry of solar-UV radiation at four
sites in Japan and Europe, Photochem. Photobiol., 2000, 72, 739-745.
Parisi AV, Kimlin MG, Turnbull DJ, Macaranas J, Potential of phenothiazine as a thin film
dosimeter for UVA exposures, Photochem. Photobiol. Sci., 2005, 4, 907-910.
The Environmental Effects Assessment Panel Report for 2006
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
Kramer GD, Herndl GJ, Photo- and bioreactivity of chromophoric dissolved organic matter
produced by marine bacterioplankton, Aquat. Microbial Ecol., 2004, 36, 239-246.
Piazena H, Perez-Rodrigues E, Häder D-P, Lopez-Figueroa F, Penetration of solar
radiation into the water column of the central subtropical Atlantic Ocean - optical
properties and possible biological consequences, Deep-Sea Res. Part II, 2002, 49, 35133528.
Tedetti M, Sempér‚ R, Penetration of ultraviolet radiation in the marine environment. A
review, Photochem. Photobiol., 2006, 82, 389-397.
Steinberg DK, Nelson NB, Craig AC, Prusak A, Production of chromophoric dissolved
organic matter (CDOM) in the open ocean by zooplankton and the colonial
cyanobacterium Trichodesmium spp., Mar. Ecol. Prog. Ser., 2004, 267, 45-56.
Bracchini L, Loiselle S, Dattilo AM, Mazzuoli S, Cózar A, Rossi C, The spatial
distribution of optical properties in the ultraviolet and visible in an aquatic ecosystem,
Photochem. Photobiol., 2004, 80, 139-149.
Williamson CE, Zagarese HE, UVR effects on aquatic ecosystems: a changing climate
perspective, in UV Effects in Aquatic Organisms and Ecosystems eds.: Helbling EW,
Zagarese HE, Royal Society of Chemistry, Cambridge, UK, 2003, pp. 547-567.
Moser KA, Smol JP, MacDonald GM, Larsen CPS, 19th century eutrophication of a
remote boreal lake: a consequence of climate warming?, J. Paleolimnol., 2002, 28, 269281.
Pastor J, Solin J, Bridgham SD, Updegraff K, Harth C, Weishampel P, Dewey B, Global
warming and the export of dissolved organic carbon from boreal peatlands, Oikos., 2003,
100, 380-386.
Leavitt PR, Cumming BF, Smol JP, Reasoner M, Pienitz R, Hodgson DA, Climatic control
of ultraviolet radiation effects on lakes, Limnol. Oceanogr., 2003, 48, 2062-2069.
Sorvari S, Korhola A, Thompson R, Lake diatom response to recent Arctic warming in
Finnish Lapland, Glob. Change Biol., 2002, 8, 171-181.
Holzapfel AM, Vinebrooke RD, Environmental warming increases invasion potential of
alpine lake communities by imported species, Glob. Change Biol., 2005, 11, 2009-2015.
Frenette J-J, Arts MT, Morin J, Spectral gradients of downwelling light in a fluvial lake
(Lake Saint-Pierre, St-Lawrence River), Aquat. Ecol., 2003, 37, 77-85.
Squires MM, Lesack LFW, Spatial and temporal patterns of light attenuation among lakes
of the Mackenzie Delta, Freshwater. Biol., 2003, 48, 1-20.
Bracchini L, Cózar A, Dattilo AM, Picchi MP, Arena C, Mazzuoli S, Loiselle SA,
Modelling the components of the vertical attenuation of ultraviolet radiation in a wetland
lake ecosystem, Ecol. Modell., 2005, 186, 43-54.
Vähätalo AV, Wetzel RG, Paerl HW, Light absorption by phytoplankton and
chromophoric dissolved organic matter in the drainage basin and estuary of the Neuse
River, North Carolina (U.S.A.), Freshwater. Biol., 2005, 50, 477-493.
Brinkmann T, Sartorius D, Frimmel FH, Photobleaching of humic rich dissolved organic
matter, Aquat. Sci., 2003, 65, 415-424.
Klug JL, Bacterial response to dissolved organic matter affects resource availability for
algae, Can. J. Fish. Aquat. Sci., 2005, 62, 472-481.
Pérez AP, Diaz MM, Ferraro MA, Cusminsky GC, Zagarese HE, Replicated mesocosm
study on the role of natural ultraviolet radiation in high CDOM, shallow lakes, Photochem.
Photobiol. Sci., 2003, 2, 118-123.
The Environmental Effects Assessment Panel Report for 2006
115
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
116
De Lange HJ, Morris DP, Williamson CE, Solar ultraviolet photodegradation of DOC may
stimulate freshwater food webs, Journal of Plankton Research, 2003, 25, 111-117.
Molot LA, Keller W, Leavitt PR, Robarts RD, Waiser MJ, Arts MT, Clair TA, Pienitz R,
Yan ND, McNicol DK, Prairie YT, Dillon PJ, Macrae M, Bello R, Nordin RN, Curtis PJ,
Smol JP, Douglas MSV, Risk analysis of dissolved organic matter-mediated ultraviolet B
exposure in Canadian inland waters, Can. J. Fish. Aquat. Sci., 2004, 61, 2511-2521.
Tulonen T, Role of allochthonous and autochthonous dissolved organic matter (DOM) as
a carbon source for bacterioplankton in boreal humic lakes, Dissertation thesis, University
of Helsinki (Helsinki, Finland), 2004.
Findlay SEG, Sinsabaugh RL, Aquatic Ecosystems. Interactivity of Dissolved Organic
Matter, Academic Press, Amsterdam, San Diego, 2003.
Sobek S, Algesten G, Bergström A-K, Jansson M, Tranvik LJ, The catchment and climate
regulation of pCO2 in boreal lakes, Glob. Change Biol., 2003, 9, 630-641.
Anesio AM, Granéli W, Increased photoreactivity of DOC by acidification: implications
for the carbon cycle in humic lakes, Limnol. Oceanogr., 2003, 48, 735-744.
Porcal P, Hejzlar J, Kop cek J, Seasonal and photochemical changes of DOM in an
acidified forest lake and its tributaries, Aquat. Sci., 2004, 66, 211-222.
Qualls RG, Richardson CJ, Factors controlling concentration, export, and decomposition of
dissolved organic nutrients in the Everglades of Florida, Biogeochemistry, 2003, 62, 197229.
Klug JL, Positive and negative effects of allochthonous dissolved organic matter and
inorganic nutrients on phytoplankton growth, Can. J. Fish. Aquat. Sci., 2002, 59, 85-95.
Obernosterer I, Benner R, Competition between biological and photochemical processes in
the mineralization of dissolved organic carbon, Limnol. Oceanogr., 2004, 49, 117-124.
Cockell CS, Córdoba-Jabonero C, Coupling of climate change and biotic UV exposure
through changing snow-ice covers in terrestrial habitats, Photochem. Photobiol., 2004, 79,
26-31.
Dierssen HM, Smith RC, Vernet M, Glacial meltwater dynamics in coastal waters west of
the Antarctic peninsula, Proc. Nat. Acad. Sci. USA., 2002, 99, 1790-1795.
Callieri C, Stockner JG, Freshwater autotrophic picoplankton: a review, J. Limnol., 2002,
61, 1-14.
Cotner JB, Biddanda BA, Small players, large role: microbial influence on biogeochemical
processes in pelagic aquatic ecosystems, Ecosystems, 2002, 5, 105-121.
Jürgens K, Matz C, Predation as a shaping force for the phenotypic and genotypic
composition of planktonic bacteria, Antonie van Leeuwenhoek, 2002, 81, 413-434.
Agogu H, Joux F, Obernosterer I, Lebaron P, Resistance of marine bacterioneuston to solar
radiation, Appl. Environ. Microbiol., 2005, 71, 5282-5289.
Cadet J, Sage E, Douki T, Ultraviolet radiation-mediated damage to cellular DNA, Mutat.
Res., 2005, 571, 3-17.
Häder D-P, Sinha RP, Solar ultraviolet radiation-induced DNA damage in aquatic
organisms: potential environmental imapct, Mutat. Res., 2005, 571, 221-233.
Visser PM, Poos JJ, Scheper BB, Boelen P, van Duyl FC, Diurnal variations in depth
profiles of UV-induced DNA damage and inhibition of bacterioplankton production in
tropical coastal waters, Mar. Ecol. Prog. Ser., 2002, 228, 25-33.
Menck CFM, Shining a light on photolyases, Nat. Genet., 2002, 32, 338-339.
The Environmental Effects Assessment Panel Report for 2006
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
Costa RMA, Chigancas V, Galhardo RdS, Carvalho H, Menck CFM, The eukaryotic
nucleotide excision repair pathway, Biochimie, 2003, 85, 1083-1099.
Xenopoulos MA, Schindler DW, Differential responses to UVR by bacterioplankton and
phytoplankton from the surface and the base of the mixed layer, Freshwater. Biol., 2003,
48, 108-122.
Buma AGJ, de Boer MK, Boelen P, Depth distributions of DNA damage in Antarctic
marine phyto-and bacterioplankton exposed to summertime UV radiation, J. Phycol, 2001,
37, 200-208.
Arrieta JM, Weinbauer MG, Herndl GJ, Interspecific variability in sensitivity to UV
radiation and subsequent recovery in selected isolates of marine bacteria, Appl. Environ.
Microbiol., 2000, 66, 1468-1473.
Joux F, Jeffrey WH, Lebaron P, Mitchell DL, Marine bacterial isolates display diverse
responses to UV-B radiation, Appl. Environ. Microbiol., 1999, 65, 3820-3827.
Carrillo P, Medina-Sánchez JM, Villar-Argaiz M, The interaction of phytoplankton and
bacteria in a high mountain lake: importance of the spectral composition of solar radiation,
Limnol. Oceanogr., 2002, 47, 1294-1306.
Hernández KL, Quinones RA, Daneri G, Helbling EW, Effects of solar radiation on
bacterioplankton production in the upwelling system off central-southern Chile, Mar. Ecol.
Prog. Ser., 2006, 315, 19-31.
Cockell C, Rettberg P, Horneck G, Scherer K, Stokes DM, Measurements of microbial
protection from ultraviolet radiation in polar terrestrial microhabitats, Polar Biol., 2003,
26, 62-69.
Prakash B, Veeregowda BM, Krishnappa G, Biofilms: a survival strategy of bacteria, Curr.
Sci., 2003, 85, 1299-1307.
McCready S, Marcello L, Repair of UV damage in Halobacterium salinarum, Biochem.
Soc. Trans., 2003, 31, 694-698.
Laybourn-Parry J, Hofer JS, Sommaruga R, Viruses in the plankton of freshwater and
saline Antarctic lakes, Freshwater. Biol., 2001, 46, 1279-1287.
Wilhelm SW, Jeffrey WH, Dean AL, Meador J, Pakulski JD, Mitchell DL, UV radiation
induced DNA damage in marine viruses along a latitudinal gradient in the southeastern
Pacific Ocean, Aquat. Microbial Ecol., 2003, 31, 1-8.
Kitamura S-I, Kamata S-I, Nakano S-I, Suzuki S, Solar UV radiation does not inactivate
marine birnavirus in coastal seawater, Dis. Aquat. Org., 2004, 58, 251-254.
Bettarel Y, Sime-Ngando T, Amblard C, Carrias J-F, Portelli C, Virioplankton and
microbial communities in aquatic systems: a seasonal study in two lakes of differing
trophy, Freshwater. Biol., 2003, 48, 810-822.
Jacquet S, Bratbak G, Effects of ultraviolet radiation on marine virus-phytoplankton
interactions, FEMS Microbiol. Ecol., 2003, 44, 279-289.
Danovaro R, Corinaldesi C, Sunscreen products increase virus production through
prophage induction in marine bacterioplankton, Micro. Ecol., 2003, 45, 109-118.
Christaki U, Vázquez-Domínguez E, Courties C, Lebaron P, Grazing impact of different
heterotrophic nanoflagellates on eukaryotic (Ostreococcus tauri) and prokaryotic
picoautotrophs (Prochlorococcus and Synechococcus), Environ. Microbiol., 2005, 7, 12001210.
Llabrés M, Agustí S, Picophytoplankton cell death induced by UV radiation: evidence for
oceanic Atlantic communities, Limnol. Oceanogr., 2006, 51, 21-29.
The Environmental Effects Assessment Panel Report for 2006
117
Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
89
90
118
Sommaruga R, Hofer JS, Alonso-Sáez L, Gasol JM, Differential sunlight sensitivity of
picophytoplankton from surface mediterranean coastal waters, Appl. Environ. Microbiol.,
2005, 71, 2154-2157.
Boelen P, Post AF, Veldhuis MJW, Buma AGJ, Diel patterns of UVBR-induced DNA
damage in picoplankton size fractions from the Gulf of Aqaba, Red Sea, Micro. Ecol.,
2002, 44, 164-174.
Sobrino C, Montero O, Lubián LM, UV-B radiation increases cell permeability and
damages nitrogen incorporation mechanisms in Nannochloropsis gaditana, Aquat. Sci.,
2004, 66, 421-429.
Sinha RP, Häder D-P, Ultraviolet screening compounds in algae: role in evolution, in
Molecular Systematics ed.: Britto SJ, The Rapinat Herbarium & Centre for Molecular
Systematics, Tiruchirappalli, India, 2004, pp. 91-117.
Sinha RP, Stress responses in cyanobacteria, in Modern Trends in Applied Aquatic
Ecology eds.: Ambasht RS, Ambasht NK, Kluwer Acad./Plenum Publ., New York, Boston,
Dordrecht, London, Moscow, 2003, pp. 201-218.
Briand J-F, Jacquet S, Bernard C, Humbert J-F, Health hazards for terrestrial vertebrates
from toxic cyanobacteria in surface water ecosystems, Vet. Res., 2003, 34, 361-377.
Oberholster PJ, Botha A-M, Grobbelaar JU, Microcystis aeruginosa: source of toxic
microcystins in drinking water, Afr. J. Biotechnol., 2004, 3, 159-168.
Staal M, Stal LJ, te Lintel-Hekkert S, Harren FJM, Light action spectra of N2 fixation by
heterocystous cyanobacteria from the Baltic Sea, J. Phycol, 2003, 39, 668-677.
WMO, Scientific Assessment of Ozone Depletion: Executive Summary, UNEP World
Metorological Organization Report No. Global Ozone Research and Monitoring Project Report No. 47, Geneva, Switzerland, pp. 1-20
Kumar A, Tyagi MB, Jha PN, Srinivas G, Singh A, Inactivation of cyanobacterial
nitrogenase after exposure to ultraviolet-B radiation, Curr. Microbiol., 2003, 46, 380-384.
Dillon JG, Miller SR, Castenholz RW, UV-acclimation responses in natural populations of
cyanobacteria (Calothrix sp.), Environ. Microbiol., 2003, 5, 473-483.
Kumar A, Tyagi MB, Jha PN, Evidences showing ultraviolet-B radiation-induced damage
of DNA in cyanobacteria and its detection by PCR assay, Biochem. Biophys. Res.
Commun., 2004, 318, 1025-1030.
Rinalducci S, Hideg É, Vass I, Zolla L, Effect of moderate UV-B irradiation on
Synechocystis PCC 6803 biliproteins, Biochem. Biophys. Res. Commun., 2006, 341, 11051112.
Sinha RP, Kumar A, Tyagi MB, Häder D-P, Ultraviolet-B-induced destruction of
phycobiliproteins in cyanobacteria, Mol. Biol. Plants, 2005, 11, 313-319.
Jiang H, Qiu B, Photosynthetic adaptation of a bloom-forming cyanobacterium Microcystis
aeruginosa (Cyanophyceae) to prolonged UV-B exposure, J. Phycol, 2005, 41, 983-992.
Helbling EW, Gao K, Ai H, Ma Z, Villafane VE, Differential responses of Nostoc
sphaeroides and Arthrospira platensis to solar ultraviolet radiation exposure, J. Appl.
Phycol., 2006, 18, 57-66.
Rajagopal S, Sicora C, Várkonyi Z, Mustárdy L, Mohanty P, Protective effect of
supplemental low intensity white light on ultraviolet-B exposure-induced impairment in
cyanobacterium Spirulina platensis: formation of air vacuoles as a possible protective
measure, Photosyn. Res., 2005, 85, 181-189.
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92
93
94
95
96
97
98
99
100
101
102
103
104
105
106
107
Norris TB, McDermott TR, Castenholz RW, The long-term effects of UV exclusion on the
microbial composition and photosynthetic competence of bacteria in hot-spring microbial
mats, FEMS Microbiol. Ecol., 2002, 39, 193-209.
Prabha GL, Kulandaivelu G, Induced UV-B resistance against photosynthesis damage by
adaptive mutagenesis in Synechococcus PCC 7942, Plant Sci., 2002, 162, 663-669.
Chaloub RM, de Magalhaes CCP, dos Santos CP, Early toxic effects of zinc on PSII of
Synechocystis aquatilis f. aquatilis (Cyanophyceae), J. Phycol, 2005, 41, 1162-1168.
Prasad SM, Zeeshan M, UV-B radiation and cadmium induced changes in growth,
photosynthesis, and antioxidant enzymes of cyanobacterium Plectonema boryanum, Biol.
Plant, 2005, 49, 229-236.
Sinha RP, Richter P, Faddoul J, Braun M, Häder D-P, Effects of UV and visible light on
cyanobacteria at the cellular level, Photochem. Photobiol. Sci., 2002, 1, 553-559.
Cadoret J-C, Rousseau B, Perewoska I, Sicora C, Cheregi O, Vass I, Houmard J, Cyclic
nucleotides, the photosynthetic apparatus and response to UV-B stress in the
cyanobacterium Synechocystis sp. PCC 6803, J. Biol. Chem., 2005, 280, 33935-33944.
Ehling-Schulz M, Schulz S, Wait R, Görg A, Scherer S, The UV-B stimulon of the
terrestial cyanobacterium Nostoc commune comprises early shock proteins and late
acclimation proteins, Mol. Microbiol., 2002, 46, 827-843.
He Y-Y, Klisch M, Häder D-P, Adaptation of cyanobacteria to UV-B stress correlated with
oxidative stress and oxidative damage, Photochem. Photobiol., 2002, 76, 188-196.
He Y-Y, Häder D-P, UV-B-induced formation of reactive oxygen species and oxidative
damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and Nacetyl-L-cysteine, J. Photochem. Photobiol. B., 2002, 66, 115-124.
Tyagi R, Kumar A, Tyagi MB, Jha PN, Kumar HD, Sinha RP, Häder D-P, Protective role
of certain chemicals against UV-B-induced damage in the nitrogen-fixing cyanobacterium,
Nostoc muscorum, J. Basic Microbiol., 2003, 43, 137-147.
Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP, Determination of nitrogen-fixing
phylotypes in Lyngbya sp. and Microcoleus chthonoplastes cyanobacterial mats from
Guerrero Negro, Baja California, Mexico, Appl. Environ. Microbiol., 2004, 70, 2119-2128.
Wu H, Gao K, Villafañe VE, Watanabe T, Helbling EW, Effects of solar UV radiation on
morphology and photosynthesis of filamentous cyanobacterium Arthrospira platensis,
Appl. Environ. Microbiol., 2005, 71, 5004-5013.
Bonilla S, Villeneuve V, Vincent WF, Benthic and planktonic algal communities in a high
Arctic lake: pigment structure and contrasting responses to nutrient enrichment, J. Phycol,
2005, 41, 1120-1130.
Dillon JG, Tatsumi CM, Tandingan PG, Castenholz RW, Effect of environmental factors
on the synthesis of scytonemin, a UV-screening pigment, in a cyanobacterium
(Chroococcidiopsis sp.), Arch. Microbiol., 2002, 177, 322-331.
Liu Z, Häder DP, Sommaruga R, Occurrence of mycosporine-like amino acids (MAAs) in
the bloom-forming cyanobacterium Microcystis aeruginosa, Journal of Plankton Research,
2004, 26, 963-966.
Sinha RP, Häder D-P, Impacts of ultraviolet-B radiation on rice-field cyanobacteria, J.
Photosci., 2002, 9, 439-441.
Conde FR, Churio MS, Previtali CM, The deactivation pathways of the excited-states of
the mycosporine-like amino acids shinorine and porphyra-334 in aqueous solution,
Photochem. Photobiol. Sci., 2004, 3, 960-967.
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119
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108 Sinha RP, Häder D-P, Biochemistry of mycosporine-like amino acids (MAAs) synthesis:
Role in photoprotection, Recent Reseach Development in Biochemistry, 2003, 4, 971-983.
109 Sinha RP, Ambasht NK, Sinha JP, Häder D-P, Wavelength-dependent induction of a
mycosporine-like amino acid in a rice-field cyanobacterium, Nostoc commune: role of
inhibitors and salt stress, Photochem. Photobiol. Sci., 2003, 2, 171-176.
110 Squier AH, Hodgson DA, Keely BJ, A critical assessment of the analysis and distributions
of scytonemin and related UV screening pigments in sediments, Organic Geochem., 2004,
35, 1221-1228.
111 Dillon JG, Castenholz RW, The synthesis of the UV-screening pigment, scytonemin, and
photosynthetic performance in isolates from closely related natural populations of
cyanobacteria (Calothrix sp.), Environ. Microbiol., 2003, 5, 484-491.
112 Turner JT, Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms,
Aquat. Microbial Ecol., 2002, 27, 57-102.
113 Cramer W, Bondeau A, Schaphoff S, Lucht W, Smith B, Sitch S, Tropical forests and the
global carbon cycle: impacts of atmospheric carbon dioxide, climate change and rate of
deforestation, Philos. Trans. R. Soc. Lond. B. Biol. Sci., 2004, 359, 331-343.
114 Bontempi PS, Yoder JA, Spatial variability in SeaWiFS imagery of the South Atlantic
bight as evidenced by gradients (fronts) in chlorophyll a and water-leaving radiance, DeepSea Res. Part II, 2004, 51, 1019-1032.
115 Stuart V, Ulloa O, Alarcón G, Sathyendranath S, Major H, Head EJH, Platt T, Bio-optical
characteristics of phytoplankton populations in the upwelling system off the coast of Chile,
Rev. Chilena Hist. Nat., 2004, 77, 87-105.
116 Teira E, Mourino B, Maranón E, Pérez V, Paz MJ, Serret P, de Armas D, Escánez J,
Woodward EMS, Fernández E, Variability of chlorophyll and primary production in the
Eastern North Atlantic subtropical gyre: potential factors affecting phytoplankton activity,
Deep-Sea Res. Part 1, 2005, 52, 569-588.
117 Xue L, Zhang Y, Zhang T, An L, Wang X, Effects of enhanced ultraviolet-B radiation on
algae and cyanobacteria, Crit. Rev. Microbiol., 2005, 31, 79-89.
118 Bertilsson S, Hansson L-A, Graneli W, Philibert A, Size-selective predation on pelagic
microorganisms in Arctic freshwaters, Journal of Plankton Research, 2003, 25, 621-631.
119 Faulkenham SE, Hall RI, Dillon PJ, Karst-Riddoch T, Effects of drought-induced
acidification on diatom communities in acid-sensitive Ontario lakes, Limnol. Oceanogr.,
2003, 48, 1662-1673.
120 Lafrancois BM, Nydick KR, Johnson BM, Baron JS, Cumulative effects of nutrients and
pH on the plankton of two mountain lakes, Can. J. Fish. Aquat. Sci., 2004, 61, 1153-1165.
121 Litchman E, Neale PJ, UV effects on photosynthesis, growth and acclimation of an
estuarine diatom and cryptomonad, Mar. Ecol. Prog. Ser., 2005, 300, 53-62.
122 Shelly K, Heraud P, Beardall J, Interactive effects of PAR and UV-B radiation on PSII
electron transport in the marine alga Dunaliella tertiolecta (Chlorophyceae), J. Phycol,
2003, 39, 509-512.
123 Glud RN, Rysgaard S, Kühl M, A laboratory study on O2 dynamics and photosynthesis in
ice algal communities: quantification by microsensors, O2 exchange rates, 14C incubations
and a PAM fluorometer, Aquat. Microbial Ecol., 2002, 27, 301-311.
124 Villafañe VE, Gao K, Helbling EW, Short- and long-term effects of solar ultraviolet
radiation on the red algae Porphyridium cruentum (S. F. Gray) Nägeli, Photochem.
Photobiol. Sci., 2005, 4, 376-382.
120
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125 McMinn A, Ryan K, Gademann R, Diurnal changes in photosynthesis of Antarctic fast ice
algal communities determined by pulse amplitude modulation fluorometry, Mar. Biol.,
2003, 143, 359-367.
126 Shelly K, Roberts S, Heraud P, Beardall J, Interactions between UV-B exposure and
phosphorus nutrition. I. Effects on growth, phosphate uptake, and chlorophyll
fluorescence, J. Phycol, 2005, 41, 1204-1211.
127 Xenopoulos MA, Frost PC, UV radiation, phosphorus, and their combined effects on the
taxonomic composition of phytoplankton in a boreal lake, J. Phycol, 2003, 39, 291-302.
128 Aubriot L, Conde D, Bonilla S, Sommaruga R, Phosphate uptake behavior of natural
phytoplankton during exposure to solar ultraviolet radiation in a shallow coastal lagoon,
Mar. Biol., 2004, 144, 623-631.
129 Sargian P, Pelletier É, Mostajir B, Ferreyra GA, Demers S, TBT toxicity on a natural
planktonic assemblage exposed to enhanced ultraviolet-B radiation, Aquat. Toxicol., 2005,
73, 299-314.
130 Pelletier É, Sargian P, Payet J, Demers S, Ecotoxicological effects of combined UVB and
organic contaminants in coastal waters: a review, Photochem. Photobiol., 2006, 82, 981993.
131 Doyle SA, Saros JE, Williamson CE, Interactive effects of temperature and nutrient
limitation on the response of alpine phytoplankton growth to ultraviolet radiation, Limnol.
Oceanogr., 2005, 50, 1362-1367.
132 Mohovic B, Gianesella SMF, Laurion I, Roy S, Ultraviolet B-photoprotection efficiency of
mesocosm-enclosed natural phytoplankton communities from different latitudes: Rimouski
(Canada) and Ubatuba (Brazil), Photochem. Photobiol., 2006, 82, 952-961.
133 Díaz S, Camilión C, Éscobar J, Deferrari G, Roy S, Lacoste K, Demers S, Belzile C,
Ferreyra G, Gianesella S, Gosselin M, Nozais C, Pelletier É, Schloss I, Vernet M,
Simulation of ozone depletion using ambient irradiance supplemented with UV lamps,
Photochem. Photobiol., 2006, 82, 857-864.
134 Bouchard JN, Roy S, Ferreyra G, Campbell DA, Curtosi A, Ultraviolet-B effects on
photosystem II efficiency of natural phytoplankton communities from Antarctica, Polar
Biol., 2005, 28, 607-618.
135 Bouchard JN, Campbell DA, Roy S, Effects of UV-B radiation on the D1 protein repair
cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and
Argentina), J. Phycol, 2005, 41, 273-286.
136 Sicora C, Máté Z, Vass I, The interaction of visible and UV-B light during photodamage
and repair of Photosystem II, Photosyn. Res., 2003, 75, 127-137.
137 Heraud P, Beardall J, Ultraviolet radiation has no effect on respiratory oxygen
consumption or enhanced post-illumination respiration in three species of microalgae, J.
Photochem. Photobiol. B., 2002, 68, 109-116.
138 Davidson A, Belbin L, Exposure of natural Antarctic marine microbial assemblages to
ambient UV radiation: effects on the marine microbial community, Aquat. Microbial Ecol.,
2002, 27, 159-174.
139 Rech M, Mouget J-L, Morant-Manceau A, Rosa P, Tremblin G, Long-term acclimation to
UV radiation: effects on growth, photosynthesis and carbonic anhydrase activity in marine
diatoms, Bot. Mar., 2005, 48, 407-420.
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140 Tank SE, Schindler DW, The role of ultraviolet radiation in structuring epilithic algal
communities in Rocky Mountain montane lakes: evidence from pigments and taxonomy,
Can. J. Fish. Aquat. Sci., 2004, 61, 1461-1474.
141 Lesser MP, Barry TM, Banaszak AT, Effects of UV radiation on a chlorophyte alga
(Scenedesmus sp.) isolated from the fumarole fields of Mt. Erebus, Antarctica, J. Phycol,
2002, 38, 473-481.
142 Wahl M, Molis M, Davis A, Dobretsov S, Dürr ST, Johansson J, Kinley J, Kirugara D,
Langer M, Lotze HK, Thiel M, Thomason JC, Worm B, Ben-Yosef DZ, UV effects that
come and go: a global comparison of marine benthic community level impacts, Glob.
Change Biol., 2004, 10, 1962-1972.
143 Villafañe VE, Marcoval MA, Helbling EW, Photosynthesis versus irradiance
characteristics in phytoplankton assemblages off Patagonia (Argentina): temporal
variability and solar UVR effects, Mar. Ecol. Prog. Ser., 2004, 284, 23-34.
144 Xenopoulos MA, Frost PC, Elser JJ, Joint effects of UV radiation and phosphorus supply
on algal growth rate and elemental composition, Ecol., 2002, 83, 423-435.
145 Vuorio K, Nuottajärvi M, Salonen K, Sarvala J, Spatial distribution of phytoplankton and
picocyanobacteria in Lake Tanganyika in March and April 1998, Aquat. Ecosyst. Health
Manag., 2003, 6, 263-278.
146 Pérez GL, Queimalinos CP, Modenutti BE, Light climate and plankton in the deep
chlorophyll maxima in North Patagonian Andean lakes, Journal of Plankton Research,
2002, 24, 591-599.
147 Helbling EW, Gao K, Goncalves RJ, Wu H, Villafane VE, Utilization of solar UV
radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing,
Mar. Ecol. Prog. Ser., 2003, 259, 59-66.
148 Sfichi L, Ioannidis N, Kotzabasis K, Thylakoid-associated polyamines adjust the UV-B
sensitivity of the photosynthetic apparatus by means of light-harvesting complex II
changes, Photochem. Photobiol., 2004, 80, 499-506.
149 Yu J, Tang X, Zhang P, Tian J, Dong S, Physiological and ultrastructural changes of
Chlorella sp. induced by UV-B radiation, Prog. Nat. Sci., 2005, 15, 678-683.
150 Lesser MP, Oxidative stress in marine environments: biochemistry and physiological
ecology, Annu. Rev. Physiol., 2006, 68, 253-278.
151 Zhang P-Y, Yu J, Tang X-X, UV-B radiation suppresses the growth and antioxidant
systems of two marine microalgae, Platymonas subcordiformis (Wille) Hazen and
Nitzschia closterium (Ehrenb.) W. Sm, J. Integrat. Plant Biol., 2005, 47, 683-691.
152 Häder D-P, Photoinhibition and UV response in the aquatic environment, in
Photoprotection, Photoinhibition, Gene Regulation, and Environment eds.: DemmigAdams B, Adams III WW, Mattoo AK, Springer, The Netherlands, 2006, pp. 87-105.
153 Sobrino C, Neale PJ, Lubián LM, Interaction of UV radiation and inorganic carbon supply
in the inhibition of photosynthesis: spectral and temporal responses of two marine
picoplankters, Photochem. Photobiol., 2005, 81, 384-393.
154 Klisch M, Sinha RP, Häder D-P, UV-absorbing compounds in algae, Cur. Top. Plant Biol.,
2002, 3, 113-120.
155 Llewellyn CA, Harbour DS, A temporal study of mycosporine-like amino acids in surface
water phytoplankton from the English Channel and correlation with solar irradiation, J.
Mar. Biol. Assoc. U.K., 2003, 83, 1-9.
122
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156 Klisch M, Induktion von UV-Schirmpigmenten in marinen Dinoflagellaten, Dissertation
thesis, Friedrich-Alexander University Erlangen-Nürnberg, Germany 2002.
157 Taira H, Aoki S, Yamanoha B, Taguchi S, Daily variation in cellular content of UVabsorbing compounds mycosporine-like amino acids in the marine dinoflagellate
Scrippsiella sweeneyae, J. Photochem. Photobiol. B., 2004, 75, 145-155.
158 Moeller RE, Gilroy S, Williamson CE, Grad G, Sommaruga R, Dietary acquisition of
photoprotective compounds (mycosporine-like amino acids, carotenoids) and acclimation
to ultraviolet radiation in a freshwater copepod, Limnol. Oceanogr., 2005, 50, 427-439.
159 Laurion I, Blouin F, Roy S, Packaging of mycosporine-like amino acids in dinoflagellates,
Mar. Ecol. Prog. Ser., 2004, 279, 297-303.
160 Sinha RP, Gröniger A, Klisch M, Häder D-P, Ultraviolet-B radiation: Photoprotection and
repair in aquatic organisms, Rec. Res. Dev. Photochem. Photobiol., 2002, 6, 107-119.
161 Suh H-J, Lee H-W, Jung J, Mycosporine glycine protects biological systems against
photodynamic damage by quenching singlet oxygen with a high efficiency, Photochem.
Photobiol., 2003, 78, 109-113.
162 Whitehead K, Hedges JI, Photodegradation and photosensitization of mycosporine-like
amino acids, J. Photochem. Photobiol. B., 2005, 80, 115-121.
163 Libkind D, Diéguez MC, Molin‚ M, Pérez P, Zagarese HE, Sommaruga R, van Broock M,
Occurrence of photoprotective compounds in yeasts from freshwater ecosystems of
northwestern Patagonia, Photochem. Photobiol., 2006, 82, 972-980.
164 Libkind D, Sommaruga R, Zagarese H, van Broock M, Mycosporines in carotenogenic
yeasts, Syst. Appl. Micobiol., 2005, 28, 749-754.
165 Pérez P, Libkind D, del Carmen Diéguez M, Summerer M, Sonntag B, Sommaruga R, van
Broock M, Zagarese HE, Mycosporines from freshwater yeasts: a trophic cul-de-sac?,
Photochem. Photobiol. Sci., 2006, 5, 25-30.
166 Gorton HL, Vogelmann TC, Ultraviolet radiation and the snow alga Chlamydomonas
nivalis (Bauer) Wille, Photochem. Photobiol., 2003, 77, 608-615.
167 Steinbrenner J, Linden H, Light induction of carotenoid biosynthesis genes in the green
alga Haematococcus pluvialis: regulation by photosynthetic redox control, Plant Mol.
Biol., 2003, 52, 343-356.
168 White AL, Jahnke LS, Contrasting effects of UV-A and UV-B on photosynthesis and
photoprotection of b-carotene in two Dunaliella spp., Plant. Cell. Physiol., 2002, 43, 877884.
169 Mengelt C, Prézelin BB, A potential novel link between organic nitrogen loading and
Pseudo-nitzschia spp. blooms, in California and the World Ocean 02. Revisiting and
Revising California's Ocean Agenda, October 27-30, 2002, Santa Barbara, California,
USA (Eds.: Magoon OT, Converse H, Baird B, Jines B, Miller-Henson M), 2002, pp. 882896.
170 Merzouk A, Levasseur M, Scarratt M, Michaud S, Gosselin M, Influence of dinoflagellate
diurnal vertical migrations on dimethylsulfoniopropionate and dimethylsulfide distribution
and dynamics (St. Lawrence Estuary, Canada), Can. J. Fish. Aquat. Sci., 2004, 61, 712720.
171 Wolfe GV, Strom SL, Holmes JL, Radzio T, Olson MB, Dimethylsulfoniopropionate
cleavage by marine phytoplankton in response to mechanical, chemical, or dark stress, J.
Phycol, 2002, 38, 948-960.
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172 Le Clainche Y, Levasseur M, Vézina A, Dacey JWH, Saucier FJ, Behaviour of the ocean
DMS(P) pools in the Sargasso Sea viewed in a coupled physical-biogeochemical ocean
model, Can. J. Fish. Aquat. Sci., 2004, 61, 788-803.
173 Simó R, From cells to globe: approaching the dynamics of DMS(P) in the ocean at
multiple scales, Can. J. Fish. Aquat. Sci., 2004, 61, 673-684.
174 Buckley FSE, Mudge SM, Dimethylsulphide and ocean-atmosphere interactions, Chem.
Ecol., 2004, 20, 73-95.
175 Archer SD, Gilbert FJ, Allen JI, Blackford J, Nightingale PD, Modelling of the seasonal
patterns of dimethylsulphide production and fate during 1989 at a site in the North Sea,
Can. J. Fish. Aquat. Sci., 2004, 61, 765-787.
176 O'Dowd CD, Jimenez JL, Bahreini R, Flagan RC, Seinfeld JH, Hämeri K, Pirjola L,
Kulmala M, Jennings SG, Hoffmann T, Marine aerosol formation from biogenic iodine
emissions, Nature, 2002, 417, 632-636.
177 Parisi AV, Downs N, Variation of the enhanced biologically damaging solar UV due to
clouds, Photochem. Photobiol. Sci., 2004, 3, 643-647.
178 Meiners K, Sea-ice communities: structure and composition in Baltic, Antarctic and Arctic
seas, Dissertation thesis, Christian-Albrechts-University, Kiel, Germany 2002.
179 Mock T, Thomas DN, Recent advances in sea-ice microbiology, Environ. Microbiol.,
2005, 7, 605-619.
180 Arrigo KR, Thomas DN, Large scale importance of sea ice biology in the Southern Ocean,
Antarctic Sci., 2004, 16, 471-486.
181 Vinebrooke RD, Schindler DW, Findlay DL, Turner MA, Paterson M, Mills KH, Trophic
dependence of ecosystem resistance and species compensation in experimentally acidified
Lake 302S (Canada), Ecosystems, 2003, 6, 101-113.
182 Belzile C, Demers S, Ferreyra GA, Schloss I, Nozais C, Lacoste K, Mostajir B, Roy S,
Gosselin M, Pelletier É, Gianesella SMF, Vernet M, UV effects on marine planktonic food
webs: a synthesis of results from mesocosm studies, Photochem. Photobiol., 2006, 82, 850856.
183 Vernet M, Introduction: enhanced UV-B radiation in natural ecosystems as an added
perturbation due to ozone depletion, Photochem. Photobiol., 2006, 82, 831-833.
184 Roy S, Mohovic B, Gianesella SMF, Schloss I, Ferrario M, Demers S, Effects of enhanced
UV-B on pigment-based phytoplankton biomass and composition of mesocosm-enclosed
natural marine communities from three latitudes, Photochem. Photobiol., 2006, 82, 909922.
185 Hernando M, Schloss I, Roy S, Ferreyra G, Photoacclimation to long-term ultraviolet
radiation exposure of natural sub-Antarctic phytoplankton communities: fixed surface
incubations versus mixed mesocosms, Photochem. Photobiol., 2006, 82, 923-936.
186 van den Belt M, Bianciotto OA, Costanza R, Demers S, Diaz S, Ferreyra GA, Koch EW,
Momo FR, Vernet M, Mediated modeling of the impacts of enhanced UV-B radiation on
ecosystem services, Photochem. Photobiol., 2006, 82, 865-877.
187 Ferrero E, Eöry M, Ferreyra G, Schloss I, Zagarese H, Vernet M, Momo F, Vertical mixing
and ecological effects of ultraviolet radiation in planktonic communities, Photochem.
Photobiol., 2006, 82, 898-902.
188 Momo F, Ferrero E, Eöry M, Esusy M, Iribarren J, Ferreyra G, Schloss I, Mostajir B,
Demers S, The whole is more than the sum of its parts: modeling community-level effects
of UVR in marine ecosystems, Photochem. Photobiol., 2006, 82, 903-908.
124
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
189 Bischof K, Wiencke C, Auswirkung der Zunahme der UV-Strahlung, in Warnsignale aus
den Polarregionen eds.: Lozan J, Graál H, Hubberten H-W, Hupfer P, Piepenburg D,
Druckerei in St.Pauli, Hamburg, Germany, 2006, pp. 259-263.
190 Johansson G, Snoeijs P, Macroalgal photosynthetic responses to light in relation to thallus
morphology and depth zonation, Mar. Ecol. Prog. Ser., 2002, 244, 63-72.
191 Bischof K, Peralta G, Kräbs G, van de Poll WH, Pérez-Lloréns JL, Breeman AM, Effects
of solar UV-B radiation on canopy structure of Ulva communities from southern Spain, J.
Exp. Bot., 2002, 53, 2411-2421.
192 Roleda MY, Wiencke C, Hanelt D, van de Poll WH, Gruber A, Sensitivity of Laminariales
zoospores from Helgoland (North Sea) to ultraviolet and photosynthetically active
radiation: implications for depth distribution and seasonal reproduction, Plant. Cell.
Environ., 2005, 28, 466-479.
193 Lotze HK, Worm B, Molis M, Wahl M, Effects of UV radiation and consumers on
recruitment and succession of a marine macrobenthic community, Mar. Ecol. Prog. Ser.,
2002, 243, 57-66.
194 Henley WJ, Major KM, Hironaka JL, Response to salinity and heat stress in two
halotolerant chlorophyte algae, J. Phycol, 2002, 38, 757-766.
195 Hanelt D, Wiencke C, Bischof K, Photosynthesis in Marine Macroalgae, in Photosynthesis
in Algae eds.: Larkum AW, Douglas SE, Raven JA, Kluwer Acad. Publ., The Netherlands,
2003, pp. 413-435.
196 Häder D-P, Lebert M, Helbling EW, Effects of solar radiation on the Patagonian
rhodophyte Corallina officinalis (L.), Photosynthsis Research, 2003, 78, 119-132.
197 Häder D-P, Lebert M, Helbling EW, Variable fluorescence parameters in the filamentous
Patagonian rhodophytes, Callithamnion gaudichaudii and Ceramium sp. under solar
radiation, J. Photochem. Photobiol. B., 2004, 73, 87-99.
198 Lüder UH, Wiencke C, Knoetzel J, Acclimation of photosynthesis and pigments during
and after six months of darkness in Palmaria decipiens (Rhodophyta): a study to simulate
Antarctic winter sea ice cover, J. Phycol, 2002, 38, 904-913.
199 Bischof K, Hanelt D, Aguilera J, Karsten U, Vögele B, Sawall T, Wiencke C, Seasonal
variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of
photosynthesis to ultraviolet radiation, Mar. Biol., 2002, 140, 1097-1106.
200 Roleda MY, Wiencke C, Hanelt D, Thallus morphology and optical characteristics affect
growth and DNA damage by UV radiation in juvenile Arctic Laminaria sporophytes,
Planta, 2006, 223, 407-417.
201 Michler T, Aguilera J, Hanelt D, Bischof K, Wiencke C, Long-term effects of ultraviolet
radiation on growth and photosynthetic performance of polar and cold-temperate
macroalgae, Mar. Biol., 2002, 140, 1117-1127.
202 van de Poll WH, Bischof K, Buma AGJ, Breeman AM, Habitat related variation in UV
tolerance of tropical marine red macrophytes is not temperature dependent, Physiol. Plant.,
2003, 118, 74-83.
203 Roleda MY, van de Poll WH, Hanelt D, Wiencke C, PAR and UVBR effects on
photosynthesis, viability, growth and DNA in different life stages of two coexisting
Gigartinales: implications for recruitment and zonation pattern, Mar. Ecol. Prog. Ser.,
2004, 281, 37-50.
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204 Bouchard JN, Roy S, Campbell DA, UVB effects on the photosystem II-D1 protein of
phytoplankton and natural phytoplankton communities, Photochem. Photobiol., 2006, 82,
936-951.
205 Gómez I, Figueroa FL, Huovinen P, Ulloa N, Morales V, Photosynthesis of the red alga
Gracilaria chilensis under natural solar radiation in an estuary in southern Chile,
Aquacukture, 2005, 244, 369-382.
206 Hanelt D, Hawes I, Rae R, Reduction of UV-B radiation causes an enhancement of
photoinhibition in high light stressed aquatic plants from New Zealand lakes, J.
Photochem. Photobiol. B., 2006, 84, 89-102.
207 Holzinger A, Lütz C, Karsten U, Wiencke C, The effect of ultraviolet radiation on
ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia
dentata from Arctic waters, Plant Biol., 2004, 6, 568-577.
208 Poppe F, Schmidt RAM, Hanelt D, Wiencke C, Effects of UV radiation on the
ultrastructure of several red algae, Phyco. Res., 2003, 51, 11-19.
209 Bischof K, Kräbs G, Wiencke C, Hanelt D, Solar ultraviolet radiation affects the activity of
ribulose-1,5-bisphosphate carboxylase-oxygenase and the composition of photosynthetic
and xanthophyll cycle pigments in the intertidal green alga Ulva lactuca L., Planta, 2002,
215, 502-509.
210 Sinha RP, Barbieri ES, Lebert M, Helbling EW, Häder D-P, Effects of solar radiation on
phycobiliproteins of marine red algae, Trends Photochem. Photobiol., 2003, 10, 149-157.
211 van de Poll WH, Hanelt D, Hoyer K, Buma AGJ, Breeman AM, Ultraviolet-B-induced
cyclobutane-pyrimidine dimer formation and repair in Arctic marine macrophytes,
Photochem. Photobiol., 2002, 76, 493-500.
212 Wolfe-Simon F, Grzebyk D, Schofield O, Falkowski PG, The role and evolution of
superoxide dismutases in algae, J. Phycol, 2005, 41, 453-465.
213 Aguilera J, Bischof K, Karsten U, Hanelt D, Wiencke C, Seasonal variation in
ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation
and biochemical defence systems against high light stress, Mar. Biol., 2002, 140, 10871095.
214 Wiencke C, Clayton MN, Schoenwaelder M, Sensitivity and acclimation to UV radiation
of zoospores from five species of Laminariales from the Arctic, Mar. Biol., 2004, 145, 3139.
215 Schoenwaelder MEA, Wiencke C, Clayton MN, Glombitza KW, The effect of elevated UV
radiation on Fucus spp. (Fucales, Phaeophyta) zygote and embryo development, Plant
Biol., 2003, 5, 366-377.
216 Han T, Han Y-S, Kain JM, Häder D-P, Thallus differentiation of photosynthesis, growth,
reproduction, and UV-B sensitivity in the green alga Ulva pertusa (Chlorophyceae), J.
Phycol, 2003, 39, 712-721.
217 Han T, Kong J-A, Han Y-S, Kang S-H, Häder D-P, UV-A/blue light-induced reactivation
of spore germination in UV-B irradiated Ulva pertusa (Chlorophyta), J. Phycol, 2004, 40,
315-322.
218 Wiencke C, Roleda MY, Gruber A, Clayton MN, Bischof K, Susceptibility of zoospores to
UV radiation determines upper depth distribution limit of Arctic kelps: evidence through
field experiments, J. Ecol., 2006, 94, 455-463.
219 Hoyer K, Karsten U, Wiencke C, Induction of sunscreen compounds in Antarctic
macroalgae by different radiation conditions, Mar. Biol., 2002, 141, 619-627.
126
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220 Huovinen P, Gómez I, Figueroa FL, Ulloa N, Morales V, Lovengreen C, Ultravioletabsorbing mycosporine-like amino acids in red macroalgae from Chile, Bot. Mar., 2004,
47, 21-29.
221 Misonou T, Saitoh J, Oshiba S, Tokitomo Y, Maegawa M, Inoue Y, Hori H, Sakurai T,
UV-absorbing substance in the red alga Porphyra yezoensis (Bangiales, Rhodophyta)
block thymine photodimer production, Mar. Biotechnol., 2003, 5, 194-200.
222 Sinha RP, Häder D-P, Photoprotection in cyanobacteria, Recent Reseach Development in
Biochemistry, 2003, 4, 915-924.
223 Korbee N, Huovinen P, Figueroa FL, Aguilera J, Karsten U, Availability of ammonium
influences photosynthesis and the accumulation of mycosporine-like amino acids in two
Porphyra species (Bangiales, Rhodophyta), Mar. Biol., 2005, 146, 645-654.
224 Kräbs G, Bischof K, Hanelt D, Karsten U, Wiencke C, Wavelength-dependent induction of
UV-absorbing mycosporine-like amino acids in the red alga Chondrus crispus under
natural solar radiation, J. Exp. Mar. Biol. Ecol., 2002, 268, 69-82.
225 Kräbs G, Watanabe M, Wiencke C, A monochromatic action spectrum for the
photoinduction of the UV-absorbing mycosporine-like amino acid shinorine in the red alga
Chondrus crispus, Photochem. Photobiol., 2004, 79, 515-519.
226 Karsten U, Friedl T, Schumann R, Hoyer K, Lembcke S, Mycosporine-like amino acids
and phylogenies in green algae: Prasiola and its relatives from the Trebouxiophyceae
(Chlorophyta), J. Phycol, 2005, 41, 557-566.
227 Han Y-S, Han T, UV-B induction of UV-B protection in Ulva pertusa (Chlorophyta), J.
Phycol, 2005, 41, 523-530.
228 Roleda MY, Hanelt D, Wiencke C, Growth kinetics related to physiological parameters in
young Saccorhiza dermatodea and Alaria esculenta sporophytes exposed to UV radiation,
Polar Biol., 2005, 28, 539-549.
229 Hoyer K, Karsten U, Wiencke C, Inventory of UV-absorbing mycosporine-like amino
acids in polar macroalgae and factors controlling their content, in Antarctic Biology in a
Global Context eds.: Huiskes AHL, Gieskes WWC, Rozema J, Schorno RML, van der
Vies SM, Wolff WJ, Backhuys Publ., Leiden, The Netherlands, 2003, pp. 56-62.
230 Aguilera J, Dummermuth A, Karsten U, Schriek R, Wiencke C, Enzymatic defences
against photooxidative stress induced by ultraviolet radiation in Arctic marine macroalgae,
Polar Biol., 2002, 25, 432-441.
231 de Bakker NVJ, van Bodegom PM, van de Poll WH, Boelen P, Nat E, Rozema J, Aerts R,
Is UV-B radiation affecting charophycean algae in shallow freshwater systems?, New.
Phytol., 2005, 166, 957-966.
232 Martínez-Abaigar J, Núnez-Olivera E, Beaucourt N, García-Álvaro MA, Tomás R, Arróniz
M, Different physiological responses of two aquatic bryophytes to enhanced ultraviolet-B
radiation, J. Bryol., 2003, 25, 17-30.
233 Arróniz-Crespo M, Núnez-Olivera E, Martínez-Abaigar J, A survey of the distribution of
UV-absorbing compounds in aquatic bryophytes from a mountain stream, Bryologist.,
2004, 107, 202-208.
234 Duarte CM, The future of seagrass meadows, Environ. Conserv., 2002, 29, 192-206.
235 Cozza R, Chiappetta A, Petrarulo M, Salimonti A, Rende F, Bitonti MB, Innocenti AM,
Cytophysiological features of Posidonia oceanica as putative markers of environmental
conditions, Chem. Ecol., 2004, 20, 215-223.
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236 Figueroa FL, Jiménez C, Vinegla B, Pérez-Rodríguez E, Aguilera J, Flores-Moya A,
Altamirano M, Lebert M, Häder D-P, Effects of solar UV radiation on photosynthesis of
the marine angiosperm Posidonia oceanica from southern Spain, Mar. Ecol. Prog. Ser.,
2002, 230, 59-70.
237 Brandt LA, Koch EW, Periphyton as a UV-B filter on seagrass leaves: a result of different
transmittance in the UV-B and PAR ranges, Aquat. Bot., 2003, 76, 317-327.
238 Squires MM, Lesack LFW, Huebert D, The influence of water transparency on the
distribution and abundance of macrophytes among lakes of the Mackenzie Delta, Western
Canadian Arctic, Freshwater. Biol., 2002, 47, 2123-2135.
239 Casati P, Lara MV, Andreo CS, Regulation of enzymes involved in C4 photosynthesis and
the antioxidant metabolism by UV-B radiation in Egeria densa, a submersed aquatic
species, Photosyn. Res., 2002, 71, 251-264.
240 Babu TS, Akhtar TA, Lampi MA, Tripuranthakam S, Dixon DG, Greenberg BM, Similar
stress responses are elicited by copper and ultraviolet radiation in the aquatic plant Lemna
gibba: implication of reactive oxygen species as common signals, Plant. Cell. Physiol.,
2003, 44, 1320-1329.
241 Collins SA, UV-B sensitivity of aquatic plants: the impact of artificial ultraviolet radiation
on the survival and chlorophyll content of Lemna minor and Spirodela polyrhiza, MSc
thesis, University of Winnipeg (Winnipeg, Canada), 2005.
242 Zagarese HE, Tartarotti B, Suárez DAA, The significance of ultraviolet radiation for
aquatic animals, in Modern Trends in Applied Aquatic Ecology eds.: Ambasht RS,
Ambasht NK, Kluwer Acad./Plenum Publ., New York, Boston, Dordrecht, London,
Moscow, 2003, pp. 173-200.
243 DeLong EF, Karl DM, Genomic perspectives in microbial oceanography, Nature, 2005,
437, 336-342.
244 Marinone MC, Marque SM, Suarez DA, del Carmen Diéguez M, Pérez P, De Los Ríos P,
Soto D, Zagarese HE, UV radiation as a potential driving force for zooplankton
community structure in Patagonian lakes, Photochem. Photobiol., 2006, 82, 962-971.
245 Rautio M, Korhola A, UV-induced pigmentation in subarctic Daphnia, Limnol. Oceanogr.,
2002, 47, 295-299.
246 Leech DM, Padeletti A, Williamson CE, Zooplankton behavioral responses to solar UV
radiation vary within and among lakes, Journal of Plankton Research, 2005, 27, 461-471.
247 Dattilo AM, Bracchini L, Carlini L, Loiselle S, Rossi C, Estimate of the effects of
ultraviolet radiation on the mortality of Artemia franciscana naupliar and adult stages, Int.
J. Biometeorol., 2005, 49, 388-395.
248 Hansson L-A, Plasticity in pigmentation induced by conflicting threats from predation and
UV radiation, Ecol., 2004, 85, 1005-1016.
249 Fischer JM, Fields PA, Pryzbylkowski PG, Nicolai JL, Neale PJ, Sublethal exposure to UV
radiation affects respiration rates of the freshwater cladoceran Daphnia catawba,
Photochem. Photobiol., 2006, 82, 547-550.
250 Boeing WJ, Leech DM, Williamson CE, Cooke S, Torres L, Damaging UV radiation and
invertebrate predation: conflicting selective pressures for zooplankton vertical distribution
in the water column of low DOC lakes, Oecologia, 2004, 138, 603-612.
251 Helbling EW, Zaratti F, Sala LO, Palenque ER, Menchi CF, Villafane VE, Mycosporinelike amino acids protect the copepod Boeckella titicacae (Harding) against high levels of
solar UVR, Journal of Plankton Research, 2002, 24, 1191-1216.
128
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252 Rocco VE, Oppezzo O, Pizarro R, Sommaruga R, Ferraro M, Zagarese HE, Ultraviolet
damage and counteracting mechanisms in the freshwater copepod Boeckella poppei from
the Antarctic Peninsula, Limnol. Oceanogr., 2002, 47, 829-836.
253 Tartarotti B, Sommaruga R, Seasonal and ontogenetic changes of mycosporine-like amino
acids in planktonic organisms from an alpine lake, Limnol. Oceanogr., 2006, 51, 15301541.
254 Grad G, Burnett BJ, Williamson CE, UV damage and photoreactivation: Timing and age
are everything, Photochem. Photobiol., 2003, 78, 225-227.
255 Gonçalves RJ, Villafane VE, Helbling EW, Photorepair activity and protective compounds
in two freshwater zooplankton species (Daphnia menucoensis and Metacyclops
mendocinus) from Patagonia, Argentina, Photochem. Photobiol. Sci., 2002, 1, 996-1000.
256 Ramos-Jiliberto R, Dauelsberg P, Zúniga LR, Differential tolerance to ultraviolet-B light
and photoenzymatic repair in cladocerans from a Chilean lake, Mar. Freshwater Res.,
2004, 55, 193-200.
257 Williamson CE, Grad G, De Lange HJ, Gilroy S, Karapelou DM, Temperature-dependent
ultraviolet responses in zooplankton: implications of climate change, Limnol. Oceanogr.,
2002, 47, 1844-1848.
258 MacFadyen EJ, Williamson CE, Grad G, Lowery M, Jeffrey WH, Mitchell DL, Molecular
response to climate change: temperature dependence of UV-induced DNA damage and
repair in the freshwater crustacean Daphnia pulicaria, Glob. Change Biol., 2004, 10, 408416.
259 Persaud AD, Williamson CE, Ultraviolet and temperature effects on planktonic rotifers and
crustaceans in northern temperate lakes, Freshwater. Biol., 2005, 50, 467-476.
260 Sanders RW, Macaluso AL, Sardina TJ, Mitchell DL, Photoreactivation in two freshwater
ciliates: differential responses to variations in UV-B flux and temperature, Aquat.
Microbial Ecol., 2005, 40, 283-292.
261 Herbert TD, Schuffert JD, Andreasen D, Heusser L, Lyle M, Mix A, Ravelo AC, Stott LD,
Herguera JC, The California current, Devils Hole, and pleistocene climate - Response,
Science., 2002, 296, U1-U2.
262 De Lange HJ, Lürling M, Effects of UV-B irradiated algae on zooplankton grazing,
Hydrobiologia., 2003, 491, 133-144.
263 De Lange HJ, Van Reeuwijk PL, Negative effects of UVB-irradiated phytoplankton on life
history traits and fitness of Daphnia magna, Freshwater. Biol., 2003, 48, 678-686.
264 Tank SE, Schindler DW, Arts MT, Direct and indirect effects of UV radiation on benthic
communities: epilithic food quality and invertebrate growth in four montane lakes, Oikos.,
2003, 103, 651-667.
265 McKee D, Atkinson D, Collings S, Eaton J, Harvey I, Heyes T, Hatton K, Wilson D, Moss
B, Macro-zooplankter responses to simulated climate warming in experimental freshwater
microcosms, Freshwater. Biol., 2002, 47, 1557-1570.
266 Fritz SC, Engstrom DR, Juggins S, Patterns of early lake evolution in boreal landscapes: a
comparison of stratigraphic inferences with a modern chronosequence in Glacier Bay,
Alaska, Holocene, 2004, 14, 828-840.
267 Williamson CE, Olson OG, Lott SE, Walker ND, Engstrom DR, Hargreaves BR,
Ultraviolet radiation and zooplankton community structure following deglaciation in
Glacier Bay, Alaska, Ecol., 2001, 82, 1748-1760.
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268 Cooney RP, Pantos O, Le Tissier MDA, Barer MR, O'Donnell AG, Bythell JC,
Characterization of the bacterial consortium associated with black band disease in coral
using molecular microbiological techniques, Environ. Microbiol., 2002, 4, 401-413.
269 Centeno CJ, Effects of recent warming events on coral reef communities of Costa Rica
(Central America), University of Bremen (Bremen, Germany), 2002.
270 Hallock P, Barnes K, Fisher EM, Coral-reef risk assessment from satellites to molecules: a
multi-scale approach to environmental monitoring and risk assessment of coral reefs,
Environ. Micropaleontol. Microbiol. Meiobenthol., 2004, 1, 11-39.
271 McClanahan TR, The near future of coral reefs, Environ. Conserv., 2002, 29, 460-483.
272 Sheppard C, Loughland R, Coral mortality and recovery in response to increasing
temperature in the southern Arabian Gulf, Aquat. Ecosyst. Health Manag., 2002, 5, 395402.
273 Kline DI, The effects of anthropogenic stress on the coral holobiont: new insights into
coral disease, Dissertation thesis, University of California (San Diego, CA, USA), 2004.
274 Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, Merle P-L,
Tambutt‚ S, The symbiotic anthozoan: a physiological chimera between alga and animal,
Integr. Comp. Biol., 2005, 45, 595-604.
275 Smith DJ, Suggett DJ, Baker NR, Is photoinhibition of zooxanthellae photosynthesis the
primary cause of thermal bleaching in corals?, Glob. Change Biol., 2005, 11, 1-11.
276 Nakamura T, van Woesik R, Yamasaki H, Photoinhibition of photosynthesis is reduced by
water flow in the reef-building coral Acropora digitifera, Mar. Ecol. Prog. Ser., 2005, 301,
109-118.
277 Coles SL, Brown BE, Coral bleaching-capacity for acclimatization and adaptation, Adv.
Mar. Biol., 2003, 46, 183-223.
278 Buck BH, Rosenthal H, Saint-Paul U, Effect of increased irradiance and thermal stress on
the symbiosis of Symbiodinium microadriaticum and Tridacna gigas, Aquat. Living
Resour., 2002, 15, 107-117.
279 Wilson WH, Dale AL, Davy JE, Davy SK, An enemy within? Observations of virus-like
particles in reef corals, Coral Reefs, 2005, 24, 145-148.
280 Levy O, Dubinsky Z, Achituv Y, Photobehavior of stony corals: responses to light spectra
and intensity, J. Exp. Biol., 2003, 206, 4041-4049.
281 Jones RJ, Kerswell AP, Phytotoxicity of Photosystem II (PSII) herbicides to coral, Mar.
Ecol. Prog. Ser., 2003, 261, 149-159.
282 Shick JM, The continuity and intensity of ultraviolet irradiation affect the kinetics of
biosynthesis, accumulation, and conversion of mycosporine-like amino acids (MAAs) in
the coral Stylophora pistillata, Limnol. Oceanogr., 2004, 49, 442-458.
283 Stoletzki N, Schierwater B, Genetic and color morph differentiation in the Caribbean sea
anemone Condylactis gigantea, Mar. Biol., 2005, 147, 747-754.
284 Shick JM, Dunlap WC, Pearse JS, Pearse VB, Mycosporine-like amino acid content in four
species of sea anemones in the genus Anthopleura reflects phylogenetic but not
environmental or symbiotic relationships, Biol. Bull., 2002, 203, 315-330.
285 Lesser MP, Kruse VA, Barry TM, Exposure to ultraviolet radiation causes apoptosis in
developing sea urchin embryos, J. Exp. Biol., 2003, 206, 4097-4103.
286 Lesser MP, Barry TM, Lamare MD, Barker MF, Biological weighting functions for DNA
damage in sea urchin embryos exposed to ultraviolet radiation, J. Exp. Mar. Biol. Ecol.,
2006, 328, 10-21.
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287 Lesser MP, Barry TM, Survivorship, development, and DNA damage in echinoderm
embryos and larvae exposed to ultraviolet radiation (290-400 nm), J. Exp. Mar. Biol. Ecol.,
2003, 292, 75-91.
288 Karentz D, Bosch I, Mitchell DM, Limited effects of Antarctic ozone depletion on sea
urchin development, Mar. Biol., 2004, 145, 277-292.
289 Lesser MP, Lamare MD, Barker MF, Transmission of ultraviolet radiation through the
Antarctic annual sea ice and its biological effects on sea urchin embryos, Limnol.
Oceanogr., 2004, 49, 1957-1963.
290 Lips KR, Reeve JD, Witters LR, Ecological traits predicting amphibian population declines
in Central America, Conserv. Biol., 2003, 17, 1078-1088.
291 Mendelson JR, III, Lips KR, Gagliardo RW, Rabb GB, Collins JP, Diffendorfer JE, Daszak
P, Ibáñez D R, Zippel KC, Lawson DP, Wright KM, Stuart SN, Gascon C, da Silva HR,
Burrowes PA, Joglar RL, La Marca E, Lötters S, du Preez LH, Weldon C, Hyatt A,
Rodriguez-Mahecha JV, Hunt S, Robertson H, Lock B, Raxworthy CJ, Frost DR, Lacy
RC, Alford RA, Campbell JA, Parra-Olea G, Bolaños F, Domingo JJC, Halliday T,
Murphy JB, Wake MH, Coloma LA, Kuzmin SL, Price MS, Howell KM, Lau M,
Pethiyagoda R, Boone M, Lannoo MJ, Blaustein AR, Dobson A, Griffiths RA, Crump ML,
Wake DB, Brodie ED, Jr, Confronting amphibian declines and extinctions, Science., 2006,
313, 48.
292 Gibbs JP, Whiteleather KK, Schueler FW, Changes in frog and toad populations over 30
years in New York State, Ecol. Appl., 2005, 15, 1148-1157.
293 Hecnar SJ, Great Lakes wetlands as amphibian habitats: a review, Aquat. Ecosyst. Health
Manag., 2004, 7, 289-303.
294 Browman HI, Vetter RD, Rodriguez CA, Cullen JJ, Davis RF, Lynn E, St.Pierre J-F,
Ultraviolet (280-400 nm)-induced DNA damage in the eggs and larvae of Calanus
finmarchicus G. (Copepoda) and Atlantic cod (Gadus morhua), Photochem. Photobiol.,
2003, 77, 397-404.
295 Hazell D, Osborne W, Lindenmayer D, Impact of post-European stream change on frog
habitat: southeastern Australia, Biodiver. Conser., 2003, 12, 301-320.
296 Houlahan JE, Findlay CS, The effects of adjacent land use on wetland amphibian species
richness and community composition, Can. J. Fish. Aquat. Sci., 2003, 60, 1078-1094.
297 Johansson M, Effects of agriculture on abundance, genetic diversity and fitness in the
common frog, Rana temporaria, Dissertation thesis, Uppsala University, Sweden 2004.
298 Burrowes PA, Joglar RL, Green DE, Potential causes for amphibian declines in Puerto
Rico, Herpetologica., 2004, 60, 141-154.
299 Carey C, Alexander MA, Climate change and amphibian declines: is there a link?, Div.
Distrib., 2003, 9, 111-121.
300 Brodkin M, Vatnick I, Simon M, Hopey H, Butler-Holston K, Leonard M, Effects of acid
stress in adult Rana pipiens, J. Exp. Zool., 2003, 298A, 16-22.
301 Räsänen K, Laurila A, Merilä J, Carry-over effects of embryonic acid conditions on
development and growth of Rana temporaria tadpoles, Freshwater. Biol., 2002, 47, 19-30.
302 Storrs SI, Kiesecker JM, Survivorship patterns of larval amphibians exposed to low
concentrations of atrazine, Environ. Hlth. Perspect., 2004, 112, 1054-1057.
303 Glennemeier KA, Begnoche LJ, Impact of organochlorine contamination on amphibian
populations in southwestern Michigan, J. Herpetol., 2002, 36, 233-244.
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304 Relyea RA, The lethal impacts of Roundup and predatory stress on six species of North
American tadpoles, Arch. Environ. Contam. Toxicol., 2005, 48, 351-357.
305 Taylor B, Skelly D, Demarchis LK, Slade MD, Galusha D, Rabinowitz PM, Proximity to
pollution sources and risk of amphibian limb malformation, Environ. Hlth. Perspect.,
2005, 113, 1497-1501.
306 Metts BS, Hopkins WA, Nestor JP, Interaction of an insecticide with larval density in
pond-breeding salamanders (Ambystoma), Freshwater. Biol., 2005, 50, 685-696.
307 Ortiz ME, Marco A, Saiz N, Lizana M, Impact of ammonium nitrate on growth and
survival of six European amphibians, Arch. Environ. Contam. Toxicol., 2004, 47, 234-239.
308 Johnson PTJ, Chase JM, Parasites in the food web: linking amphibian malformations and
aquatic eutrophication, Ecol. Lett., 2004, 7, 521-526.
309 Matthews KR, Knapp RA, Pope KL, Garter snake distributions in high-elevation aquatic
ecosystems: Is there a link with declining amphibian populations and nonnative trout
introductions?, J. Herpetol., 2002, 36, 16-22.
310 Hamer A, Lane S, Mahony M, The role of introduced mosquitofish (Gambusia holbrooki)
in excluding the native green and golden bell frog (Litoria aurea) from original habitats in
south-eastern Australia, Oecologia, 2002, 132, 445-452.
311 Knapp RA, Effects of nonnative fish and habitat characteristics on lentic herpetofauna in
Yosemite National Park, USA, Biol. Conserv., 2005, 121, 265-279.
312 Blaustein AR, Romansic JM, Kiesecker JM, Hatch AC, Ultraviolet radiation, toxic
chemicals and amphibian population declines, Div. Distrib., 2003, 9, 123-140.
313 Boone MD, Semlitsch RD, Interactions of bullfrog tadpole predators and an insecticide:
predation release and facilitation, Oecologia, 2003, 137, 610-616.
314 Denoel M, Dzukic G, Kalezic ML, Effects of widespread fish introductions on
paedomorphic newts in Europe, Conserv. Biol., 2005, 19, 162-170.
315 Parris MJ, Beaudoin JG, Chytridiomycosis impacts predator-prey interactions in larval
amphibian communities, Oecologia, 2004, 140, 626-632.
316 Muths E, Corn PS, Pessier AP, Green DE, Evidence for disease-related amphibian decline
in Colorado, Biol. Conserv., 2003, 110, 357-365.
317 Johnson PTJ, Lunde KB, Zelmer DA, Werner JK, Limb deformities as an emerging
parasitic disease in amphibians: evidence from museum specimens and resurvey data,
Conserv. Biol., 2003, 17, 1724-1737.
318 Bell BD, Carver S, Mitchell NJ, Pledger S, The recent decline of a New Zealand endemic:
how and why did populations of Archey's frog Leiopelma archeyi crash over 1996-2001?,
Biol. Conserv., 2004, 120, 193-203.
319 Blaustein AR, Romansic JM, Scheessele EA, Han BA, Pessier AP, Longcore JE,
Interspecific variation in susceptibility of frog tadpoles to the pathogenic fungus
Batrachochytrium dendrobatidis, Conserv. Biol., 2005, 19, 1460-1468.
320 Gardiner D, Ndayibagira A, Grün F, Blumberg B, Deformed frogs and environmental
retinoids, Pure. Appl. Chem., 2003, 75, 2263-2273.
321 Kiesecker JM, Belden LK, Shea K, Rubbo MJ, Amphibian decline and emerging disease,
Am. Sci., 2004, 92, 138-147.
322 Blaustein AR, Johnson PTJ, Explaining frog deformities, Sci. Am., 2003, 288, 60-65.
323 Roy D, Amphibians as environmental sentinels, J. Biosci., 2002, 27, 187-188.
324 Blaustein AR, Kiesecker JM, Complexity in conservation: lessons from the global decline
of amphibian populations, Ecological Letters, 2002, 5, 597-608.
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325 Blaustein AR, Kats LB, Amphibians in a very bad light, Bioscience., 2003, 53, 1028-1029.
326 Licht LE, Shedding light on ultraviolet radiation and amphibian embryos, Bioscience.,
2003, 53, 551-561.
327 Ankley GT, Diamond SA, Tietge JE, Holcombe GW, Jensen KM, DeFoe DL, Peterson R,
Assessment of the risk of solar ultraviolet radiation to amphibians. I. Dose-dependent
induction of hindlimb malformations in the northern leopard frog (Rana pipiens), Environ.
Sci. Technol., 2002, 36, 2853-2858.
328 Peterson GS, Johnson LB, Axler RP, Diamond SA, Assessment of the risk of solar
ultraviolet radiation to amphibians. II. In situ characterization of exposure in amphibian
habitats, Environ. Sci. Technol., 2002, 36, 2859-2865.
329 Tietge JE, Diamond SA, Ankley GT, DeFoe DL, Holcombe GW, Jensen KM, Degitz SJ,
Elonen GE, Hammer E, Ambient solar UV radiation causes mortality in larvae of three
species of Rana under controlled exposure conditions, Photochem. Photobiol., 2001, 74,
261-268.
330 Brooks PD, O'Reilly CM, Diamond SA, Campbell DH, Knapp R, Bradford D, Corn PS,
Hossack B, Tonnessen K, Spatial and temporal variability in the amount and source of
dissolved organic carbon: implications for ultraviolet exposure in amphibian habitats,
Ecosystems, 2005, 18, 1-10.
331 Palen WJ, Williamson CE, Clauser AA, Schindler DE, Impact of UV-B exposure on
amphibian embryos: linking species physiology and oviposition behaviour, Proc. R. Soc.
Lond. B. Biol. Sci., 2005, 272, 1227-1234.
332 Belden LK, Blaustein AR, UV-B induced skin darkening in larval salamanders does not
prevent sublethal effects of exposure on growth, Copeia., 2002, 2002, 748-754.
333 Blaustein AR, Belden LK, Amphibian defenses against ultraviolet-B radiation, Evol. Dev.,
2003, 5, 89-97.
334 Zamzow JP, Effects of diet, ultraviolet exposure, and gender on the ultraviolet absorbance
of fish mucus and ocular structures, Mar. Biol., 2004, 144, 1057-1064.
335 Ylönen O, Karjalainen J, Growth and survival of European whitefish larvae under
enhanced UV-B irradiance, J. Fish Biol., 2004, 65, 869-875.
336 Chatzifotis S, Pavlidis M, Jimeno CD, Vardanis G, Sterioti A, Divanach P, The effect of
different carotenoid sources on skin coloration of cultured red porgy (Pagrus pagrus),
Aquacult. Res., 2005, 36, 1517-1525.
337 Adachi K, Kato K, Wakamatsu K, Ito S, Ishimaru K, Hirata T, Murata O, Kumai H, The
histological analysis, colorimetric evaluation, and chemical quantification of melanin
content in 'suntanned' fish, Pigment Cell Res., 2005, 18, 465-468.
338 Häkkinen J, Vehniäinen E, Oikari A, Histopathological responses of newly hatched larvae
of whitefish (Coregonus lavaretus s.l.) to UV-B induced toxicity of retene, Aquat. Toxicol.,
2003, 63, 159-171.
339 Wiegand MD, Young DLW, Gajda BM, Thuen DJM, Rittberg DAH, Huebner JD,
Loadman NL, Ultraviolet light-induced impairment of goldfish embryo development and
evidence for photorepair mechanisms, J. Fish Biol., 2004, 64, 1242-1256.
340 Gajda BM, Shedding light on the photorepair of ultraviolet radiation induced DNA
damage in goldfish (Carassius auratus) embryos, MSc thesis, Department of Biology,
University of Winnipeg (Winnipeg, Canada), 2003.
341 Yabu T, Ishibashi Y, Yamashita M, Stress-induced apoptosis in larval embryos of Japanese
flounder, Fish. Sci., 2003, 69, 1218-1223.
The Environmental Effects Assessment Panel Report for 2006
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Effects of solar UV radiation on aquatic ecosystems and interactions with climate change
342 Alemanni ME, Lozada M, Zagarese HE, Assessing sublethal effects of ultraviolet radiation
in juvenile rainbow trout (Oncorhynchus mykiss), Photochem. Photobiol. Sci., 2003, 2,
867-870.
343 Huff DD, Grad G, Williamson CE, Environmental constraints on spawning depth of yellow
perch: the roles of low temperature and high solar ultraviolet radiation, Trans. Am. Fish.
Soc., 2004, 133, 718-726.
344 Olson MH, Colip MR, Gerlach JS, Mitchell DL, Quantifying ultraviolet radiation mortality
risk in bluegill larvae: effects of nest location, Ecol. Appl., 2006, 16, 328-338.
345 Epel D, Using cell and developmental biology to enhance embryo survival in aquaculture,
Aquacult. Int., 2005, 13, 19-28.
346 Przeslawski R, Davis AR, Benkendorff K, Synergistic effects associated with climate
change and the development of rocky shore molluscs, Glob. Change Biol., 2005, 11, 515522.
347 Przeslawski R, Combined effects of solar radiation and desiccation on the mortality and
development of encapsulated embryos of rocky shore gastropods, Mar. Ecol. Prog. Ser.,
2005, 298, 169-177.
348 Helbling EW, Menchi CF, Villafane VE, Bioaccumulation and role of UV-absorbing
compounds in two marine crustacean species from Patagonia, Argentina, Photochem.
Photobiol. Sci., 2002, 1, 820-825.
349 Ferreyra GA, Mostajir B, Schloss IR, Chatila K, Ferrario ME, Sargian P, Roy S,
Prod'homme J, Demers S, Ultraviolet-B radiation effects on the structure and function of
lower trophic levels of the marine planktonic food web, Photochem. Photobiol., 2006, 82,
887-897.
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Chapter 5. Interactive effects of solar UV radiation and climate
change on biogeochemical cycling
R. G. Zeppa, D. J. Erickson IIIb, N. D. Paulc and B. Sulzbergerd
a
U.S. Environmental Protection Agency. National Exposure Research Laboratory, 960 College
Station Road, Athens, Georgia 30605-2700 USA
b
Computational Earth Sciences Group, Computer Science and Mathematics Division, Oak
Ridge National Laboratory, MS 6016 Oak Ridge TN 37831-6016 USA;
c Department of Biological Sciences, Lancaster Environment Centre, Lancaster University,
Lancaster LA1 4YQ, UK;
d
Swiss Federal Institution of Aquatic Science and Technology (Eawag), Überlandstrasse 133,
CH-8600 Dübendorf, Switzerland.
Summary
This report assesses research on the interactions of UV radiation (280-400 nm) and global
climate change with global biogeochemical cycles at the Earth’s surface. The effects of UV-B
(280-315 nm), which are dependent on the stratospheric ozone layer, on biogeochemical cycles
are often linked to concurrent exposure to UV-A radiation (315-400 nm), which is influenced by
global climate change. These interactions involving UV radiation (the combination of UV-B and
UV-A) are central to the prediction and evaluation of future Earth environmental conditions.
There is increasing evidence that elevated UV-B radiation has significant effects on the
terrestrial biosphere with implications for the cycling of carbon, nitrogen and other elements.
The cycling of carbon and inorganic nutrients such as nitrogen can be affected by UV-Bmediated changes in communities of soil organisms, probably due to the effects of UV-B
radiation on plant root exudation and/or the chemistry of dead plant material falling to the soil. In
arid environments direct photodegradation can play a major role in the decay of plant litter, and
UV-B radiation is responsible for a significant part of this photodegradation. UV-B radiation
strongly influences aquatic carbon, nitrogen, sulfur and metals cycling that affect a wide range of
life processes. UV-B radiation changes the biological availability of dissolved organic matter to
microorganisms, and accelerates its transformation into dissolved inorganic carbon and nitrogen,
including carbon dioxide and ammonium. The coloured part of dissolved organic matter
(CDOM) controls the penetration of UV radiation into water bodies, but CDOM is also
photodegraded by solar UV radiation. Changes in CDOM influence the penetration of UV
radiation into water bodies with major consequences for aquatic biogeochemical processes.
Changes in aquatic primary productivity and decomposition due to climate-related changes in
circulation and nutrient supply occur concurrently with exposure to increased UV-B radiation,
and have synergistic effects on the penetration of light into aquatic ecosystems. Future changes
in climate will enhance stratification of lakes and the ocean, which will intensify
photodegradation of CDOM by UV radiation. The resultant increase in the transparency of
water bodies may increase UV-B effects on aquatic biogeochemistry in the surface layer.
Changing solar UV radiation and climate also interact to influence exchanges of trace gases,
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135
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
such as halocarbons (e.g., methyl bromide) which influence ozone depletion, and sulfur gases
(e.g., dimethylsulfide) that oxidize to produce sulfate aerosols that cool the marine atmosphere.
UV radiation affects the biological availability of iron, copper and other trace metals in aquatic
environments thus potentially affecting metal toxicity and the growth of phytoplankton and other
microorganisms that are involved in carbon and nitrogen cycling. Future changes in ecosystem
distribution due to alterations in the physical and chemical climate interact with ozonemodulated changes in UV-B radiation. These interactions between the effects of climate change
and UV-B radiation on biogeochemical cycles in terrestrial and aquatic systems may partially
offset the beneficial effects of an ozone recovery.
Introduction
Global biogeochemistry plays a critical role in controlling life processes, climate and their
interactions, including effects on atmospheric greenhouse gas concentrations. Changes in
stratospheric ozone and hence in solar UV-B radiation (280-315nm) have many different effects
on global biogeochemistry. Longer wavelength UV-A radiation (315- 400 nm) is little affected
by ozone depletion, but can be affected by global climate change. UV radiation (280-400 nm),
including both UV-B and UV-A, modifies carbon cycling through changes in its capture
(photosynthesis), storage in biomass and non-living organic matter, and release (respiration and
photochemical decomposition). The effects of UV radiation on carbon cycling are linked to
effects on the cycling of metals and mineral nutrients such as nitrogen. Carbon and nutrient
cycles are also substantially affected by other components of climate change, including warming,
elevated CO2 and altered patterns of precipitation, and there are also significant interactions
between these factors and changes in UV radiation. Interactions between changing solar UV
radiation and climate change occur through the effects of UV radiation on emissions of trace
gases, such as carbon monoxide, carbonyl sulfide, methane, methyl bromide and dimethylsulfide.
Climate change can alter the exposure of ecosystems to UV-B radiation by influencing the Earth
system processes that affect ozone depletion (Chapter 1) as well as changes in aquatic UVabsorbing substances such as colored dissolved organic matter (CDOM). Biological responses
of organisms to changing UV radiation and interactions with climate change are considered in
detailed in Chapers 3 and 4. This chapter examines the responses of global biogeochemistry to
interactions between stratospheric ozone depletion and co-occurring environmental changes in
climate, land use, and atmospheric CO2 (Figure 5-1). The primary focus is on new information
obtained since our 2002 report1 although in some instances reference is also made to earlier key
publications.
Carbon Cycling
There is a consensus that terrestrial ecosystems are currently net sinks for carbon, i.e. that the
uptake of CO2 exceeds its release. The net accumulation of carbon by terrestrial ecosystems has
been calculated to be around 0.7 petagrams (Pg) (1 Pg equals 1015 g, or 109 metric tons) carbon
per year for the 1990s, although estimates vary widely.2 This is substantially smaller than
current estimates of oceanic CO2 uptake (around 2.4 Pg carbon per year for the 1990s). However,
the carbon balance of terrestrial systems is profoundly influenced by human activities such as
land-use change, which may result in CO2 emissions as great as 2.2 Pg carbon per year.2, 3
The exchange of carbon dioxide between the atmosphere and ecosystems is a balance between
CO2 uptake by photosynthesis, its storage in biomass and non-living organic matter, and its
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
release through respiration, photodegradation, and burning. Changes in solar UV radiation have
been shown to influence many of these processes.
Figure 5-1. Conceptual model illustrating the potential effects of enhanced UV radiation and climate change on
biogeochemical cycles : OM organic matter; DOM dissolved organic matter; CDOM colored (chromophoric)
DOM; CO2 carbon dioxide; CO carbon monoxide; DMS dimethylsulfide; OCS carbonyl sulfide; VOCs volatile
organic hydrocarbons; CH3Br methyl bromide.
Carbon Fixation
The balance of evidence continues to suggest that changes in UV-B radiation resulting from
ozone depletion will have little effect on carbon fixation and growth in most terrestrial plants
(see Chapter 3) and hence on large-scale carbon capture and storage by terrestrial vegetation.
However, certain plant species or communities may be vulnerable to increased UV-B radiation
and this may have significant ecological impacts in specific systems (see Chapter 3).
Whereas in terrestrial ecosystems changes in solar UV radiation influence carbon fixation
directly through effects on plants, in aquatic systems, the primary producers are affected both
directly and indirectly by solar UV radiation. The indirect effects are caused by changes in
exposure to UV radiation due to variations in the concentration of CDOM and, to a lesser extent,
suspended particles. CDOM is the main UV-absorbing constituent in aquatic systems and
controls the penetration of UV radiation into water bodies. Organic matter produced on land and
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137
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
transported by rivers is an important source of CDOM to the coastal oceans.4-7 However,
CDOM undergoes UV-induced transformations, resulting in loss of colour and UV absorbance
(referred to as photobleaching).8-10 Photobleaching of CDOM increases the penetration depth of
UV radiation into water bodies and enhances the exposure of aquatic ecosystems to UV radiation.
This increased exposure enhances the negative, direct effects of UV on carbon fixation in aquatic
systems (see Chapter 4). The effects of CDOM on UV penetration are determined by its
chemical composition11, and the optical properties and the mechanisms of photobleaching of
CDOM are being intensively investigated.8, 10-18
Carbon Storage and Release
The storage of organic carbon in terrestrial ecosystems is estimated to be approximately 20003000 Pg, with about three times as much stored in soil as in vegetation.19-21 Approximately
38,500 Pg of inorganic carbon are stored in the ocean and sediments, and approximately 750 Pg
are stored as living and non-living organic carbon. The effects of changes in solar UV-B on
long-term carbon storage remain unclear. However, UV-B influences short-term carbon turnover from plant litter (dead plant material) in terrestrial systems, and dissolved organic matter
(DOM) and particulate organic matter (POM) in aquatic systems. The release of carbon can
result not only from respiration but also from photodegradation of organic matter or
phototransformation into forms more readily available to microbes. The photodegradation of
wood is also discussed in Chapter 7.
Global respiration from terrestrial vegetation and from soils are both of the order of 50-60 Pg of
carbon per year.3, 22 The release of carbon differs among sources such as living plant material
and dead organic matter and is highly dependent on factors such as temperature. Altered UV-B
will influence carbon release from terrestrial ecosystems through changes in the efflux of CO2
and/or CH4.23, 24 However, research over the past four years reinforces the conclusion of the
previous UNEP report1 that the effects of changing UV on carbon release from terrestrial
ecosystems are complex and are likely to vary between species and ecosystems.
Carbon release from soils is a function of the activities of soil fauna and micro-organisms. Soil
organisms may be vulnerable to UV-B damage (e.g.,25) but are rarely exposed to solar radiation
in nature. Even so, plant responses to changing UV-B may indirectly affect soil organisms.
Attenuation of solar UV-B modifies the communities of fungi and microfauna in the surface
layer of Sphagnum wetland communities.26, 27 These changes in soil communities are probably
related to UV-induced changes in the quantity or chemistry of dead plant material or root
exudates entering the soil, for example attenuation of solar UV-B reduced the leaching of DOC
and P from Sphagnum moss27 (Figure 5-2a). UV-B induced changes in leaf litter chemistry may
also influence soil fauna, for example earthworms, although responses appear to be rather subtle
and species-dependent.28 Recent studies in the Antarctic29, temperate grassland30, and arctic
heath31 have also shown changes in soil microbial community structure in response to UV-B
manipulations, rather than the changes in total microbial biomass that were evident in some
previous studies.32
The effects of changed solar UV on the chemistry of leaf litter have been studied in a range of
species. Changes in litter chemistry can occur in two ways: by the effects of UV exposure on
decomposing litter (which are called direct effects), or the effects of UV on the chemistry of
living tissues before litter-fall (so-called indirect effects). Direct effects occur when dead plant
material decomposes on or above the soil surface, when directly exposed to solar UV. Recent
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
-1
)
35
DOC concentration (mg l
data33 highlights that direct photodegradation
can be the dominant process in the
decomposition of plant litter in ecosystems
with high sunlight and limited rainfall, and
that UV-B may account for 50% of such
photodegradation (Figure 5-3a). In these
dryland ecosystems changes in solar UV
resulting either from variation in ozone or
elements of climate change such as cloud
cover may have substantial effects of carbon
cycling. In other terrestrial ecosystems the
effects of UV on litter decomposition are more
complex. Exclusion of ambient solar UV-B
during decomposition accelerated the break
down of litter in some species (Figure 5-3b)
but had only marginal effects in others (e.g.,
barley:34). Similarly, exclusion of ambient
UV-B may increase litter colonization by
fungi in some systems35, but not others.36
Overall, the direct effects of changing UV-B
on litter decomposition appear to depend on
species-specific differences in litter chemistry,
and on absolute differences in UV dose and
weather conditions between different sites.
A
30
Full sun
25
UV-B only attenuated
20
15
10
5
0
0-5 mm
5-10 mm
Sample depth
B
Figure 5-2. Figure 2. UV radiation influences the
The indirect effects of changing UV on litter
production of dissolved organic carbon in both terrestrial
and aquatic ecosystems. In terrestrial ecosystems, recent
chemistry and consequent changes in
evidence shows that UV-B exposure significantly
decomposition are species specific. The
increases the release of DOC from Sphagnum moss, the
previous observation that elevated UV-B
dominant plant in global peatland ecosystems (A,
during plant growth and development
modified from Robson et al.26). This effect of UV-B
accelerated the decomposition of oak leaf
was not confined to the surface layers exposed to UV-B,
but occurs also in deeper layers (5-10 mm below the
litter37 was shown recently to be associated
surface) where no UV-B penetrates. In aquatic systems,
with reductions in the extractability of some
carbohydrate fractions in litter produced under UV-B can result in the release of DOC from particulate
organic carbon (POM). For example simulated solar
elevated UV-B (Figure 5-3c), which
radiation results in the loss of suspended POM and the
stimulated colonization by some fungal
production of DOC (B, from Mayer et al.37: data are
38
means of triplicate experiments and the error bars are ±
decomposers. In barley UV-B exposure
during plant growth and development caused 1 standard deviation). Other studies using light filters
showed that the POC to DOC conversions were mainly
significant changes in litter chemistry,
induced by UV radiation (Figure 2b, Reprinted with
including nitrogen, and this was associated
permission from Mayer et al.37, Figure 1, p. 1066,
with a significant reduction in the loss of dry
Copyright 2006 by the American Society for Limnology
and Oceanography, Inc.). The continual resuspension
weight and nitrogen from litter during
34
and exposure of deposited particulates to sunlight in
decomposition. In the herbaceous plant
shallow parts of systems such as the Missisippi Delta
Gunnera magellanica there were persistent
region provides an opportunity for cumulative
differences in the fungal community
photodissolution over time.
colonizing litter produced under different UV
environments35, but this was not related to significant changes in litter chemistry or
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139
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
decomposition. In two grasses UV-B exposure during plant growth and development had no
effect on litter quality or decomposition.39
Increased UV-B significantly modifies the chemistry of secondary metabolites produced by and
released from plants (also see Chapter 3). The majority of studies of UV effects on plant
chemistry have dealt with leaves, but increased UV may also induce accumulation of certain
carbohydrates and UV-absorbing phenolics in the bark of birch saplings.40 The chemistry of
tissues not directly exposed to UV can also be affected, as in the roots of lupin (Lupinus luteus)
plants grown under increased UV.41 As with many UV responses, this effect on root chemistry
appears to be species specific.42, 43 Although these studies of UV effects on plant chemistry have
not explicitly considered biogeochemical cycles, there is increasing evidence that plant-derived
chemicals, especially phenolic compounds, have major consequences for soil processes.44-46 It is
notable that many of the plant-derived phenolic compounds considered to play vital roles in
affecting soil processes have also been shown to be influenced by UV exposure.40, 45, 47-49 Since
UV-B effects on such phenolic compounds are specific both to plant species and individual
compounds, the observed variation in effects on soil processes might be expected.
A
0.3
0.2
0.1
0
Full sun
UV-B only All wavelengths
attenuated
attenuated
25
B
Annual fractional mass loss
0.4
Decomposition (% mass loss)
Annual fractional mass loss
Since existing studies of the effects of increased UV-B on decomposition or soil processes have
20
15
10
5
0
Full sun
UVB only
attenuated
0.22
C
0.2
0.18
0.16
0.14
0.12
0.1
215
220
225
230
235
240
Carbohydrate extracted (mg g-1)
Figure 5-3. The effects of UV-B radiation of the decomposition of dead plant material in terrestrial ecosystems vary
with factors such as climate and plant species. In high, light, arid ecosystems the break-down of dead plant material
(“litter”) may be largely due to photodegradation, and UV-B may accelerate this process. This is clear from a study
of decomposition in the Patagonian steppe (A, modified from Austin and Vivanco33) where litter was decomposed
either under full sunlight, sunlight in which only UV-B had been attenuated, or sunlight with all wavelengths
attenuated by 90%. (Data are presented as the annual fractional mass loss obtained from the slope of the regression
between ln(organic matter remaining/initial organic matter) against time. Error bars are ± standard error of the
mean). In ecosystems less limited by water, the effects of UV-B on litter break-down are more variable, but there
are many examples where UV-B suppresses decomposition, as in the herbaceous plant Gunnera magellanica grown
in Tierra del Fuego (B, modified from Pancotto et al.35: data are means ± standard error of the mean). UV-B
exposure during growth may also influence subsequent decomposition of leaf litter, as in oak (C, modified from
McLeod et al.39) where the annual fractional mass loss is significantly increased in litter produced under elevated
UV-B, and this is associated with reductions in the amount of carbohydrate released from this litter. (Data are means
± standard errors).
largely focused on individual species, the net effects of changed UV-B acting across areas of
vegetation remain unclear. A recent modeling approach to the effects of climate change on
decomposition suggests that the principal effect of elevated UV-B will be to increase litter
accumulation and so contribute to carbon sequestration.50 However, the conclusion of the
previous assessment1 that any such effect of UV on terrestrial carbon budgets is likely to be local
and determined by species-specific responses in both plants and decomposers has not been
changed by recent research.
Carbon dioxide (CO2) in aquatic systems is produced via microbial respiration, UV-induced
mineralization of DOM into inorganic carbon, and/or shifts in the carbonate equilibrium.1
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
Whether photochemical mineralization or microbial respiration is the predominant process
largely depends on the source and thus the chemical composition of DOM. A number of studies
have shown that algal-derived DOM is more biodegradable and less photoreactive than terrestrial
DOM.5, 51-54 The extent of DOM photomineralization increases with decreasing pH55 and also
depends on the precipitation history.56 Furthermore, photomineralization is catalyzed by iron10
(see also the section “Metal Cycling”).
Photochemical and microbial decomposition of DOM may interact since DOM is a key nutrient
and energy source for consumers, including heterotrophic bacteria and metazooplankton.
However, not all chemical forms of DOM are available to these organisms, and UV-induced
transformations of DOM can alter its bioavailability.1 UV-induced transformations of DOM
may increase bioavailability of biorecalcitrant DOM and vice versa.52, 57 The UV-induced
increase in DOM bioavailability may enhance microbial respiration of DOM58 or increase
microbial biomass through the microbial loop.59
Transfers of carbon and nutrients between the water column and bottom sediments of
freshwaters and the ocean are mediated by particles. Solar UV can affect the dynamics of such
transfers by photooxidation of particulate organic carbon (POC).1 UV also can induce the
conversion of POC to dissolved organic carbon (DOC)60(Figure 5-2b).
Nutrient Cycling
Nitrogen and phosphorus can limit productivity in terrestrial and aquatic ecosystems. UV
radiation can affect nitrogen cycling in several ways, including changes in the decomposition of
N-containing organic matter and through effects on nitrogen fixation. In addition, in aquatic
environments UV interactions with inorganic nitrogen species such as nitrate and nitrite are an
important source of reactive oxygen species, including the highly reactive hydroxyl radical.
Biologically labile nitrogen compounds such as nitrate, ammonium, and amino acids are rapidly
recycled by the biota in aquatic systems, while N-containing substances that have structural
features that inhibit assimilation, accumulate in the water column. Interactions of UV radiation
and dissolved organic nitrogen (DON) provide a pathway for the conversion of persistent DON
to compounds that are more easily assimilated by aquatic microorganisms, such as ammonium.1
Ammonium photoproduction, i.e. “photoammonification”, which is affected by solar UV-B
radiation,61 occurs in both freshwater lakes62 and in coastal regions such as the Baltic Sea61,
where it can periodically be the largest source of new bioavailable nitrogen in the Baltic Sea.61
Solar UV can affect phosphorus cycling by photodegradation of enzymes such as alkaline
phosphatase (APase) or release of APase sorbed to humic substances.1 Additional evidence
obtained in Canadian lakes confirmed that exposure to solar UV reduced APase activity.63
Sorption of APase to clay particles protected the enzyme from UV-induced photodegradation,
although enzymatic activity was reduced by sorption.64
Nitrogen inputs into soil originate from a number of sources, including atmospheric deposition,
decomposition, biological nitrogen fixation and, in agricultural ecosystems, fertilizers.65
Variation in responses of litter decomposition to changing UV-B affect the release of nitrogen
from decaying plant litter.34, 35, 39 The effects of changing UV on plant-derived phenolic
compounds in soils may be especially important for nitrogen transformation processes.44-46
Biological nitrogen fixation by free living cyanobacteria can be reduced by increased UV-B
radiation1, 66 (see Chapters 3 and 4). Increased UV-B may also inhibit nitrogen fixation by
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141
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
cyanobacteria within lichens1 but recent data suggest that this does not occur in all species.67 In
recent studies of tropical legumes, elevated UV had no significant effects on symbiotic nitrogen
fixation41-43, in contrast to a number of previous studies.1
In terrestrial plants the uptake of nutrients such as phosphate and some forms of nitrogen is often
achieved through the mycorrhizal symbiosis between plant roots and fungi. There is evidence
that changing UV-B can influence root colonization by mycorrhizal fungi1, but recent evidence
shows that this response varies between sites, even within a single system31, as well as between
species.30, 68 We are unaware of any studies that have explicitly measured mycorrhizal function
rather than colonization.
Metal Cycling
Many trace metals are essential micronutrients for aquatic organisms69-72, but most of them can
be toxic to terrestrial and aquatic organisms, depending on their concentration and chemical
speciation.73-76 Solar UV radiation has significant effects on the chemical speciation of trace
metals, for example, iron, manganese, copper, chromium, and mercury (Figure 5-4).
Iron
Iron is an essential micronutrient
for phytoplankton and has been
Air
shown to co-limit phytoplankton
growth in several marine
Water
Cu(II)
Fe(III)
environments.77-79 The role of iron
Re-oxidation
Dissolved
Re-oxidation
supply in stimulating phytoand formation
and formation
Organic
Matter
plankton blooms in high-nitrate,
of ROS, e.g.
of ROS, e.g.
(DOM)
.OH
.OH
low-chlorophyll oceanic waters has
Cu(I)
Fe(II)
been demonstrated80, 81 and its
DOM transformed
effect on carbon sequestration is
+ ROS
being intensively investigated.82-84
Bacterio- and
Fe(III) is the most common form
Phytoplankton
of iron in sunlit aquatic systems,
but Fe(II) is the key form that
Organic and inorganic pollutants,
determines the availability of iron
e.g., Hg0aq
85
for uptake by organisms. In oxic,
sunlit surface waters the maintenance of low Fe(II) concentrations is Figure 5-4. UV radiation is a key factor in the chemistry of iron and
a result of the UV-induced reduct- copper in aquatic systems, including its interactions with dissolved
organic matter (DOM) and microorganisms. This schematic represents
ion of Fe(III), both dissolved and
the UV-induced redox cycling of iron and copper, and the concomitant
colloidal,86-89 and Fe(II) oxidatphototransformation of DOM and production of reactive oxygen
species (ROS), for example the highly reactive hydroxyl radical (·OH),
ion.90-93 In surface waters of the
Southern Ocean the photoreduction that can adversely affect bacterio- and phytoplankton and react with
organic and inorganic pollutants, for example dissolved gaseous
was primarily caused by UV-A
mercury, Hg0aq.
radiation, although ozone depletion
was estimated to increase the UV-B contribution to this photoreduction from 3.5 to 6.2%.89
UV-induced iron chemistry will interact with large scale inputs of iron, such as dust deposition,
that are influenced by climate change.94 Dust deposition is the major source of iron in some
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The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
remote regions of the ocean and UV exposure can affect the bioavailability of this iron.
Enhanced iron bioavailability could affect both phytoplankton abundance and community
structure particularly in these regions. Indeed, satellite observations of productivity in remote
regions of the Southern Hemisphere correlate with dust deposition.95 The regions in the
Southern Hemisphere where oceanic productivity is strongly correlated with dust deposition
(Figure 5-5) are those in which future changes in total ozone, and thus UV-B exposure, are likely
to be most dynamic (see Chapter 1). Thus future changes in total ozone over this region could
interact with dust deposition to alter the spatial distribution of primary and secondary pelagic
production and may place additional stress on already depleted fish and mammal populations
(also see Chapter 4).
Copper
The bioavailability and thus
toxicity of copper depends on its
chemical speciation. It is likely
that, by analogy to iron, reduced
copper, Cu(I), is an important
species with regard to the bioavailability and hence toxicity of
copper. As with iron, reduction
of Cu(II) to Cu(I) in oxic aquatic
systems occurs to a large extent
via UV-induced photochemical
reactions of Cu(II) complexed by
strong organic ligands.96, 97 In the
case of coastal estuaries, these
strong Cu ligands are
components of humic substances
that can be photodegraded.
Although solar UV radiation was
primarily responsible for the
Figure 5-5. The productivity of marine ecosystems is highly correlated
with inputs of dust derived from terrestrial ecosystems, which may be
photolysis of these strong Cu
changing due to climate change. This map shows correlation coefficient
ligands, visible radiation also
observed between dust deposition and marine productivity as estimated
98
was involved. Up to 25% of
by satellite estimates of chlorophyll.95 The time series of dust deposition
total dissolved copper detected in is estimated from a global transport model that has been verified against
marine surface waters is Cu(I)
observations. The high correlations (>0.80) indicate that the input of
atmospheric Fe in dust elicits a very quick and discernable response in
which is stabilized by inorganic
some
regions of the ocean. The strong covariance of dust input and
and organic ligands such as
biological activity is occurring in regions where productivity is Fe limited
chloride and phytoplanktonand the magnitude of the dust flux is quite small as this is occurring far
derived organosulfur comfrom strong dust sources. These regions continue to experienced the
pounds.75, 76 During its longgreatest changes in stratospheric ozone concentration and, hence, in UVB radiation (see Chapter 1).
range transport in atmospheric
waters, copper undergoes UVinduced redox cycling so that a large fraction of total copper in rainwater is Cu(I).97 It was
hypothesized that part of the strong Cu-complexing ligands found to be present in these
rainwater samples were Cu(I)-complexing ligands that retard Cu(I) oxidation.
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
Mercury
UV-induced redox processes also largely determine the bioavailability and thus toxicity of
mercury. Mercury is a globally dispersed toxic pollutant that can be transported far from its
emission sources.99 Divalent mercury, Hg(II), can be methylated and bioaccumulated in the
aquatic and terrestrial food chain100 and methylmercury can adversely impact reproduction of
wild fishes.74 Reduction of Hg(II)101, 102 and oxidation of dissolved gaseous mercury (Hg0aq)103105
are both induced by UV radiation. Especially critical is the UV-induced oxidation of Hg0aq
since this process increases the pool of methylmercury. The photooxidation of Hg0aq is chiefly
mediated by UV radiation in natural brackish waters, and ·OH may be partly responsible for
Hg0aq oxidation in these systems.103, 104 The photoproduction of methylmercury was dependent
on DOM concentration and type in freshwater samples.105 For example, water from lakes with
logged watersheds generated methylmercury when exposed to sunlight whereas water from lakes
with low levels of logging in the undisturbed watershed did not. Hence solar UV radiation can
have significant and complex impacts on mercury volatilization, solubilization, and
methylation.106
UV-Enhanced Oxidative Activity of Aquatic Systems
Reactive oxygen species (ROS), important in the processing of natural and anthropogenic
compounds, are produced by UV-induced photoreactions of inorganic nitrogen, organic matter
and/or metals.10, 18, 58, 107 The most reactive ROS, ·OH, damages cellular components such as
proteins, lipids, and nucleic acids108 and inhibits bacterial carbon uptake.57 UV-induced
reactions involving iron or copper and hydrogen peroxide (Figure 5-4) can be an important
source of ·OH in iron-rich, sunlit surface waters18, 109 and can enhance the oxidative activity of
aquatic systems.
The hydroxyl radical and other ROS also react with natural compounds and man-made
chemicals such as pharmaceuticals110-112, certain herbicides113 and commercial dyes114, as well as
with naturally-occurring organic matter such as lignin115 and DOM.16-18, 58, 116-118 The oxidation
of contaminants by ROS, however, is not always beneficial but may increase the toxicity of
contaminants as in the case of mercury (see above subsection “ Mercury”).
Interactions Between UV Radiation and Other Co-Occurring Environmental
Changes
Changes in the surface flux of UV will interact with co-occurring changes in climate, land use
and atmospheric carbon dioxide all of which have the potential to influence the biogeochemical
cycling in terrestrial and aquatic ecosystems. In the future, changes in temperature and rainfall
patterns119, cloud cover, forest fires120, aquatic biological production, deforested land surfaces
and aquatic circulation will interact with themselves and with changing surface UV radiation.
These interactions will affect biogeochemical cycles, including carbon cycling, movement of
CDOM from land to water, stratification of aquatic ecosystems, and trace gas exchange between
the biosphere and atmosphere.
Interactions Involving Carbon Cycling
The effects of environmental change on carbon cycling may interact with those of solar UV
radiation via changes in carbon fixation, storage and release, as discussed above. The greatest
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
source of uncertainty in global carbon budgets of terrestrial ecosystems appears to be the tropical
regions, where the balance between the high potential carbon fixation of tropical forests is
balanced by substantial carbon release due to deforestation and other changes in land use.2, 20
Since the effects of stratospheric ozone depletion on the UV climate of the tropics are minimal121,
122
, these uncertainties may be of little importance in assessing ecosystem responses to
interactions between ozone depletion and climate change in this region. However, it is notable
that several reports indicate that the main driver of increased carbon fixation in tropical forests is
an increase in total solar radiation driven by changing patterns of clouds.123, 124 The ecological
effects of increased exposure to UV due to decreased clouds are unclear since, unlike
stratospheric ozone depletion, variation in cloud cover will cause concurrent changes in both UV
and photosynthetic radiation. While many tropical plants are considered tolerant of UV,
significant UV responses have recently been reported in a range of tropical plants.42, 43, 125 Thus,
there is potential for a UV contribution to ecosystem responses to altered cloud cover even in the
tropics, although this is likely to be species-specific. In addition, changes in aerosols, for
example from combustion, affect UV-B radiation more than photosynthetic radiation122 with
unknown ecological consequences.
There is a clearer understanding of large-scale carbon budgets in temperate and high latitude
regions, especially for the Northern Hemisphere. Analysis of atmospheric CO2 trends in the
Northern Hemisphere since 1994 provides evidence that warming may be increasing CO2
fixation in spring, but this effect is offset by reductions in photosynthesis due to increasing
summer drought.126 While remote imaging shows greening at high latitudes over the last two
decades127, 128 and increases in the length of the growing season, such changes do not occur in all
high-latitude ecosystems perhaps due to interactions with water supply.129, 130 Carbon
sequestration in high latitude forests due to warming may also be offset by increased respiration
from burned forests.131 Thus, while effects of changes in the growing season of carbon budgets
may interact with changes in UV exposure,1 these interactions remain hard to predict. Especially
at high latitudes future climate changes are also likely to contribute strongly to changes in
ecosystem distribution132 (Figure 5-6), and since UV effects on both carbon fixation and release
are specific to particular plants or ecosystems (see above and Chapter 3), this may significantly
alter regional responses to changing UV climates. Increased temperatures generally increase
decomposition rates, but the magnitude of temperature dependence varies substantially between
different types of organic matter. While there is clearly a considerable variation in temperature
dependence, carbon release from soils, reflecting microbial processes, appears to be more
sensitive than that from living plants.22 There is recent evidence for both soil organic matter133136
and leaf litters137 that the temperature sensitivity of decomposition increases with decreasing
litter quality. It is also notable that increased temperature may particularly favour those soil
microbes best able to decompose recalcitrant organic material.138 These effects of warming
might interact with those caused by UV-B (see above), and this may be particularly pertinent for
“high latitude” ecosystems where future changes are likely to be the most dynamic in the Earth
system (see Chapter 1). Carbon release may also be influenced by many co-occurring
environmental changes. Recent research shows that the effects of elevated CO2 on carbon
release from soil are complex.139-142 The mechanisms involved include increased root growth143,
144
, altered litter quality145, and changes in the soil microbial community146-149, and so may
interact with comparable responses caused by changing UV-B (see above). Interactions between
UV and drought may occur through similar mechanisms, since drought substantially inhibits soil
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
Figure 5-6. Climate change is expected to result in substantial shifts in the distribution of major ecosystems.
Present and projected future geographic distributions of vegetation types north of 55ºN are illustrated here: A,
Present-day potential natural vegetation; B, The potential vegetation driven by the mean climate of the decade 2090–
2100 simulated by the HADCM2-SUL coupled model, using the IS92a scenario. The future vegetation types were
predicted from climatology using a set of plant functional types embedded in the biogeochemistry-biogeography
model BIOME4.132
respiration150-152 and even mild water deficits can reduce the carbon flow from roots to the soil
microbial community153 and increase the abundance of phenolic degrading bacteria.154
Effects of Climate Change on Carbon Inputs from Terrestrial to Aquatic Systems and
Implications for Aquatic Ecosystems
Deforestation and changes in land use have substantial effects on carbon losses from soils via
leaching or run-off into water bodies where it is an important source of CDOM and DOM. Shifts
in soil moisture content and related changes in oxygen content affect the microbial production of
soil humic substances and thus can alter inputs of this important source of CDOM in freshwaters.
UV-induced transformation of CDOM differs between aquatic and terrestrially derived DOM
due to differences in composition, particularly phenolic content. Given the well-defined effects
of elevated UV-B on the phenolic chemistry of litter and root exudates, it is possible that the
composition of DOM leaching from or running-off terrestrial systems could be altered, with
consequent effects in aquatic systems. That mechanism remains unexplored, but there are many
ways by which climate change may enhance UV-induced CDOM bleaching. Warming affects
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
the composition of CDOM produced by microbial decomposition of seagrass, rendering CDOM
more susceptible to UV-induced bleaching.155
Climate-related changes in continental hydrology can alter the production and transport of UVabsorbing substances from land to the ocean. These changes involve alterations in discharge
rates from rivers and the chemical content of the water transported and mixed into the ocean.
Important factors influencing these changes include climate-related changes in the frequency and
intensity of precipitation, extent of land use change, dams and anthropogenic and natural
chemical inputs to the river basins. For example, in Arctic systems boreal wetlands are the major
source of DOM in streams, rivers, lakes and the coastal ocean. Changes in temperature,
precipitation and CO2 affect the concentration and discharge of DOM from terrestrial
ecosystems.156, 157 UV-B radiation induces the degradation of CDOM in aquatic system and is
especially significant at high latitudes.1, 55 Degradation of terrestrially-derived DOM in the
Arctic Ocean limits its movement into the deep ocean.6 The effect of past climate changes on
aquatic-terrestrial interactions also has been demonstrated.158 Paleoecological techniques were
used to demonstrate that periods of deforestation over the past 10,000 years were associated with
rapid declines in the inputs of UV-absorbing CDOM, which in turn caused up to a ten-fold
reduction in algal biomass. Climate-related changes in ice and snow cover will result in a greater
area of the high latitude biosphere being exposed directly to UV-B (also see Figure 5-6).
Climate Change and Mixing in Aquatic Systems
UV-induced bleaching of CDOM in the surface layers of aquatic systems is intensified by
stratification.159 Climate models predict that global warming will result in reduced vertical
mixing and increased stratification in the upper ocean.160-162 Thus, the effects of elevated UV-B
may interact with the effects of climate change on stratification, and the quantity and chemical
composition of inputs from terrestrial systems. Observations in Europe during the 2003 heatwave demonstrated that warming can enhance lake stratification.163 Climate-related changes in
atmospheric circulation and related changes in vertical mixing dynamics in the ocean and
freshwaters can also affect UV exposure of aquatic organisms. For example, in the case of
phytoplankton in the ocean, increased variability in the deep chlorophyll maximum164 could
result in more variable UV exposure, with possible consequences for primary production.
Moreover, UV-B damage to microorganisms is strongly affected by changes in climate-induced
mixing of the upper layers of aquatic environments and thus will affect carbon and nutrient
cycling and the production and consumption of trace gases.
Satellite imagery has provided a first view of the global distribution of CDOM that controls the
penetration of UV-B into the sea.165 Photoreactions of CDOM and changes in ocean circulation
patterns related to El Niño events strongly influence CDOM distributions. Remote sensing
techniques also facilitate the global high resolution analysis of aquatic UV impacts on marine
biogeochemical cycles. Relationships have been developed between remotely sensed ocean
colour and UV attenuation in coastal regions of the ocean. The relationships were applied to
determine changes in UV penetration into the Mid-Atlantic and South-Atlantic Bight near the
eastern coast of the U.S.A.166 These recent studies highlight the possibility of monitoring from
space the interactions of climate-related mixing trends with the chemical compounds that are
produced from UV interactions.
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
Interactions between Ozone Depletion and Climate Change Mediated Via Changes in
Trace Gases Abundance and Chemistry
The budgets of trace gases such as methane, halocarbons, nitrogen oxides (NOx) and carbon
monoxide may be influenced by changing solar UV radiation, and through their effects on
atmospheric chemistry some may also influence ozone (Chapter 6). Since climate change may
influence the budgets of these trace gases, they are a key link between ozone depletion and other
elements of environment change. There is increasing understanding of the responses of specific
trace gases to climate change. As discussed in our previous report1, at high latitudes ice and snow
can play a key role in the budgets of many trace gases. Climate change is having major effects
on ice and snow cover, and hence on the budgets of trace gases such as bromoform, NOx,
alkenes, formaldehyde and CO.1 These reactions have consequences for concentrations of
tropospheric ozone at high latitudes (see Chapters 1 and 6).
New, high-resolution models of oceanic ecosystems have been developed which provide
estimates of phytoplankton and trace gas distributions with high spatial resolution globally.
Figure 5-7 illustrates the use of such Earth system models to estimate global distributions of
surface ocean DMS based on a global ocean biogeochemistry physical circulation model. The
ability to use high performance computing that enables future biogeochemical states to be
estimated will allow assessments of UV stress on ocean ecosystems over the next 100 years.167
The use of this type of global Earth system models can provide future estimates of O3 and UV
levels that contribute to trace gas exchange between the surface ocean and the atmosphere.
Methane, carbon monoxide and volatile organic compounds
Enhanced UV-B can reduce emissions of methane from peatland ecosystems and paddy fields,
and this is partly explained by morphological changes in plant structure.23 Emissions of methane
from wetland ecosystems are highly dependent on the plant species present23, 24, 168 and so could
be affected by changes in ecosystem distribution (Figure 5-6). Recent research has demonstrated
that plants themselves can be methane sources, even under aerobic conditions169, although the
contribution of such emissions to global methane budgets remains unclear. Changes in light and
temperature affect plant production of methane but the role of UV-B is unknown. Thus, changes
in UV might alter methane budgets through effects on the balance of different plant species, or
on plant morphology. In addition, the soil can be a net sink for methane in some terrestrial
ecosystems.170, 171
Other volatile organic compounds (VOCs) emitted from terrestrial vegetation (e.g., isoprene) are
indirect sources of CO2172 and are important in the chemistry of the troposphere, which in turn
may influence the UV climate (see Chapters 1 and 6). The production of VOCs is sensitive to
elements of climate such as increased CO2 concentration, drought and warming.173, 174
There are substantial emissions of carbon monoxide from both terrestrial and marine
ecosystems.1 In terrestrial ecosystems major peaks of CO are associated with periods of largescale forest burning.175, 176 CO emissions from terrestrial ecosystems are partly caused by
photodegradation, in which solar UV plays a major role.1, 177, 178 This is consistent with the
observation that increases in CO emissions following burning are exacerbated by sunlight177 and
demonstrates the potential for interactions between burning and changing UV on CO emissions.
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
Figure 5-7. Dimethylsulfide plays a substantial role in the balance between incoming and outgoing radiation in the
marine atmosphere. This figure shows the global distribution of the flux of DMS from the ocean to the atmosphere,
based on a model created by the use of a detailed ecosystem model of oceanic nutrients, phytoplankton and DMS
production.167 As climate change occurs and ocean circulation changes this will alter the surface ocean distributions
of DMS and change the exposure to surface UV-B. This is an example of how climate change alters the exposure of
climate reactive chemicals to UV-B radiation that is dependent on atmospheric ozone distributions.
Halogen-Containing Compounds
Climate change and UV-B influence the budget of halogen-containing compounds that alter
ozone chemistry in the atmosphere (see Chapters 1 and 6). The generation of halogen atoms in
atmospheric aerosols can be driven by processes involving UV radiation in the marine boundary
layer. Emissions of halomethanes related to climate change may interact with the flux of UV-B
to the Earth’s surface to modulate trends in atmospheric ozone concentrations.
Terrestrial ecosystems may be sources or sinks of methyl halides, the balance depending on a
range of environmental variables.179-182 Increased temperatures strongly influence emissions of
methyl bromide and methyl iodide from plants180, 182-184, but nothing is known about direct UV
effects on these emissions. The observation that ectomycorrhizal fungi are significant sources of
methyl halides181 may be pertinent since increasing UV can affect the activity of these fungi in at
least some systems.185 Agricultural ecosystems remain a significant source of methyl bromide
due to its continued use as a horticultural fumigant. The phase-out of methyl bromide fumigant
has been constrained by the perceived lack of alternatives for the control of major soil-borne
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
pests and pathogens, but recent research is pointing to economically viable alternatives, both
chemical and biological.186-189 Recent observations indicate that atmospheric methyl bromide
concentrations are decreasing at a rate of 2.5 – 3.0 % per year.190 However, because biogenic
emissions of methyl bromide from terrestrial ecosystems generally respond positively to
increased temperature, future global warming may change the current rate of decline of methyl
bromide concentrations in the atmosphere.
Marine systems also have significant influences on concentrations of halogenated compounds in
the atmosphere.1 Photoreactions involving UV can degrade brominated and iodinated methanes
in water191, 192 and halocarbons also are hydrolyzed in the ocean.1 Halogen chemistry as related
to oceanic releases of organic and inorganic bromine and chlorine has impacts on atmospheric
ozone.193, 194 The production of bromocarbons by marine algae in tropical surface waters leads to
significant emissions to the atmosphere.193, 194 Since these emissions of halogen containing
compounds occur in the same region as significant deep oceanic convection, there is evidence
that this oceanic source of bromine influences tropospheric ozone concentrations. Photolysis of
bromocarbons and reactions with ·OH create BrO that interacts with the ozone cycle. This is an
example of where the physical climate system, through atmospheric dynamics and circulation,
has feedbacks and interactions with the atmospheric chemical systems that influence ozone
concentrations and surface UV-B fluxes (also see Chapter 6).
Sulfur Gases
Sulfur emissions from the ocean are affected by interactions between UV-B radiation and
climate change. Of particular interest are dimethylsulfide (DMS) and carbonyl sulfide (COS).
DMS emissions influence the balance between incoming and outgoing radiation in the marine
atmosphere. Oceanic emissions of DMS produce particulates (i.e., sulfate aerosols) that directly
and indirectly have a cooling effect on the marine atmosphere. Upper ocean mixing dynamics
and the depth of the mixed layer can alter the effects of solar UV radiation on the biological
production of DMS.1 Several new studies have shown that UV and climate changes strongly
influence sea to air exchange of DMS by interacting with biological and photochemical sinks of
DMS in the upper ocean. Loss of DMS induced by UV-B is an important determinant of its
concentrations in the surface ocean.195-198 However, the effects of enhanced UV-B on DMS
emissions are complex and can vary from one ocean region to another.199-201 The results indicate
that the influence of DMS-related atmospheric sulfate particles is modulated by the levels of
surface UV radiation. As discussed previously UV may play a role in the production of carbonyl
sulfide, the most concentrated sulfur gas in the troposphere.1 New research has clarified this
role.202
Nitrogen containing compounds
Emissions of nitrogen oxides (NOx) can participate in tropospheric reactions that affect air
quality (see Chapter 6). One new finding has indicated that UV radiation induces NOx
emissions from terrestrial plants.203 NOx emissions can also be affected by elements of climate
change204 and especially by management practices in agroecosystems.205, 206
Concluding Remarks
Since our last report in 2002 there has been increasing international recognition of the
interactions and feedbacks between climate change and surface UV radiation, especially in
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
relation to biogeochemical cycles. It is in the nature of many of these interactions that they act
over medium-long time scales and as a result, understanding of the consequences remains limited.
It is clear that climate related changes in the input of organic matter to water bodies influences
the penetration of UV in to aquatic ecosystems. However, the role of such changes in specific
regions, especially at high latitudes, remains uncertain.
The following have been identified as important areas of uncertainty:
•
•
•
•
•
•
•
The interactions between trace gas generation and UV-B exposure.
The role of UV-B radiation in the formation of bio-available metal species in aquatic
systems.
The link between the chemical composition and the bio- and photo- reactivity of DOM.
The interactions of climate change induced ecosystem changes with changing surface
UV-B radiation.
The effects of the changing surface UV-B environment on future trends in climate and
atmospheric chemistry.
The role of UV-B in controlling biogeochemical cycling in terrestrial ecosystems,
especially in the context of changing patterns of drought and cloud-cover resulting from
climate change.
The influence of climate-induced changes in aquatic mixing and stratification and
continental runoff on biogeochemical cycling in freshwaters and the ocean.
Acknowledgements
We gratefully acknowledge the input and assistance of many other scientists in providing prepublication copies of some of the manuscripts that were cited here. This paper has been
reviewed in accordance with the U.S. Environmental Protection Agency’s peer and
administrative review policies and approved for publication. Mention of trade names or
commercial products does not constitute endorsement or recommendation for use by the U.S.
References
1
2
3
4
5
6
Zepp RG, Callaghan TV, Erickson DJ, III, Interactive effects of ozone depletion and
climate change on biogeochemical cycles, Photochem. Photobiol. Sci., 2003, 2, 51-61.
Houghton RA, Why are estimates of the terrestrial carbon balance so different?, Glob.
Change Biol., 2003, 9, 500-509.
Grace J, Understanding and managing the global carbon cycle, J. Ecol., 2004, 92, 189-202.
Cauwet G, DOM in the coastal zone, in Biogochemistry of Marine Dissolved Organic
Matter eds.: Hansell DA, Carlson CA, Academic Press, Amsterdam, 2002, pp. 579-609.
Chen RF, Bissett P, Coble P, Conmy R, Gardner GB, Moran MA, Wang XC, Wells ML,
Whelan P, Zepp RG, Chromophoric dissolved organic matter (CDOM) source
characterization in the Louisiana Bight, Mar. Chem., 2004, 89, 257-272.
Hansell DA, Kadko D, Bates NR, Degradation of terrigenous dissolved organic carbon in
the western Arctic Ocean, Science., 2004, 304, 858-861.
The Environmental Effects Assessment Panel Report for 2006
151
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
152
Zanardi-Lamardo E, Moore CA, Zika RG, Seasonal variation in molecular mass and optical
properties of chromophoric dissolved organic material in coastal waters of southwest
Florida, Mar. Chem., 2004, 89, 37-54.
Del Vecchio R, Blough NV, Photobleaching of chromophoric dissolved organic matter in
natural waters: kinetics and modeling, Mar. Chem., 2002, 78, 231-253.
Twardowski MS, Donaghay PL, Photobleaching of aquatic dissolved materials: Absorption
removal, spectral alteration, and their interrelationship, Journal of Geophysical ResearchOceans, 2002, 107, C8, 3091, DOI:10.1029/1999JC000281.
Xie HX, Zafiriou OC, Cai WJ, Zepp RG, Wang YC, Photooxidation and its effects on the
carboxyl content of dissolved organic matter in two coastal rivers in the Southeastern
United States, Environ. Sci. Technol., 2004, 38, 4113-4119.
Del Vecchio R, Blough NV, On the origin of the optical properties of humic substances,
Environ. Sci. Technol., 2004, 38, 3885-3891.
Brinkmann T, Sartorius D, Frimmel FH, Photobleaching of humic rich dissolved organic
matter, Aquat. Sci., 2003, 65, 415-424.
Kowalczuk P, Cooper WJ, Whitehead RF, Durako MJ, Sheldon W, Characterization of
CDOM in an organic-rich river and surrounding coastal ocean in the South Atlantic Bight,
Aquat. Sci., 2003, 65, 384-401.
Stabenau ER, Zika RG, Correlation of the absorption coefficient with a reduction in mean
mass for dissolved organic matter in southwest Florida river plumes, Mar. Chem., 2004, 89,
55-67.
Zepp RG, Sheldon WM, Moran MA, Dissolved organic fluorophores in southeastern US
coastal waters: correction method for eliminating Rayleigh and Raman scattering peaks in
excitation-emission matrices, Mar. Chem., 2004, 89, 15-36.
Goldstone JV, Pullin MJ, Bertilsson S, Voelker BM, Reactions of hydroxyl radical with
humic substances: Bleaching, mineralization, and production of bioavailable carbon
substrates, Environ. Sci. Technol., 2002, 36, 364-372.
Molot LA, Hudson JJ, Dillon PJ, Miller SA, Effect of pH on photo-oxidation of dissolved
organic carbon by hydroxyl radicals in a coloured, softwater stream, Aquat. Sci., 2005, 67,
189-195.
White EM, Vaughan PP, Zepp RG, Role of the photo-Fenton reaction in the production of
hydroxyl radicals and photobleaching of colored dissolved organic matter in a coastal river
of the southeastern United States, Aquat. Sci., 2003, 65, 402-414.
Batjes NH, Sombroek WG, Possibilities for carbon sequestration in tropical and subtropical
soils, Glob. Change Biol., 1997, 3, 161-173.
IPCC, Climate Change 2001: the Scientific Basis. Contribution of Working Group I to the
Third Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge
University Press, Cambridge, UK., 2001.
Ito A, Climate-related uncertainties in projections of the twenty-first century terrestrial
carbon budget: off-line model experiments using IPCC greenhouse-gas scenarios and
AOGCM climate projections, Climate Dynamics, 2005, 24, 435-448.
Lenton TM, Huntingford C, Global terrestrial carbon storage and uncertainties in its
temperature sensitivity examined with a simple model, Glob. Change Biol., 2003, 9, 13331352.
The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
Niemi R, Martikainen PJ, Silvola J, Wulff A, Turtola S, Holopainen T, Elevated UV-B
radiation alters fluxes of methane and carbon dioxide in peatland microcosms, Glob.
Change Biol., 2002, 8, 361-371.
Rinnan R, Impio M, Silvola J, Holopainen T, Martikainen PJ, Carbon dioxide and methane
fluxes in boreal peatland microcosms with different vegetation cover - effects of ozone or
ultraviolet-B exposure, Oecologia, 2003, 137, 475-483.
Hughes KA, Lawley B, Newsham KK, Solar UV-B radiation inhibits the growth of
antarctic terrestrial fungi, Appl. Environ. Microbiol., 2003, 69, 1488-1491.
Robson TM, Pancotto VA, Ballare CL, Sala OE, Scopel AL, Caldwell MM, Reduction of
solar UV-B mediates changes in the Sphagnum capitulum microenvironment and the
peatland microfungal community, Oecologia, 2004, 140, 480-490.
Robson TM, Pancotto VA, Scopel AL, Flint SD, Caldwell MM, Solar UV-B influences
microfaunal community composition in a Tierra del Fuego peatland, Soil. Biol. Biochem.,
2005, 37, 2205-2215.
Gwynn-Jones D, Huang W, Easton G, Goodacre R, Scullion J, UV-B radiation induced
changes in litter quality affects earthworm growth and cast characteristics as determined by
metabolic fingerprinting, Pedobiologia., 2003, 47, 784-787.
Avery LM, Smith RIL, West HM, Response of rhizosphere microbial communities
associated with Antarctic hairgrass (Deschampsia antarctica) to UV radiation, Polar Biol.,
2003, 26, 525-529.
Avery LM, Thorpe PC, Thompson K, Paul ND, Grime JP, West HM, Physical disturbance
of an upland grassland influences the impact of elevated UV-B radiation on metabolic
profiles of below-ground micro-organisms, Glob. Change Biol., 2004, 10, 1146-1154.
Rinnan R, Keinanen MM, Kasurinen A, Asikainen J, Kekki TK, Holopainen T, Ro-Poulsen
H, Mikkelsen TN, Michelsen A, Ambient ultraviolet radiation in the Arctic reduces root
biomass and alters microbial community composition but has no effects on microbial
biomass, Glob. Change Biol., 2005, 11, 564-574.
Johnson D, Campbell CD, Lee JA, Callaghan TV, Gwynn-Jones D, Arctic microorganisms
respond more to elevated UV-B radiation than CO2, Nature, 2002, 416, 82-83.
Austin AT, Vivanco L, Plant litter decomposition in a semi-arid ecosystem controlled by
photodegradation, Nature, 2006, 442, 555-558.
Pancotto VA, Sala OE, Robson TM, Caldwell MM, Scopel AL, Direct and indirect effects
of solar ultraviolet-B radiation on long-term decomposition, Glob. Change Biol., 2005, 11,
1982-1989.
Pancotto VA, Sala OE, Cabello M, Lopez NI, Robson TM, Ballare CL, Caldwell MM,
Scopel AL, Solar UV-B decreases decomposition in herbaceous plant litter in Tierra del
Fuego, Argentina: potential role of an altered decomposer community, Glob. Change Biol.,
2003, 9, 1465-1474.
Verma B, Robarts RD, Headley JV, Seasonal changes in fungal production and biomass on
standing dead Scirpus lacustris litter in a northern prairie wetland, Appl. Environ.
Microbiol., 2003, 69, 1043-1050.
Newsham KK, Anderson JM, Sparks TH, Splatt P, Woods C, McLeod AR, UV-B effect on
Quercus robur leaf litter decomposition persists over four years, Glob. Change Biol., 2001,
7, 479-483.
McLeod A, Newsham K, Fry S, Elevated UV-B radiation modifies the extractability of
carbohydrates from leaf litter of Quercus robur, Soil. Biol. Biochem., 2007, 39, 116-126.
The Environmental Effects Assessment Panel Report for 2006
153
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
39
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
154
Hoorens B, Aerts R, Stroetenga M, Elevated UV-B radiation has no effect on litter quality
and decomposition of two dune grassland species: evidence from a long-term field
experiment, Glob. Change Biol., 2004, 10, 200-208.
Tegelberg R, Aphalo PJ, Julkunen-Tiitto R, Effects of long-term, elevated ultraviolet-B
radiation on phytochemicals in the bark of silver birch (Betula pendula), Tree. Physiol.,
2002, 22, 1257-1263.
Chimphango SBM, Musil CF, Dakora FD, Response of purely symbiotic and NO3-fed
nodulated plants of Lupinus luteus and Vicia atropurpurea to ultraviolet-B radiation, J. Exp.
Bot., 2003, 54, 1771-1784.
Chimphango SBM, Musil CF, Dakora FD, Effects of UV-B radiation on plant growth,
symbiotic function and concentration of metabolites in three tropical grain legumes, Funct.
Plant Biol., 2003, 30, 309-318.
Chimphango SBM, Musil CF, Dakora FD, Responses to ultraviolet-B radiation by purely
symbiotic and NO3-fed nodulated tree and shrub legumes indigenous to Southern Africa,
Tree. Physiol., 2004, 24, 181-192.
Bertin C, Yang XH, Weston LA, The role of root exudates and allelochemicals in the
rhizosphere, Plant and Soil, 2003, 256, 67-83.
Kraus TEC, Zasoski RJ, Dahlgren RA, Horwath WR, Preston CM, Carbon and nitrogen
dynamics in a forest soil amended with purified tannins from different plant species, Soil.
Biol. Biochem., 2004, 36, 309-321.
Smolander A, Loponen J, Suominen K, Kitunen V, Organic matter characteristics and C
and N transformations in the humus layer under two tree species, Betula pendula and Picea
abies, Soil. Biol. Biochem., 2005, 37, 1309-1318.
Bassman JH, Ecosystem consequences of enhanced solar ultraviolet radiation: Secondary
plant metabolites as mediators of multiple trophic interactions in terrestrial plant
communities, Photochem. Photobiol., 2004, 79, 382-398.
Keski-Saari S, Pusenius J, Julkunen-Tiitto R, Phenolic compounds in seedlings of Betula
pubescens and B. pendula are affected by enhanced UVB radiation and different nitrogen
regimens during early ontogeny, Glob. Change Biol., 2005, 11, 1180-1194.
Warren JM, Bassman JH, Eigenbrode S, Leaf chemical changes induced in Populus
trichocarpa by enhanced UV-B radiation and concomitant effects on herbivory by
Chrysomela scripta (Coleoptera: Chrysomelidae), Tree. Physiol., 2002, 22, 1137-1146.
Kuijper LDJ, Berg MP, Morrien E, Kooi BW, Verhoef HA, Global change effects on a
mechanistic decomposer food web model, Glob. Change Biol., 2005, 11, 249-265.
Bertilsson S, Jones JL, Supply of dissolved organic matter to aquatic ecosystems:
Autochthonous sources, in Aquatic Ecosystems: Interactivity of Dissolved Orgnaic Matter
eds.: Findlay SEG, Sinsabaugh RL, Academic Press, Amsterdam, 2003, pp. 3-25.
Biddanda BA, Cotner JB, Enhancement of dissolved organic matter bioavailability by
sunlight and its role in the carbon cycle of Lakes Superior and Michigan, J. Great Lakes
Res., 2003, 29, 228-241.
Obernosterer I, Benner R, Competition between biological and photochemical processes in
the mineralization of dissolved organic carbon, Limnol. Oceanogr., 2004, 49, 117-124.
Vähätalo AV, Wetzel RG, Photochemical and microbial decomposition of chromophoric
dissolved organic matter during long (months-years) exposures, Mar. Chem., 2004, 89,
313-326.
The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
Anesio AM, Graneli W, Photochemical mineralization of dissolved organic carbon in lakes
of differing pH and humic content, Archiv Fur Hydrobiologie, 2004, 160, 105-116.
Clark CD, Hiscock WT, Millero FJ, Hitchcock G, Brand L, Miller WL, Ziolkowski L,
Chen RF, Zika RG, CDOM distribution and CO2 production on the southwest Florida shelf,
Mar. Chem., 2004, 89, 145-167.
Kaiser E, Sulzberger B, Phototransformation of riverine dissolved organic matter (DOM) in
the presence of abundant iron: Effect on DOM bioavailability, Limnol. Oceanogr., 2004, 49,
540-554.
Pullin MJ, Bertilsson S, Goldstone JV, Voelker BM, Effects of sunlight and hydroxyl
radical on dissolved organic matter: Bacterial growth efficiency and production of
carboxylic acids and other substrates, Limnol. Oceanogr., 2004, 49, 2011-2022.
Daniel C, Graneli W, Kritzberg ES, Anesio AM, Stimulation of metazooplankton by
photochemically modified dissolved organic matter, Limnol. Oceanogr., 2006, 51, 101-108.
Mayer LM, Schick LL, Skorko K, Boss E, Photodissolution of particulate organic matter
from sediments, Limnol. Oceanogr., 2006, 51, 1064-1071.
Vähätalo AV, Zepp RG, Photochemical mineralization of dissolved organic nitrogen to
ammonium in the Baltic Sea, Environ. Sci. Technol., 2005, 39, 6985-6992.
Vähätalo AV, Salonen K, Münster U, Järvinen M, Wetzel RG, Photochemical
transformation of allochthonous organic matter provides bioavailable nutrients in a humic
lake, Arch. Hydrobiol., 2003, 156, 287-314.
Tank SE, Xenopoulos MA, Hendzel LL, Effect of ultraviolet radiation on alkaline
phosphatase activity and planktonic phosphorus acquisition in Canadian boreal shield lakes,
Limnol. Oceanogr., 2005, 50, 1345-1351.
Tietjen T, Wetzel RG, Extracellular enzyme-clay mineral complexes: Enzyme adsorption,
alteration of enzyme activity, and protection from photodegradation, Aquat. Ecol., 2003, 37,
331-339.
Dalton H, Brand-Hardy R, Nitrogen: the essential public enemy, J. Appl. Ecol., 2003, 40,
771-781.
Caldwell MM, Ballaré CL, Bornman JF, Flint SD, Björn LO, Teramura AH,
Kulandaivelu G, Tevini M, Terrestrial ecosystems, increased solar ultraviolet radiation and
interactions with other climate change factors, Photochem. Photobiol. Sci., 2003, 2, 29-38.
Bjerke JW, Zielke M, Solheim B, Long-term impacts of simulated climatic change on
secondary metabolism, thallus structure and nitrogen fixation activity in two cyanolichens
from the Arctic, New. Phytol., 2003, 159, 361-367.
de la Rosa TM, Aphalo PJ, Lehto T, Effects of ultraviolet-B radiation on growth,
mycorrhizas and mineral nutrition of silver birch (Betula pendula Roth) seedlings grown in
low-nutrient conditions, Glob. Change Biol., 2003, 9, 65-73.
Morel FMM, Price NM, The biogeochemical cycles of trace metals in the oceans, Science.,
2003, 300, 944-947.
Peers G, Price NM, A role for manganese in superoxide dismutases and growth of irondeficient diatoms, Limnol. Oceanogr., 2004, 49, 1774-1783.
Peers G, Quesnel SA, Price NM, Copper requirements for iron acquisition and growth of
coastal and oceanic diatoms, Limnol. Oceanogr., 2005, 50, 1149-1158.
Sunda WG, Huntsman SA, Effect of CO2 supply and demand on zinc uptake and growth
limitation in a coastal diatom, Limnol. Oceanogr., 2005, 50, 1181-1192.
The Environmental Effects Assessment Panel Report for 2006
155
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
73
74
75
76
77
78
79
80
81
82
83
84
85
86
87
88
156
Dryden CL, Goron AS, Donat JR, Interactive regulation of dissolved copper toxicity by an
estuarine microbial community, Limnol. Oceanogr., 2004, 49, 1115-1122.
Drevnick PE, Sandheinrich MB, Effects of dietary methylmercury on reproductive
endocrinology of fathead minnows, Environ. Sci. Technol., 2003, 37, 4390-4396.
Dupont CL, Ahner BA, Effects of copper, cadmium, and zinc on the production and
exudation of thiols by Emiliania huxleyi, Limnol. Oceanogr., 2005, 50, 508-515.
Tang D, Shafer MM, Karner DA, Armstrong DE, Response of nonprotein thiols to copper
stress and extracellular release of glutathione in the diatom Thalassiosira weissflogii,
Limnol. Oceanogr., 2005, 50, 516-525.
Bruland KW, Rue EL, Smith GJ, DiTullio GR, Iron, macronutrients and diatom blooms in
the Peru upwelling regime: brown and blue waters of Peru, Mar. Chem., 2005, 93, 81-103.
Price NM, The elemental stoichiometry and composition of an iron-limited diatom, Limnol.
Oceanogr., 2005, 50, 1159-1171.
Mills MM, Ridame C, Davey M, La Roche J, Geider RJ, Iron and phosphorus co-limit
nitrogen fixation in the eastern tropical North Atlantic, Nature, 2004, 429, 292-294.
Buesseler KO, Boyd PW, Will ocean fertilization work?, Science., 2003, 300, 67-68.
Coale KH, Johnson KS, Chavez FP, Buesseler KO, Barber RT, Brzezinski MA, Cochlan
WP, Millero FJ, Falkowski PG, Bauer JE, Wanninkhof RH, Kudela RM, Altabet MA,
Hales BE, Takahashi T, Landry MR, Bidigare RR, Wang XJ, Chase Z, Strutton PG,
Friederich GE, Gorbunov MY, Lance VP, Hilting AK, Hiscock MR, Demarest M, Hiscock
WT, Sullivan KF, Tanner SJ, Gordon RM, Hunter CN, Elrod VA, Fitzwater SE, Jones JL,
Tozzi S, Koblizek M, Roberts AE, Herndon J, Brewster J, Ladizinsky N, Smith G, Cooper
D, Timothy D, Brown SL, Selph KE, Sheridan CC, Twining BS, Johnson ZI, Southern
ocean iron enrichment experiment: Carbon cycling in high- and low-Si waters, Science.,
2004, 304, 408-414.
Boyd PW, Law CS, Wong CS, Nojiri Y, Tsuda A, Levasseur M, Takeda S, Rivkin R,
Harrison PJ, Strzepek R, Gower J, McKay RM, Abraham E, Arychuk M, Barwell-Clarke J,
Crawford W, Crawford D, Hale M, Harada K, Johnson K, Kiyosawa H, Kudo I, Marchetti
A, Miller W, Needoba J, Nishioka J, Ogawa H, Page J, Robert M, Saito H, Sastri A, Sherry
N, Soutar T, Sutherland N, Taira Y, Whitney F, Wong SKE, Yoshimura T, The decline and
fate of an iron-induced subarctic phytoplankton bloom, Nature, 2004, 428, 549-553.
Buesseler KO, Andrews JE, Pike SM, Charette MA, The effects of iron fertilization on
carbon sequestration in the Southern Ocean, Science., 2004, 304, 414-417.
Buesseler KO, Andrews JE, Pike SM, Charette MA, Goldson LE, Brzezinski MA, Lance
VP, Particle export during the southern ocean iron experiment (SOFeX), Limnol. Oceanogr.,
2005, 50, 311-327.
Shaked Y, Kustka AB, Morel FMM, A general kinetic model for iron acquisition by
eukaryotic phytoplankton, Limnol. Oceanogr., 2005, 50, 872-882.
Fujii M, Rose AL, Waite TD, Omura T, Superoxide-mediated Dissolution of Amorphous
Ferric Oxyhydroxide in Seawater, Environ. Sci. Technol., 2006, 40, 880-887.
Rose AL, Waite TD, Reduction of organically complexed ferric iron by superoxide in a
simulated natural water, Environ. Sci. Technol., 2005, 39, 2645-2650.
Rijkenberg MJA, Fischer AC, Kroon JJ, Gerringa LJA, Timmermans KR, Wolterbeek HT,
de Baar HJW, The influence of UV irradiation on the photoreduction of iron in the
Southern Ocean, Mar. Chem., 2005, 93, 119-129.
The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
89
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
Rijkenberg MJA, Gerringa LJA, Neale PJ, Timmermans KR, Buma AGJ, de Baar HJW,
UVA variability overrules UVB ozone depletion effects on the photoreduction of iron in
the Southern Ocean, Geophys Res Lett, 2004, 31, L24310, DOI:10.1029/2004GL020829.
Rose AL, Waite TD, Effect of dissolved natural organic matter on the kinetics of ferrous
iron oxygenation in seawater, Environ. Sci. Technol., 2003, 37, 4877-4886.
Rose AL, Waite TD, Kinetic model for Fe(II) oxidation in seawater in the absence and
presence of natural organic matter, Environ. Sci. Technol., 2002, 36, 433-444.
Santana-Casiano JM, Gonzaalez-Davila M, Millero FJ, Oxidation of nanomolar levels of
Fe(II) with oxygen in natural waters, Environ. Sci. Technol., 2005, 39, 2073-2079.
Santana-Casiano JM, Gonzalez-Davila M, Millero FJ, The oxidation of Fe(II) in NaClHCO3- and seawater solutions in the presence of phthalate and salicylate ions: a kinetic
model, Mar. Chem., 2004, 85, 27-40.
Mahowald NM, Baker AR, Bergametti G, Brooks N, Duce RA, Jickells TD, Kubilay N,
Prospero JM, Tegen I, Atmospheric global dust cycle and iron inputs to the ocean, Glob.
Biogeochem. Cycles, 2005, 19, GB4025, DOI:10.1029/2004GB002402.
Erickson DJ, III, Hernandez J, Ginoux P, Gregg W, McClain C, Christian J, Atmospheric
iron delivery and surface ocean biological activity in the Southern Ocean and Patagonian
region, Geophys. Res. Lett., 2003, 30, DOI:10.1029/2003GL017241.
Buerge-Weirich D, Sulzberger B, Formation of Cu(I) in estuarine and marine waters:
Application of a new solid-phase extraction method to measure Cu(I), Environ. Sci.
Technol., 2004, 38, 1843-1848.
Kieber RJ, Skrabal SA, Smith C, Willey JD, Redox speciation of copper in rainwater:
Temporal variability and atmospheric deposition, Environ. Sci. Technol., 2004, 38, 35873594.
Shank GC, Whitehead RF, Smith ML, Skrabal SA, Kieber RJ, Photodegradation of strong
copper-complexing ligands in organic-rich estuarine waters, Limnol. Oceanogr., 2006, 51,
884-892.
Balcom PH, Fitzgerald WF, Vandal GM, Lamborg CH, Rolfllus KR, Langer CS,
Hammerschmidt CR, Mercury sources and cycling in the Connecticut River and Long
Island Sound, Mar. Chem., 2004, 90, 53-74.
Kainz M, Mazumder A, Effect of algal and bacterial diet on methyl mercury concentrations
in zooplankton, Environ. Sci. Technol., 2005, 39, 1666-1672.
O'Driscoll NJ, Lean DRS, Loseto LL, Carignan R, Siciliano SD, Effect of dissolved
organic carbon on the photoproduction of dissolved gaseous mercury in lakes: Potential
impacts of forestry, Environ. Sci. Technol., 2004, 38, 2664-2672.
Rolfhus KR, Fitzgerald WF, Mechanisms and temporal variability of dissolved gaseous
mercury production in coastal seawater, Mar. Chem., 2004, 90, 125-136.
Hines NA, Brezonik PL, Mercury dynamics in a small Northern Minnesota lake: water to
air exchange and photoreactions of mercury, Mar. Chem., 2004, 90, 137-149.
Lalonde JD, Amyot M, Orvoine J, Morel FMM, Auclair JC, Ariya PA, Photoinduced
oxidation of Hg0(aq) in the waters from the St. Lawrence estuary, Environ. Sci. Technol.,
2004, 38, 508-514.
Siciliano SD, O'Driscoll NJ, Tordon R, Hill J, Beauchamp S, Lean DRS, Abiotic
production of methylmercury by solar radiation, Environ. Sci. Technol., 2005, 39, 10711077.
The Environmental Effects Assessment Panel Report for 2006
157
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
106 Bonzongo JCJ, Donkor AK, Increasing UV-B radiation at the earth's surface and potential
effects on aqueous mercury cycling and toxicity, Chemosphere, 2003, 52, 1263-1273.
107 Meunier L, Laubscher H-U, Hug SJ, Sulzberger B, Effects of size and origin of natural
dissolved organic matter compounds on the redox cycling of iron in sunlit surface waters,
Aquat. Sci., 2005, 67, in press.
108 Lupinkova L, Komenda J, Oxidative modifications of the Photosystem II D1 protein by
reactive oxygen species: From isolated protein to cyanobacterial cells, Photochem.
Photobiol., 2004, 79, 152-162.
109 Southworth BA, Voelker BM, Hydroxyl radical production via the photo-Fenton reaction
in the presence of fulvic acid, Environ. Sci. Technol., 2003, 37, 1130-1136.
110 Boreen AL, Arnold WA, McNeill K, Triplet-sensitized photodegradation of sulfa drugs
containing six-membered heterocyclic groups: Identification of an SO2 extrusion
photoproduct, Environ. Sci. Technol., 2005, 39, 3630-3638.
111 Lam MW, Mabury SA, Photodegradation of the pharmaceuticals atorvastatin,
carbamazepine, levofloxacin, and sulfamethoxazole in natural waters, Aquat. Sci., 2005, 67,
177-188.
112 Lam MW, Young CJ, Brain RA, Johnson DJ, Hanson MA, Wilson CJ, Richards SM,
Solomon KR, Mabury SA, Aquatic persistence of eight pharmaceuticals in a microcosm
study, Environ. Toxicol. Chem., 2004, 23, 1431-1440.
113 Miller PL, Chin YP, Indirect photolysis promoted by natural and engineered wetland water
constituents: Processes leading to alachlor degradation, Environ. Sci. Technol., 2005, 39,
4454-4462.
114 Chin YP, Miller PL, Zeng LK, Cawley K, Weavers LK, Photosensitized degradation of
bisphenol a by dissolved organic matter, Environ. Sci. Technol., 2004, 38, 5888-5894.
115 McNally AM, Moody EC, McNeill K, Kinetics and mechanism of the sensitized
photodegradation of lignin model compounds, Photochem. Photobiol. Sci., 2005, 4, 268274.
116 Kwan WP, Voelker BM, Rates of hydroxyl radical generation and organic compound
oxidation in mineral-catalyzed Fenton-like systems, Environ. Sci. Technol., 2003, 37, 11501158.
117 Kwan WP, Voelker BM, Decomposition of hydrogen peroxide and organic compounds in
the presence of dissolved iron and ferrihydrite, Environ. Sci. Technol., 2002, 36, 1467-1476.
118 Scully NM, Cooper WJ, Tranvik LJ, Photochemical effects on microbial activity in natural
waters: the interaction of reactive oxygen species and dissolved organic matter, Fems
Microbiology Ecology, 2003, 46, 353-357.
119 Ciais P, Reichstein M, Viovy N, Granier A, Ogée J, Allard V, Aubinet M, Buchmann N,
Bernhofer C, Carrara A, Chevallier F, De Noble N, Friend AD, Friedlingstein P, Grünwald
T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteucci G,
Miglietta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz
MJ, Schulze ED, Vesala T, Valentini R, Europe-wide reduction in primary productivity
caused by the heat and drought in 2003, Nature, 2005, 437, 529-533.
120 Jones CD, Cox PM, On the significance of atmospheric CO2 growth rate anomalies in
2002-2003, Geophys Res Lett, 2005, 32, L14816 DOI:10.1029/2005GL023027.
121 Madronich S, McKenzie RL, Björn LO, Caldwell MM, Changes in biologically active
ultraviolet radiation reaching the Earth's surface, J. Photochem. Photobiol. B: Biology,
1998, 46, 1-27.
158
The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
122 McKenzie RL, Björn LO, Bais A, Ilyas M, Changes in biologically active radiation
reaching the Earth's surface, Photochem. Photobiol. Sci., 2003, 2, 5-15.
123 Ichii K, Hashimoto H, Nemani R, White M, Modeling the interannual variability and trends
in gross and net primary productivity of tropical forests from 1982 to 1999, Glob. Planet.
Change, 2005, 48, 274-286.
124 Nemani RR, Keeling CD, Hashimoto H, Jolly WM, Piper SC, Tucker CJ, Myneni RB,
Running SW, Climate-driven increases in global terrestrial net primary production from
1982 to 1999, Science., 2003, 300, 1560-1563.
125 Liu LX, Xu SM, Woo KC, Solar UV-B radiation on growth, photosynthesis and the
xanthophyll cycle in tropical acacias and eucalyptus, Environ. Exp. Bot., 2005, 54, 121-130.
126 Angert A, Biraud S, Bonfils C, Henning CC, Buermann W, Pinzon J, Tucker CJ, Fung I,
Drier summers cancel out the CO2 uptake enhancement induced by warmer springs, Proc.
Nat. Acad. Sci. USA., 2005, 102, 10823-10827.
127 Jia GSJ, Epstein HE, Walker DA, Greening of arctic Alaska, 1981-2001, Geophys Res Lett,
2003, 30, 20, 2067 DOI:10.1029/2003GL018268.
128 Xiao J, Moody A, Geographical distribution of global greening trends and their climatic
correlates: 1982-1998, International Journal of Remote Sensing, 2005, 26, 2371-2390.
129 Goetz SJ, Bunn AG, Fiske GJ, Houghton RA, Satellite-observed photosynthetic trends
across boreal North America associated with climate and fire disturbance, Proc. Nat. Acad.
Sci. USA., 2005, 102, 13521-13525.
130 D'Arrigo RD, Kaufmann RK, Davi N, Jacoby GC, Laskowski C, Myneni RB, Cherubini P,
Thresholds for warming-induced growth decline at elevational tree line in the Yukon
Territory, Canada, Glob. Biogeochem. Cycles, 2004, 18, GB3021,
DOI:10.1029/2004GB002249.
131 Burke RA, Zepp RG, Tarr MA, Miller WL, Stocks BJ, Effect of fire on soil-atmosphere
exchange of methane and carbon dioxide in Canadian boreal forests, J. Geophys. Res.,
1997, 102, 29289-29300.
132 Kaplan JO, Bigelow NH, Prentice IC, Harrison SP, Bartlein PJ, Christensen TR, Cramer W,
Matveyeva NV, McGuire AD, Murray DF, Razzhivin VY, Smith B, Walker DA, Anderson
PM, Andreev AA, Brubaker LB, Edwards ME, Lozhkin AV, Climate change and Arctic
ecosystems: 2. Modeling, paleodata-model comparisons, and future projections, J. Geophys.
Res. Atmos., 2003, 108, D19, 8171, DOI:10.1029/2002JD002559.
133 Fierer N, Allen AS, Schimel JP, Holden PA, Controls on microbial CO2 production: a
comparison of surface and subsurface soil horizons, Glob. Change Biol., 2003, 9, 13221332.
134 Knorr W, Prentice IC, House JI, Holland EA, Long-term sensitivity of soil carbon turnover
to warming, Nature, 2005, 433, 298-301.
135 Leifeld J, Fuhrer J, The temperature response of CO2 production from bulk soils and soil
fractions is related to soil organic matter quality, Biogeochemistry, 2005, 75, 433-453.
136 Mikan CJ, Schimel JP, Doyle AP, Temperature controls of microbial respiration in arctic
tundra soils above and below freezing, Soil. Biol. Biochem., 2002, 34, 1785-1795.
137 Fierer N, Craine JM, McLauchlan K, Schimel JP, Litter quality and the temperature
sensitivity of decomposition, Ecol., 2005, 86, 320-326.
138 Biasi C, Rusalimova O, Meyer H, Kaiser C, Wanek W, Barsukov P, Junger H, Richter A,
Temperature-dependent shift from labile to recalcitrant carbon sources of arctic
heterotrophs, Rapid Communications in Mass Spectrometry, 2005, 19, 1401-1408.
The Environmental Effects Assessment Panel Report for 2006
159
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
139 Heath J, Ayres E, Possell M, Bardgett RD, Black HIJ, Grant H, Ineson P, Kerstiens G,
Rising atmospheric CO2 reduces sequestration of root-derived soil carbon, Science., 2005,
309, 1711-1713.
140 Hoosbeek MR, Lukac M, van Dam D, Godbold DL, Velthorst EJ, Biondi FA, Peressotti A,
Cotrufo MF, de Angelis P, Scarascia-Mugnozza G, More new carbon in the mineral soil of
a poplar plantation under Free Air Carbon Enrichment (POPFACE): Cause of increased
priming effect?, Glob. Biogeochem. Cycles, 2004, 18, GB1040,
DOI:10.1029/2003GB002127.
141 van Groenigen KJ, Gorissen A, Six J, Harris D, Kuikman PJ, van Groenigen JW, van
Kessel C, Decomposition of C-14-labeled roots in a pasture soil exposed to 10 years of
elevated CO2, Soil. Biol. Biochem., 2005, 37, 497-506.
142 Xie ZB, Cadisch G, Edwards G, Baggs EM, Blum H, Carbon dynamics in a temperate
grassland soil after 9 years exposure to elevated CO2 (Swiss FACE), Soil. Biol. Biochem.,
2005, 37, 1387-1395.
143 Norby RJ, Ledford J, Reilly CD, Miller NE, O'Neill EG, Fine-root production dominates
response of a deciduous forest to atmospheric CO2 enrichment, Proc. Nat. Acad. Sci. USA.,
2004, 101, 9689-9693.
144 van Ginkel JH, Gorissen A, Polci D, Elevated atmospheric carbon dioxide concentration:
effects of increased carbon input in a Lolium perenne soil on microorganisms and
decomposition, Soil. Biol. Biochem., 2000, 32, 449-456.
145 Norby RJ, Cotrufo MF, Ineson P, O'Neill EG, Canadell JG, Elevated CO2, litter chemistry,
and decomposition: a synthesis, Oecologia, 2001, 127, 153-165.
146 Fransson PMA, Taylor AFS, Finlay RD, Mycelial production, spread and root colonisation
by the ectomycorrhizal fungi Hebeloma crustuliniforme and Paxillus involutus under
elevated atmospheric CO2, Mycorrhiza, 2005, 15, 25-31.
147 Freeman C, Kim SY, Lee SH, Kang H, Efflects of elevated atmospheric CO2
concentrations on soil microorganisms, Journal of Microbiology, 2004, 42, 267-277.
148 Janus LR, Angeloni NL, McCormack J, Rier ST, Tuchman NC, Kelly JJ, Elevated
atmospheric CO2 alters soil microbial communities associated with trembling aspen
(Populus tremuloides) roots, Micro. Ecol., 2005, 50, 102-109.
149 Klamer M, Roberts MS, Levine LH, Drake BG, Garland JL, Influence of elevated CO2 on
the fungal community in a coastal scrub oak forest soil investigated with terminalrestriction fragment length polymorphism analysis, Appl. Environ. Microbiol., 2002, 68,
4370-4376.
150 Davidson EA, Belk E, Boone RD, Soil water content and temperature as independent or
confounded factors controlling soil respiration in a temperate mixed hardwood forest, Glob.
Change Biol., 1998, 4, 217-227.
151 Flanagan LB, Johnson BG, Interacting effects of temperature, soil moisture and plant
biomass production on ecosystem respiration in a northern temperate grassland, Agric.
Forest Meteorol., 2005, 130, 237-253.
152 Xu LK, Baldocchi DD, Tang JW, How soil moisture, rain pulses, and growth alter the
response of ecosystem respiration to temperature, Glob. Biogeochem. Cycles, 2004, 18,
GB4002, DOI:10.1029/2004GB002281.
153 Gorissen A, Tietema A, Joosten NN, Estiarte M, Penuelas J, Sowerby A, Emmett BA,
Beier C, Climate change affects carbon allocation to the soil in shrublands, Ecosystems,
2004, 7, 650-661.
160
The Environmental Effects Assessment Panel Report for 2006
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
154 Nathalie F, Freeman C, Reynolds B, Hydrological effects on the diversity of phenolic
degrading bacteria in a peatland: implications for carbon cycling, Soil. Biol. Biochem.,
2005, 37, 1277-1287.
155 Stabenau ER, Zepp RG, Bartels E, Zika RG, Role of the seagrass Thalassia testudinum as a
source of chromophoric dissolved organic matter in coastal south Florida, Mar. Ecol.-Prog.
Ser., 2004, 282, 59-72.
156 Pastor J, Solin J, Bridgham SD, Updegraff K, Harth C, Weishampel P, Dewey B, Global
warming and the export of dissolved organic carbon from boreal peatlands, Oikos., 2003,
100, 380-386.
157 Scully NM, Maie N, Dailey SK, Boyer JN, Jones RD, Jaffe R, Early diagenesis of plantderived dissolved organic matter along a wetland, mangrove, estuary ecotone, Limnol.
Oceanogr., 2004, 49, 1667-1678.
158 Leavitt PR, Cumming BF, Smol JP, Reasoner M, Pienitz R, Hodgson DA, Climatic control
of ultraviolet radiation effects on lakes, Limnol. Oceanogr., 2003, 48, 2062-2069.
159 Del Vecchio R, Blough NV, Spatial and seasonal distribution of chromophoric dissolved
organic matter and dissolved organic carbon in the Middle Atlantic Bight, Mar. Chem.,
2004, 89, 169-187.
160 Bopp L, Monfray P, Aumont O, Dufresne J, Le Treut H, Madec G, Terray L, Orr JC,
Potential impact of climate change on marine export production, Glob. Biogeochem. Cycles,
2001, 15, 81-100.
161 Sarmiento JL, Slater R, Barber R, Bopp L, Doney SC, Hirst AC, Kleypas J, Matear R,
Mikolajewicz U, Monfray P, Soldatov V, Spall SA, Stouffer R, Response of ocean
ecosystems to climate warming, Global Biogeochem. Cycles, 2004, 18,
DOI:10.1029/2003GB002134.
162 Schmittner A, Decline of the marine ecosystem caused by a reduction in the Atlantic
overturning circulation, Nature, 2005, 434, 628-633.
163 Jankowski T, Livingstone DM, Bührer H, Forster R, Niederhauser P, Consequences of the
2003 European heat wave for lake temperature profiles, thermal stability, and hypolimnetic
oxygen depletion: Implications for a warmer world, Limnol. Oceanogr., 2006, 51, 815-819.
164 Huisman J, Pham Thi NN, Karl DM, Sommeijer B, Reduced mixing generates oscillations
and chaos in the oceanic deep chlorophyll maximum, Nature, 2006, 439, 322-325.
165 Siegel DA, Maritorena S, Nelson NB, Hansell DA, Lorenzi-Kayser M, Global distribution
and dynamics of colored dissolved and detrital organic materials, Journal of Geophysical
Research-Oceans, 2002, 107, DOI:10.1029/2001JC000965.
166 Johannessen SC, Miller WL, Cullen JJ, Calculation of UV attenuation and colored
dissolved organic matter absorption spectra from measurements of ocean color, Journal of
Geophysical Research-Oceans, 2003, 108, C9, 3301 DOI:10.1029/2000JC000514.
167 Chu S, Elliot S, Multrud M, Hernandez J, Erickson DJ, III, Ecodynamics and eddyadmitting dimethyl sulfide simulations in a global ocean biogeochemistry-circulation
model, Earth Interactions, 2004, 8, 1-15.
168 Strom L, Mastepanov M, Christensen TR, Species-specific effects of vascular plants on
carbon turnover and methane emissions from wetlands, Biogeochemistry, 2005, 75, 65-82.
169 Keppler F, Hamilton J, Bra M, Röckmann T, Methane emissions from terrestrial plants
under aerobic conditions, Nature, 2006, 439, 187-191.
The Environmental Effects Assessment Panel Report for 2006
161
Interactive effects of solar UV radiation and climate change on biogeochemical cycling
170 Liebig MA, Morgan JA, Reeder JD, Ellert BH, Gollany HT, Schuman GE, Greenhouse gas
contributions and mitigation potential of agricultural practices in northwestern USA and
western Canada, Soil. Tillage. Res., 2005, 83, 25-52.
171 Mosier AR, Halvorson AD, Peterson GA, Robertson GP, Sherrod L, Measurement of net
global warming potential in three agroecosystems, Nutrient Cycling in Agroecosystems,
2005, 72, 67-76.
172 Guenther A, The contribution of reactive carbon emissions from vegetation to the carbon
balance of terrestrial ecosystems, Chemosphere, 2002, 49, 837-844.
173 Naik V, Delire C, Wuebbles DJ, Sensitivity of global biogenic isoprenoid emissions to
climate variability and atmospheric CO2, J. Geophys. Res. Atmos., 2004, 109, D06301,
DOI:10.1029/2003JD004236.
174 Pegoraro E, Rey A, Bobich EG, Barron-Gafford G, Grieve KA, Malhi Y, Murthy R, Effect
of elevated CO2 concentration and vapour pressure deficit on isoprene emission from
leaves of Populus deltoides during drought, Funct. Plant Biol., 2004, 31, 1137-1147.
175 Edwards DP, Emmons LK, Hauglustaine DA, Chu DA, Gille JC, Kaufman YJ, Petron G,
Yurganov LN, Giglio L, Deeter MN, Yudin V, Ziskin DC, Warner J, Lamarque JF, Francis
GL, Ho SP, Mao D, Chen J, Grechko EI, Drummond JR, Observations of carbon monoxide
and aerosols from the Terra satellite: Northern Hemisphere variability, J. Geophys. Res.
Atmos., 2004, 109, D24202, DOI:10.1029/2004JD004727.
176 Simmonds PG, Manning AJ, Derwent RG, Ciais P, Ramonet M, Kazan V, Ryall D, A
burning question. Can recent growth rate anomalies in the greenhouse gases be attributed to
large-scale biomass burning events?, Atmos. Environ., 2005, 39, 2513-2517.
177 Kisselle KW, Zepp RG, Burke RA, Pinto AD, Bustamante MMC, Opsahl S, Varella RF,
Viana LT, Seasonal soil fluxes of carbon monoxide in burned and unburned Brazilian
savannas, J. Geophys. Res. Atmos., 2002, 107, D20, 8051, DOI:10.1029/2001JD000638.
178 Tarr MA, Miller WL, Zepp RG, Direct carbon-monoxide photoproduction from plant
matter, J. Geophys. Res. Atmos., 1995, 100, 11403-11413.
179 Cox ML, Fraser PJ, Sturrock GA, Siems ST, Porter LW, Terrestrial sources and sinks of
halomethanes near Cape Grim, Tasmania, Atmos. Environ., 2004, 38, 3839-3852.
180 Lee-Taylor J, Redeker KR, Reevaluation of global emissions from rice paddies of methyl
iodide and other species, Geophys Res Lett, 2005, 32, L15801,
DOI:10.1029/2005GL022918.
181 Redeker KR, Treseder KK, Allen MF, Ectomycorrhizal fungi: A new source of
atmospheric methyl halides?, Glob. Change Biol., 2004, 10, 1009-1016.
182 White ML, Varner RK, Crill PM, Mosedale CH, Controls on the seasonal exchange of
CH3Br in temperate peatlands, Glob. Biogeochem. Cycles, 2005, 19, GB4009,
DOI:10.1029/2004GB002343.
183 Redeker KR, Cicerone RJ, Environmental controls over methyl halide emissions from rice
paddies, Glob. Biogeochem. Cycles, 2004, 18, DOI:10.1029/2003GB002092.
184 Redeker KR, Manley SL, Walser M, Cicerone RJ, Physiological and biochemical controls
over methyl halide emissions from rice plants, Glob. Biogeochem. Cycles, 2004, 18,
GB1007, DOI:10.1029/2003GB002042.
185 Klironomos JN, Allen MF, UV-B-mediated changes on below-ground communities
associated with the roots of Acer saccharum, Funct. Ecol., 1995, 9, 923-930.
162
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
186 Arnault I, Mondy N, Diwo S, Auger J, Soil behaviour of sulfur natural fumigants used as
methyl bromide substitutes, International Journal of Environmental Analytical Chemistry,
2004, 84, 75-82.
187 Carter CA, Chalfant JA, Goodhue RE, Han FM, DeSantis M, The methyl bromide ban:
Economic impacts on the California strawberry industry, Review of Agricultural Economics,
2005, 27, 181-197.
188 De Cal A, Martinez-Treceno A, Lopez-Aranda JM, Melgarejo P, Chemical alternatives to
methyl bromide in Spanish strawberry nurseries, Plant Disease, 2004, 88, 210-214.
189 Sydorovych O, Safley CD, Ferguson LM, Poling EB, Fernandez GE, Brannen PA, Monks
DM, Louws FJ, Economic evaluation of methyl bromide alternatives for the production of
strawberries in the southeastern United States, Horttechnology, 2006, 16, 118-128.
190 Simmonds PG, Derwent RG, Manning AJ, Fraser PJ, Krummel PB, O'Doherty S, Prinn RG,
Cunnold DM, Miller BR, Wang HJ, Ryall DB, Porter LW, Weiss RF, Salameh PK,
AGAGE observations of methyl bromide and methyl chloride at Mace Head, Ireland, and
Cape Grim, Tasmania, 1998-2001, J Atmos Chem, 2004, 47, 243-269.
191 Du Y, Guan XG, Kwok WM, Chu LM, Phillips DL, Comparison of the dehalogenation of
dihalomethanes (CH2XI, where X = Cl, Br, I) following ultraviolet photolysis in aqueous
and NaCl saltwater environments, J. Phys. Chem. A, 2005, 109, 5872-5882.
192 Guan XG, Du Y, Li YL, Kwok WM, Phillips DL, Comparison of the dehalogenation of
polyhalomethanes and production of strong acids in aqueous and salt (NaCl) water
environments: Ultraviolet photolysis of CH2I2, J. Chem. Phys., 2004, 121, 8399-8409.
193 Salawitch RJ, Biogenic bromine, Nature, 2006, 439, 275-276.
194 Yang X, Cox RA, Warwick NJ, Pyle JA, Carver GD, O'Connor FM, Savage NH,
Tropospheric bromine chemistry and its impacts on ozone: A model study, J. Geophys. Res.
Atmos., 2005, 110, D23311, DOI:10.1029/2005JD006244.
195 Kieber DJ, Kiene RP, Siegel DA, Nelson NB, Photolysis and the dimethylsulfide (DMS)
summer paradox in the Sargasso Sea, Limnol. Oceanogr., 2003, 48, 1088-1100.
196 Kniveton DR, Todd MC, Sciare J, Variability of atmospheric dimethylysulphide over the
Southern Ocean due to changes in ultraviolet radiation, in 7th International Conference on
Southern Hemisphere Meteorology and Oceanography, Wellington, New Zealand, 2003,
pp. 218-219.
197 Deal CD, Kieber DJ, Toole DA, Stamnes K, Jiang S, Uzuka N, Dimethylsulfide photolysis
rates and apparent quantum yields in Bering Sea seawater, Cont. Shelf. Res., 2005, in press.
198 Bouillon R-C, Miller WL, Photodegradation of Dimethyl Sulfide (DMS) in Natural Waters:
Laboratory Assessment of the Nitrate-Photolysis-Induced DMS Oxidation, Environ. Sci.
Technol., 2005, 39, 9471-9477.
199 Harada H, Rouse MA, Sunda W, Kiene RP, Latitudinal and vertical distributions of
particle-associated dimethylsulfoniopropionate (DMSP) lyase activity in the western North
Atlantic Ocean, Can. J. Fish. Aquat. Sci., 2004, 61, 700-711.
200 Toole DA, Kieber DJ, Kiene RP, White EM, Bisgrove J, del Valle DA, Slezak D, High
dimethylsulfide photolysis rates in nitrate-rich Antarctic waters, Geophys Res Lett, 2004,
31, L11307, DOI:10.1029/2004GL019863.
201 Toole DA, Siegel DA, Light-driven cycling of dimethylsulfide (DMS) in the Sargasso Sea:
Closing the loop, Geophys Res Lett, 2004, 31, L09308, DOI:10.1029/2004GL019581.
202 Cutter GA, Cutter LS, Filippino KC, Sources and cycling of carbonyl sulfide in the
Sargasso Sea, Limnol. Oceanogr., 2004, 49, 555-565.
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Interactive effects of solar UV radiation and climate change on biogeochemical cycling
203 Hari P, Raivonen M, Vesala T, Munger JW, Pilegaard K, Kulmala M, Ultraviolet light and
leaf emission of NOx, Nature, 2003, 422, 134.
204 Davidson EA, Ishida FY, Nepstad DC, Effects of an experimental drought on soil
emissions of carbon dioxide, methane, nitrous oxide, and nitric oxide in a moist tropical
forest, Glob. Change Biol., 2004, 10, 718-730.
205 Bolan NS, Saggar S, Luo JF, Bhandral R, Singh J, Gaseous emissions of nitrogen from
grazed pastures: Processes, measurements and modelling, environmental implications, and
mitigation, in Advances in Agronomy, Vol. 84, 2004, pp. 37-120.
206 Li CS, Frolking S, Butterbach-Bahl K, Carbon sequestration in arable soils is likely to
increase nitrous oxide emissions, offsetting reductions in climate radiative forcing,
Clim.Change, 2005, 72, 321-338.
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Chapter 6. Changes in tropospheric composition and air quality
due to stratospheric ozone depletion and climate change
S. R. Wilsona, K. R. Solomonb, and X. Tangc
a
Department of Chemistry, University of Wollongong, NSW, 2522, Australia
Centre for Toxicology, University of Guelph, ON, N1G 2W1, Canada
c
Peking University, Center of Environmental Sciences, Beijing 100871, China
b
Summary
It is well-understood that reductions in air quality play a significant role in both environmental
and human health. Interactions between ozone depletion and global climate change will
significantly alter atmospheric chemistry which, in turn, will cause changes in concentrations of
natural and human-made gasses and aerosols. Models predict that tropospheric ozone near the
surface will increase globally by up to 10 to 30 ppbv (33 to 100% increase) during the period
2000 to 2100. With the increase in the amount of the stratospheric ozone, increased transport
from the stratosphere to the troposphere will result in different responses in polluted and
unpolluted areas. In contrast, global changes in tropospheric hydroxyl radical (OH) are not
predicted to be large, except where influenced by the presence of oxidizable organic matter, such
as from large-scale forest fires. Recent measurements in a relatively clean location over 5 years
showed that OH concentrations can be predicted by the intensity of solar ultraviolet radiation. If
this relationship is confirmed by further observations, this approach could be used to simplify
assessments of air quality. Analysis of surface-level ozone observations in Antarctica suggests
that there has been a significant change in the chemistry of the boundary layer of the atmosphere
in this region as a result of stratospheric ozone depletion. The oxidation potential of the
Antarctic boundary layer is estimated to be greater now than before the development of the
ozone hole.
Recent modeling studies have suggested that iodine and iodine-containing substances from
natural sources, such as the ocean, may increase stratospheric ozone depletion significantly in
polar regions during spring. Given the uncertainty of the fate of iodine in the stratosphere, the
results may also be relevant for stratospheric ozone depletion and measurements of the influence
of these substances on ozone depletion should be considered in the future.
In agreement with known usage and atmospheric loss processes, tropospheric concentrations of
HFC-134a, the main human-made source of trifluoroacetic acid (TFA), is increasing rapidly. As
HFC-134a is a potent greenhouse gas; this increasing concentration has implications for climate
change. However, the risks to humans and the environment from substances, such as TFA,
produced by atmospheric degradation of hydrochlorofluorocarbons (HCFCs) and
hydrofluorocarbons (HFCs) are considered minimal. Perfluoropolyethers, commonly used as
industrial heat transfer fluids and proposed as chloro-hydrofluorocarbon (CHFC) substitutes,
show great stability to chemical degradation in the atmosphere. These substances have been
suggested as substitutes for CHFCs but, as they are very persistent in the atmosphere, they may
be important contributors to global warming. It is not known whether these substances will
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165
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
contribute significantly to global warming and its interaction with ozone depletion but they
should be considered for further evaluation.
Introduction
Reductions in air quality (from the presence of pollutants in the atmosphere) play a significant
role in both environmental and human health. Poor air quality can lead to many adverse
outcomes such as acid rain and respiratory disease. In the context of this assessment, it is
recognized that increases in concentrations of tropospheric ozone and harmful substances
generated from ozone have been shown to have significant impacts on human health as well as in
the environment, particularly on plants. These effects have been widely reported and reviewed1-7
and are not discussed further here. The quality of the air depends on a wide range of factors,
including how rapidly chemicals are released and the reactions these substances undergo once
they are released into the atmosphere. Solar UV-B radiation (280 – 315 nm) provides the energy
for many of the chemical transformations that occur in the atmosphere. For example, the energy
provided causes photolysis of a number of important atmospheric trace gases, such as sulfur
dioxide (SO2), formaldehyde (HCHO), and ozone (O3). These processes will be altered by
anything that changes the amount of UV-B radiation, including the elevation of the sun, clouds,
and attenuation by some air pollutants.
The release of Ozone Depleting Substances (ODS), when transported to the stratosphere, reduces
the amount of ozone. Decreases in stratospheric ozone lead to enhanced UV-B radiation in the
lower atmosphere (troposphere), increasing the rate of the photolytic processes.8, 9 As a result,
there is a direct link between stratospheric ozone depletion and air quality.
There are other factors that change the reactive chemistry of the atmosphere, including increased
air pollution and the emissions of climatically important greenhouse gases. Changes in climate
can also dramatically change the chemistry of the atmosphere. Higher temperatures can lead to
increases in the rates of chemical reactions, in the amount of water vapor present, and thus OH
production10 as well as enhance emissions of volatile organic compounds such as isoprene from
biological sources.11 All of these factors then potentially interact in determining the actual
atmospheric condition.12, 13 Thus, while change in atmospheric composition and circulation are
observed, assigning cause and effect requires careful assessment.
The replacements for the original ozone depleting chemicals (chlorofluorocarbons (CFCs)), such
as the hydrochlorofluorocarbons (HCFCs) and the hydrofluorocarbons HFCs, decompose
primarily in the lower atmosphere. This decomposition can produce chemicals that impact air
quality.8
Here we present a summary of recent work on understanding the impacts of ozone depletion,
ozone depleting chemicals and their replacements on atmospheric composition and how these
may interact with climate change. This is an update of the information in the previous report.8
Stratosphere – Troposphere Exchange
One direct impact of stratospheric ozone depletion is a potential reduction in the amount of
ozone transported into the troposphere (Stratosphere Troposphere Exchange, STE). It has been
estimated that there has been an approximate 30% reduction in the amount of ozone transported
from the stratosphere to the troposphere due to stratospheric ozone depletion.14 While there is
agreement that ozone concentrations in the upper troposphere are very sensitive to change in
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
stratospheric ozone, there remains a divergence of opinion on the sensitivity of ground-level
ozone. Some calculations have predicted that up to 40% of ground-level ozone is due to
transport of ozone from the stratosphere, depending on season and location,15, 16 but other
estimates are a factor of two lower.14 All three models estimate that the contribution of vertically
transported ozone to ground-level ozone concentrations is smallest in summer compared with
other season in both hemispheres.
The mixing of stratospheric air (and hence ozone) into the troposphere is critically dependent on
atmospheric circulation. A modeling study of the chemistry-climate interactions showed that the
rate of ozone transport into the troposphere is affected by El Niño Southern Oscillation (ENSO)
events.13 An analysis of satellite ozone measurements also detected a dependence on ENSO,
although they suggest it is due to the impact of circulation changes on in situ production.17
Climatic variability can therefore mask changes in the contribution of stratospheric ozone to the
troposphere due to stratospheric ozone depletion.
The situation is further complicated as stratospheric ozone depletion appears to explain most of
the cooling observed in the lower stratosphere over the last two decades.18 Such a cooling will
modify STE, although it is not clear that this has been explicitly included in most current
atmospheric models. We can conclude, however, that stratospheric ozone depletion will have a
significant but small impact on tropospheric ozone amounts to date due to STE.
Significant longer-term increases in the amount of ozone brought into the troposphere from the
stratosphere have been predicted due to climate change (80% by 2100).19 This calculation
ignored the increase in stratospheric ozone, which would increase the stratospheric-tropospheric
transport further. Such changes in the upper troposphere are not directly convertible into
ground-level concentrations due to possible changes in chemical processes in the troposphere.
However, predictions indicate that ground-level ozone is likely to increase significantly in the
next century,14, 15 a trend enhanced by increases in stratospheric ozone. The predictions of these
models could be verified against measured concentrations. However, the number of sites with
long-term temporal and spatial measurements is few. This is an obvious data gap that could be
addressed with collection of additional monitoring information.
Atmospheric photolysis
There has been ongoing work studying the fundamental atmospheric processes that are driven by
solar radiation and, in particular, by UV-B radiation. Syntheses of data (photolysis cross
sections and reaction rates) have recently been produced.20-22 This section summarizes some of
the key recent outcomes of this work.
Ozone in the troposphere. Ozone in the lower atmosphere plays a number of key roles. Due to
its adverse impact upon both human and environmental health in many regions (e.g., European
Union2), it is used as a key indicator of air quality.
Photolysis of ozone in the lower atmosphere is the primary source of the hydroxyl radical (OH)
in unpolluted, humid environments, and OH initiates the removal process for most organic
chemicals in the atmosphere, including methane and CO. It is estimated that OH initiates the
destruction of 3 700 million tonnes of trace gases each year, including many gases involved in
ozone depletion, the greenhouse effect, and urban air pollution.23 These reactions lead to the
formation of products which are subsequently taken up by cloud droplets and precipitation and
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167
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
washed out of the atmosphere. OH therefore plays a dominant role in the ability of the
atmosphere to “cleanse” itself.
The formation of OH radical in clean environments is described by the following two reactions:
O3 + hν (λ < 340nm) → O2 + O( 1 D)
O(1 D) + H 2O → 2OH
(1)
(2)
The key ozone photolysis product for the formation of OH is the O(1D) atom. O(1D) is an oxygen
atom that has sufficient energy to react with H2O. Another possible product of light absorption
by ozone is the less energetic O(3P) oxygen atom which has insufficient energy to react with
water (reaction (2)) and primarily reacts with oxygen again to form ozone. The chemical
reactions have been discussed in more detail elsewhere.9
The production rate of O(1D) depends critically on the amount of UV radiation which, in turn, is
dependent upon stratospheric ozone. As stratospheric ozone depletion increases solar radiation in
the critical wavelength region, the loss of stratospheric ozone would be expected to lead to an
increase in tropospheric O(1D), if nothing else changed. The total rate of production of O(1D) is
determined by the concentration of ozone and the photodissociation constant J, which is given by
J = ∫ F ( λ ).σ ( λ , T ).φ ( λ , T )d λ ,
(6.1)
Relative units
where the integral is over wavelength (λ) at the temperature T. Here F(λ) is the actinic flux, a
measure of the amount of solar radiation available for initiating the chemical reaction, σ(λ,Τ) is
the strength of ozone absorption (cross section) and φ(λ,Τ) is the efficiency (quantum yield) of
O(1D) production. The wavelength dependence of these
Solar radiation
is shown in Figure 6-1. With decreasing wavelength, the
Ozone absorption
Relative O(1D) production rate
actinic flux (F(λ)) of solar radiation decreases
dramatically due to the absorption by (mainly
stratospheric) ozone, but the efficiency of production
increases (given by the product σ(λ,Τ)φ(λ,Τ)). This
results in a small range of wavelengths (primarily in the
UV-B region) where the maximum production of O(1D)
occurs. The wavelength of maximum O(1D) production
shifts depending on the amount of stratospheric ozone,
the elevation of the sun above the horizon, and
environmental parameters such as temperature.
There have been significant advances in the
determination of the actinic flux (see Chapter 1), which is
more formally defined as the amount of solar radiation
available at a point in the atmosphere. There are
instruments designed to measure actinic flux directly.24, 25
However, most measurements are of irradiance (the solar
300
320
340
energy falling on a horizontal surface – see Figure 6-2).
Wavelength (nm)
Methods have now been developed for converting
Figure 6-1. Production rate of O(1D) as a
irradiance to actinic flux.26-31 The uncertainty in
irradiance-derived actinic flux for J(O1D) is greater than function of wavelength with a solar zenith
angle of 60°
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
for directly measured values. The uncertainty in the conversion of irradiance into actinic flux
depends on the solar zenith angle, wavelength, and ambient conditions, but can be as low as 7%
(95% confidence).27
The quantum yield (φ(λ,Τ)) for production of O(1D) in the wavelength region around 308 nm is
crucial. First, this is the wavelength of maximum production. Secondly, many of the estimates
of the quantum yield at other wavelengths have been made relative to the quantum yield at 308
nm. Recent work has reduced the uncertainty in the quantum yield at 308 nm (298K = 25ºC) by
nearly a factor of two.32 These new values agree closely with previous best estimates based on
the average of various laboratory measurements.20
It is now realized that the quantum yield for
O(1D) production is non-zero up to at least 340
nm. While at these longer wavelengths the
product σ(λ,Τ)φ(λ,Τ) is small (Figure 6-1), this
longer wavelength dependence does reduce the
dependence of O(1D) on the amount of
stratospheric ozone.20, 22 This has resulted in
very good agreement between chemical and
spectroradiometric measurements of the
photolysis rate.33 Measurements and models of
UV actinic flux at the surface now show good
agreement.34 Similarly, measurements of OH
and chemical model predictions of OH based on
UV radiation measurements now normally agree
to within measurement accuracy in remote,
clean observation sites.35, 36 As discussed in
Chapter 1, the impact of clouds on actinic flux
can be as large.37 With such large variations,
any future changes in cloud amount due to
climate change could significantly change
photochemically induced atmospheric processes.
Actinic flux: The
photochemically active
radiation flux in the earth's
atmosphere. This flux is
spherically integrated and
is not dependent the
direction of the radiation.
Irradiance: The
radiation flux incident on
a (horizontal) surface.
Figure 6-2. Two commonly used measures of the
“intensity” of solar radiation from the sun. Both have
units of W·m-2
In air substantially affected by land, other
sources of OH have now been recognized as important, such as the photolysis of nitrous acid
(HONO) (predominantly by UV-A radiation) in both urban environments38 and in forests.39 The
wide variety of compounds present and variability of the atmospheric composition in continental
air makes modeling assessments, like those described above for clean remote sites, very difficult.
Observed changes in OH. The OH radical has a very short atmospheric lifetime and is present
in very small amounts, making direct detection of long term trends impossible. Two alternative
methods have been used to determine global trends in OH indirectly.
The main method used for OH-trend detection involves interpretation of the long-term record of
methylchloroform (Cl3C-CH3; 1,1,1-trichloroethane). Its only source is anthropogenic and the
dominant sink is reaction with OH. With a good knowledge of the source, it is possible to infer
the removal rate, and hence the amount of OH. Original estimates based on this technique
suggested that there was little change in OH since 1980.40 More recent analysis suggested
substantial changes in the amount of OH occurred during the 1990s.41 The issue of unaccounted
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169
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
emissions of methylchloroform has been raised. The magnitude of methylchloroform emissions
from landfills has been debated as a result of measurements in Europe42, 43 and the US.44, 45
Consideration has also been given to the magnitude of ocean exchange,46 which illustrates how
difficult it is to account for the complexity of the atmosphere.47 The most recent assessment,
including a consideration of these factors, indicates that OH concentrations in 2003 are very
similar to those of 1978, with the major alterations in the global OH concentration being driven
by wildfires and climatic variations.23 Global increases in the OH concentration due to
stratospheric ozone depletion48, 49 are therefore masked by other factors or are smaller than the
uncertainties of the measurements themselves.
A second method of estimating OH has recently been developed using 14CO.50 No significant
trend in OH for the Southern Hemisphere in the 1990s could be detected. Unfortunately, the data
do not extend back far enough in time to be especially sensitive to changes induced by
stratospheric ozone depletion.
A five-year study of OH at a European mountain site51 found no detectable long term trend in
OH concentration, and highlighted that, in this somewhat polluted site, there were clearly factors
that were affecting OH concentration that were not part of existing atmospheric chemical
models.51, 52 Rohrer and Berresheim51 concluded that OH concentration is essentially
proportional to J(O1D) and that scaling of OH by J(O1D), which depends on solar UV radiation,
eliminated most of the diurnal and seasonal variation, and transformed OH into a parameter with
significantly reduced variability, provided that factors dependent on local conditions are
considered.51 Rohrer and Berresheim51 proposed that regional or even global OH distributions
could be characterized by a simple set of coefficients for timescales on the order of months or
even years and suggested that this approach may be used to define an ‘OH index’ that
characterizes the oxidation efficiency of the troposphere in different chemical regimes. This
would establish a direct link between stratospheric ozone concentrations and OH concentrations
on regional scales. An overarching issue is that most of these models are based on measured
data from a limited number of locations, such as in Europe, Japan, North America, and over the
Pacific. The troposphere still remains largely under-sampled with respect to OH measurements
from the tropics (rain forests) or very large cities such as those in East Asia, key areas for the
understanding of how climate change and air quality will influence each other in the near
future.53
Global numerical models of OH in the atmosphere have advanced significantly. Three
dimensional models that include the important known atmospheric chemistry processes54 are
now being augmented with models that include atmospheric transport.55 Such models will be
useful in assessing the impacts of climate change on OH concentrations. One such study has
been carried out for the United States, which predicts an increase in OH of between 10 and 15%,
and significant increases in ozone in the eastern states.56
Observed changes in tropospheric ozone. Hydroxyl radicals (OH) are believed to be one of
the major reactive intermediates in the atmosphere. As stated earlier, the process of the
production of hydroxyl radicals couples stratospheric ozone depletion directly to tropospheric
chemistry. The chemistry of hydroxyl radicals with organic compounds can be simply
summarized in two generalized reactions:
OH
organic compounds ⎯⎯→
removal
O3
170
(4)
The Environmental Effects Assessment Panel Report for 2006
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
or
OH
organic compounds ⎯⎯→
removal + O3
NO
(5)
The distinction between the two routes (4) and (5) is the amount of nitric oxide (NO) in the
atmosphere, with the first route occurring at low NO concentrations found in remote (clean)
environments.
Estimates have been made of the impact of stratospheric ozone depletion on tropospheric
chemistry, using ground-level ozone as the primary indicator. There are two competing
processes. A decrease in stratospheric ozone will decrease the amount of ozone transported from
the stratosphere to the troposphere (as discussed earlier). Secondly, the reduction in
stratospheric ozone will lead to enhanced UV-B radiation, leading to a change in ozone due to
the photolytically driven OH reactions shown above.
Two different chemical transport models have been used, with Isaksen et al.57 calculating the
impact of a uniform 10% decrease in ozone column, and Fusco and Logan14 using the measured
stratospheric ozone amounts from 1979 and 1993. The results from Isaksen et al.57 are shown in
Figure 6-3 for both the ozone amount (left hand panels) and the change in ground-level ozone
(right hand panels). While the details of the models are quite different, the broad conclusions
they draw are similar. In clean Southern Hemispheric air, the ground-level ozone amount is
1
5
10
15
20
25
30
35
40
45
50
Amount of ozone (nmol/mol)
55
60
77
-3 -2.5
-1.9
-1.5 -1.13 -0.75 0
0.14
0.29
0.43
0.57
0.71
0.86
1.28
Change in ground level ozone (nmol/mol)
Figure 6-3. Illustration of modeled ground level ozone and the change in ground level ozone resulting from
changes in stratospheric ozone. The left hand panels show the modeled monthly average amount of ozone in
January and July. The right hand panel shows the changes calculated using a 10% decrease in total ozone column.
Figure adapted from Isaksen et al.58
predicted to decrease with decreased stratospheric ozone (Equation (4)). In the northern
hemisphere, a slight increase in ozone amounts is predicted with decreasing stratospheric ozone
The Environmental Effects Assessment Panel Report for 2006
171
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
(Equation (5)). This difference between the hemispheres is caused by the concentration of NOX
from air pollution. Some features of the modeled results differ, and the swap between ozone
removal and production would be expected at lower nitrogen oxide concentrations (e.g.58),
however, the changes estimated by the models indicate that the magnitude of the induced change
in tropospheric ozone is small in comparison with the impacts of air pollution.14, 59
The impact of likely future changes in atmospheric composition has been assessed using eleven
different atmospheric climate models, and they predicted that tropospheric ozone will increase
globally by 10 to 30 ppbv from 2000 to 2100.60 These models have ignored the impact of
changes in atmospheric circulation, and so this increase is driven by the increase in
anthropogenic emissions of gases like NO/NO2 and hydrocarbons. Stratospheric ozone recovery
is predicted to increase tropospheric ozone by a further 3 ppbv.60
Other relevant photolytic processes. Ketones such as acetone ((CH3)2CO), are present in the
atmosphere either due to direct release at the ground or as a product of the decomposition of a
range of organic compounds. They are important atmospheric trace gases,61 playing a key role in
the formation and transport of pollutants. For example, acetone can decompose via direct
photolysis or via OH, which can be abbreviated as follows:
(CH 3 ) 2 CO + OH →→ CH 3COO
⎯⎯
→ CH 3COONO2
CH 3COO + NO2 ←⎯
⎯
(6)
(7)
The product CH3COONO2 (PAN) is a well known urban pollutant but is also stable at upper
troposphere temperatures, and has been recognized as a means of long-range transport of
pollutants, such as reactive nitrogen.62
A reassessment of the direct photolysis reaction for acetone63 and for some other ketones64 has
significantly decreased estimates of their overall photolytic sensitivity (quantum yield) in the
UV-B region. The changes increase the relative importance of the UV-B region, but decreases
the calculated rate of photolysis by 80 – 90%.65 This indicates that acetone will be quite widely
distributed in the upper troposphere in both hemispheres and hence available for reaction to
produce PAN. Consequently, the reaction with OH is now understood to be the dominant loss
mechanism for acetone. When included in calculations of the global atmosphere, these changes
improve the agreement between the theoretical estimates and observations.65
The photolysis rate for formaldehyde, one of the key products of the atmospheric decomposition
of organic molecules, has been investigated. There are two different routes for decay, and the
rate of both routes will depend on stratospheric ozone. Methods for deriving the photolysis rate
from irradiance have been proposed,31 although to date such estimates have not been widely
used.
Antarctic atmosphere. Surface ozone at the South Pole is of particular interest as it lies
underneath the region of greatest stratospheric ozone depletion. An analysis of measurement
records has shown that, during November – December, there was a decrease in ground-level
ozone over the period 1970 – 1990.66 Since 1990, there has been a detectable increase in surface
ozone (up to 20%).67
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
Photolysis of ozone and NO in the Antarctic
The importance of photolysis was elegantly demonstrated by measurements of a second
peroxide, methylhydroperoxide (CH3OOH). In this clean environment, the following two
reactions represent a significant fraction of the OH reactions:
CO + OH + O2 → → CO2 + HO2
CH 4 + OH + O2 → → H 2O + CH 3OO
(8)
(9)
It should be noted that there are other reactions which produce these radicals. HO2 can then
react to form H2O2 or other peroxides:
2HO2 → H 2O2 + O2
HO2 + CH 3O2 → CH 3OOH + O2
(10)
(11)
Additional NO can permit the following reactions to become significant:
NO + CH 3OO + O2 → → NO2 + HCHO + HO2
NO + HO2 → NO2 + OH
(12)
(13)
The NO removes methylperoxide and produces HO2 (Reaction (13)). So, when UV was
enhanced the increased H2O2 was accompanied by a 20% decrease in CH3OOH.
In the clean Antarctic atmosphere, the NO concentrations would be expected to be low enough
that enhanced radical chemistry should result in a decrease in ozone (reaction (4)), as observed in
the period before 1990. The change after 1990 is attributed to the impact of additional UV
radiation on the snowpack, enhancing nitrogen oxide release.67 The extra NO produced then
alters the atmospheric reactions so that additional UV radiation enhances ozone production. This
effect is most noticeable during November when the largest absolute increase in UV radiation is
experienced.
Measurements made on the West Antarctic Ice Sheet in 2000 – 2002 showed strong evidence of
a negative correlation between stratospheric ozone and ground-level hydrogen peroxide (H2O2).
A 70% increase in surface H2O2 concentration under conditions of low stratospheric ozone (less
than 220DU compared to around 320 DU) has been observed.68 The increase in hydrogen
peroxide was explained by an enhanced photolysis of ozone and NO production (see box).
If the impact of UV radiation on NO was not included in a theoretical model, it failed to capture
the magnitude of the observed H2O2 changes.68 These changes imply that the atmospheric
boundary layer in Antarctica has become more oxidizing due to stratospheric ozone depletion.
The ecological impact of this has not been studied.
Impact of air pollution on photolysis by UV-B radiation. The transmission of UV-B radiation
to the Earth’s surface is increased by removal of stratospheric ozone. The reduction in UV-B
radiation by aerosols, and primarily carbon black from combustion has been found to be
significant.38 A global chemical transport model69 has been used to estimate the impact of
aerosols on tropospheric chemistry. Calculations of the impact of aerosols indicate that they
typically cause a 1 – 5% reduction in radiation driving O(1D) formation (UV-B radiation) in
The Environmental Effects Assessment Panel Report for 2006
173
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
general (see Figure 6-4). However, there are regions, notably in Africa, Europe and Asia where
impacts of the order of 30% or more are predicted due to increased aerosol release. The net
effects on ozone concentrations are more modest (< 5%) and are somewhat smaller than the
direct effect of reactions on the aerosol surface.
(J[O3] ->O1D Jun, Jul, Aug)
-40
-30
-20
(J[O3] ->O1D Dec, Jan, Feb)
-10
-5
-1
0
Percent change in ground-level ozone concentrations
Figure 6-4. Calculated change in ground-level ozone concentration due to the effect of aerosols on (UV-B)
photolysis. From Tie et al. 70.
Fluorinated substances
Volatile halogenated substances have an important role in ozone depletion and global warming.
Since several of these substances are used as refrigerants, there is a potential for interaction
between their use, their effects on ozone, and climate change. A number of highly fluorinated
compounds (PFCs) undergo degradation and transformation in the atmosphere and several of
these have relevance to interactions between global warming and stratospheric ozone depletion.
The ultimate degradation products are perfluorinated acids with varying chain lengths, depending
on the starting material. The mechanisms of the atmospheric transport and breakdown of longand short-chain hydrochlorofluorocarbons (HCFCs) have been well-characterized70, 71 and the
results indicate that they are not likely to form the short-chain perfluorocarboxylic acids
(PFCAs), such as trifluoroacetic acid (TFA). Perfluorinated aldehydes formed during the
atmospheric oxidation of HFCs, HCFCs, and fluorinated alcohols are transported in the
atmosphere dissolved in cloud water and react and are subsequently transported to the surface in
precipitation. This mechanism has been identified as an additional source of longer chain
PFCAs (such as of perfluorooctanoic acid), from the breakdown of fluorotelomer alcohols and
possibly explains the presence of perfluorooctanoic acid in remote regions such as the Arctic.71
These longer chain acids and their parent materials are very resistant to breakdown and have
been observed to become more concentrated up the food chain in mammals and birds,72, 73 where
they may have harmful effects.74
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The Environmental Effects Assessment Panel Report for 2006
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
In contrast to the longer chain PFCs discussed above, several of the HCFCs and HFCs can break
down into trifluoroacetic acid (TFA Figure 6-5). These are halothane, isoflurane, HCFC 123,
HCFC-124, HFC-134a, and HFC-143a. Observations in both hemispheres (Mace Head, Ireland
and Cape Grim, Tasmania) between 1998 and 2002 showed that the concentration of HFC-134a
had increased rapidly (3 picomol mol-1 year-1) equivalent to 12% year-1 based on measured
concentrations of approximately 25 picomol mol-1 year-1 measured in the troposphere at Mace
Head, Ireland in 2002.75 This increase is in agreement with the known usage and atmospheric
loss processes. As HFC-134a is a potent greenhouse gas, this increasing concentration has
implications for climate change76 as well as the production of TFA.
F
The final environmental sink for TFA is in the
F F
O
oceans and landlocked lakes. Concentrations of
F
C
C
F C C F
TFA in rainwater range from <0.5 to 350 ng L-1,
OH
F
F H
depending on location and distance from
anthropogenic activity.77 The predominant source
TFA
HFC-134a
of TFA in non-oceanic surface waters is likely
Figure 6-5. Formation of trifluoracetic acid (TFA)
anthropogenic as concentrations in surface water
from an HFC.
samples >2 000 years-old obtained from
groundwater and ice cores in Greenland were not detectable (< 2 ng L-1).78 There are probably
natural sources of TFA in seawater; relatively large concentrations have occasionally been
detected in close proximity to undersea volcanic vents.79 Concentrations up to 350 ng L-1 in
flowing surface waters have been reported from several locations.80-82 However, in landlocked
lakes, they may be as large as 40 000 ng L-1.80 Reports of TFA concentrations in oceans are
generally less than or equal to 200 ng L-179, 80, 82 and much of this appears to have pre-industrial
natural origins.83 Based on historical production84 of HFCs and HCFCs that are potential sources
of TFA as well as projections of future uses,76 an estimate of total production was made (Table
6-1). A worst-case estimate of TFA release from complete conversion of HFCs and HCFCs to
TFA produced a total of 22 x 106 tonnes of TFA. After dilution and complete mixing in the
volume of the oceans (1.34 x 1021 L), the increase in concentration above the nominal base level
of 200 ng L-1 reported by Frank et al.83 would be small (0.016 ng L-1). Even if mixing were
slow, concentrations in receiving zones would be less than those in flowing fresh waters or less
than double the nominal base concentration. Even considering other sources of TFA, the added
inputs from anthropogenic activity will be insignificant.
Table 6-1. Historical and projected production of HFCs and HCFCs in tonnes
HCFC-124
Total production as of 2003a
Estimated annual production in 2015b
Estimated total production by
2020/2040c
HFC-134a
HFC-143a
32 253
1 172 891
39 615
1 000
446 000
72 000
93 681
19 402 446
3 351 615
a
From84. b From76. c Phaseout projected for 2020 in developed countries and 2040 in
developing countries, half of the total use attributed to developed countries and half to
developing countries.
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
TFA is a strong acid (dissociation constant, pKa, = 0.3) and is completely ionised at normal
environmental pHs and is present in the environment as a salt form. It is also highly stable under
normal environmental conditions. Its stability in the environment is a direct result of the great
strength of the C-F bond and the lack of functional groups on the molecule that are susceptible to
chemical or biological degradation (Figure 6-5).
Laboratory and microcosm studies with TFA and related substances81, 85, 86 have suggested no
additional environmental hazards from current environmental loadings in fresh or salt water.
The smallest effect concentrations (EC50s) for TFA in sensitive species such as aquatic plants
ranged from 0.222 x 106 to 10 x 106 ng L-1.86 Estimates of more sensitive responses (assay
endpoints) suggested a toxic benchmark concentration87 of 0.046 x 106 ng L-1,81 which is much
greater than current81 or projected concentrations in fresh and saltwater environments. The
projected future increased loadings to the oceans from fresh water due to climate change and
continued use of HCFCs and HFCs, are judged to present negligible risks for aquatic organisms
and humans.
There is evidence that the perfluoropolyethers, substances which are proposed as chlorohydrofluorocarbon (CHFC) substitutes, have great stability to chemical degradation in the
atmosphere as well as very large global warming potential.88 Perfluoropolyethers (PFPEs) are
commonly used industrial heat transfer fluids that may be released to the atmosphere. In smog
chamber studies on a distilled fraction of a commercial mixture containing
perfluoropolymethylisopropyl ethers (PFPMIEs, Figure 6-6), reactivity of PFPMIE with Cl was
less than 2 x 10-17 cm3 molecule-1 s-1, while reactivity with OH was less than 6.8 x10-16 cm3
molecule-1s-1, indicating low reactivity in the troposphere.
Using half-life data from perfluorinated alkanes, a lower
limit for the total atmospheric lifetime of PFPMIE was
calculated to be 800 years. PFPMIE was shown to have
instantaneous radiative forcing of 0.65 W m-2 ppb-1.88 This
corresponds to a global warming potential (GWP) on a 100 Figure 6-6. Structure of a perfluoropolyyear time-frame of 9000 relative to carbon dioxide (GWP
methylisopropyl ether.
of one) and 1.95 relative to CFC-11, a value exceeded by
only a few hydrofluoro ethers.88 PFPMIE has a longer atmospheric lifetime than CFC-11, and
hence, the GWP of PFPMIE increases with the time horizon. For example, the GWP of PFPMIE
over a 500 year horizon was estimated at 6.89 relative CFC-11.88 These substances have been
suggested as substitutes for CHFCs89 but, as they are very persistent in the atmosphere, they may
be important contributors to global warming. It is not known whether these substances will
contribute significantly to global warming and its interaction with ozone depletion but they
should be considered for further evaluation.
Conclusions, uncertainties and data needs
Research has now uncovered a distinct signature in air quality due to changes in stratospheric
ozone. This is most noticeable in the Antarctic, where the change in stratospheric ozone is the
largest and there are relatively few sources of atmospheric contamination. Elsewhere, changes in
stratospheric ozone have apparent impacts on air quality, in particular ground level ozone
concentrations, which depend on the composition of the atmosphere at that location. These
conclusions are in agreement with current understanding of the chemistry of the atmosphere.
Calibration and verification data for models are frequently taken from less polluted areas in
temperate regions. Additional spatial and temporal measurements of air pollutants, OH, and
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
ozone from other regions such the tropics, forested areas, and highly polluted areas would allow
models of interactions between UV-B radiation, climate change, and air quality to be improved.
The decomposition products of CFC’s and their replacements do not appear to have a significant
environmental impact at this time. Trifluoroacetic acid is very persistent in water, but unlikely to
be found at concentrations which present a significant environmental risk. Some other highly
fluorinated compounds do have significant global warming potentials and long environmental
lifetimes, so their climate impact will need to be considered carefully.
Future impacts of variations in stratospheric ozone on air quality will depend heavily on the
magnitude of other changes to the atmosphere, driven by effects such as climate change and
increasing industrialization. The projected increase in ground level ozone due to human activities
is likely to be somewhat enhanced by recovering stratospheric ozone in the next century.
Our understanding of the atmosphere and the changes that are occurring within it are focused on
relatively small regions of the globe. In particular little is known about the tropics, partially
because of a lack of measurement but also because of the complexity of the environment. This
lack will need to be redressed.
References
1
2
3
4
5
6
7
8
9
World Health Organization, Health Aspects of Air Pollution, World Health Organization,
Regional Office for Europe Report No., Copenhagen, Denmark, June 2004, p. 30.
http://www.euro.who.int/document/E83080.pdf#search=%22ozone%20human%20health%
20review%22
European Environment Agency, Europe's Environment: The Third Assessment, European
Environment Agency Report No., Copenhagen, May 12, 2003, p. 334.
http://reports.eea.eu.int/environmental_assessment_report_2003_10/en/kiev_eea_low.pdf
Stieb DM, Burnett RT, Beveridge RC, Brook JR, Association between ozone and asthma
emergency department visits in Saint John, New Brunswick, Canada, Environ. Hlth.
Perspect., 1996, 104, 1354-1360.
Weisel CP, Cody RP, Lioy PJ, Relationship between summertime ambient ozone levels and
emergency department visits for asthma in central New Jersey, Environ. Hlth. Perspect.,
1995, 103, 97-102.
Stedman JR, Anderson HR, Atkinson RW, Maynard RL, Emergency hospital admissions
for respiratory disorders attributable to summer time ozone episodes in Great Britain,
Thorax, 1997, 52, 958-963.
Fuhrer J, Skarby L, Ashmore MR, Critical levels for ozone effects on vegetation in Europe,
Environ. Pollut., 1997, 97, 91-106.
Rinnan R, Holopainen T, Ozone effects on the ultrastructure of peatland plants: Sphagnum
mosses, Vaccinium oxycoccus, Andromeda polifolia and Eriophorum vaginatum, Ann. Bot.,
2004, 94, 623-634.
Solomon KR, Tang X, Wilson SR, Zanis P, Bais AF, Changes in tropospheric composition
and air quality due to stratospheric ozone depletion, Photochemical and Photobiological
Science, 2003, 2, 62-67.
Tang X, Madronich S, Wallington T, Calamari D, Changes in tropospheric composition
and air quality, J. Photochem. Photobiol. B., 1998, 46, 83-95.
The Environmental Effects Assessment Panel Report for 2006
177
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
178
Hofzumahaus A, Brauers T, Platt U, Callies J, Latitudinal variation of measured O3
photolysis frequencies J(O1D) and primary OH production rates over the Atlantic ocean
between 50ºN and 30ºS, J Atmos Chem, 1992, 15, 283-298.
Liao H, Chen WT, Seinfeld JH, Role of climate change in global predictions of future
tropospheric ozone and aerosols, J. Geophys. Res., 2006, 111, D12304.
Shindell DT, Schmidt GA, Southern Hemisphere climate response to ozone changes and
greenhouse gas increases, Geophys Res Lett, 2004, 31, DOI:10.1029/2004GL020724.
Pyle JA, Braesicke P, Zeng G, Dynamical variability in the modelling of chemistry-climate
interactions, Faraday Discussions, 2005, 130, 27-39.
Fusco AC, Logan JA, Analysis of 1970-1995 trends in tropospheric ozone at Northern
Hemisphere midlatitudes with the GEOS-CHEM model, J. Geophys. Res. Atmos., 2003,
108, 4449-4449.
Crutzen PJ, Lawrence MG, Poschl U, On the background photochemistry of tropospheric
ozone, Tellus Series A-Dynamic Meteorology And Oceanography, 1999, 51, 123-146.
Lelieveld J, Dentener FJ, What controls tropospheric ozone?, J. Geophys. Res. Atmos.,
2000, 105, 3531-3551.
Fishman J, Creilson JK, Wozniak AE, Crutzen PJ, Interannual variability of stratospheric
and tropospheric ozone determined from satellite measurements, J. Geophys. Res., 2005,
110, DOI:10.1029/2005JD005868.
Ramaswamy V, Schwarzkopf MD, Randel WJ, Santer BD, Soden BJ, Stenchikov GL,
Anthropogenic and natural influences in the evolution of lower stratospheric cooling,
Science., 2006, 311, 1138-1141.
Sudo K, Takahashi M, Akimoto H, Future changes in stratosphere-troposphere exchange
and their impacts on future tropospheric ozone simulations, Geophys Res Lett, 2003, 30,
DOI:10.1029/2003GL018526.
Sander SP, Finlayson-Pitts BJ, Friedl RR, Golden DM, Huie RE, Kolb CE, Kurylo MJ,
Molina MJ, Moortgat GK, Orkin VL, Ravishankara AR, Chemical Kinetics and
Photochemical Data for Use in Atmospheric Studies, Evaluation Number 14, Jet Propulsion
Laboratory Report No. JPL Publication 02-25, Pasadena, CA, USA, February 1, 2003, p.
334. http://jpldataeval.jpl.nasa.gov/pdf/JPL_02-25_rev02.pdf
Atkinson R, Baulch DL, Cox RA, Crowley JN, Hampson RF, Hynes RG, Jenkin ME, Rossi
MJ, Troe J, Evaluated kinetic and photochemical data for atmospheric chemistry: Volume I
- gas phase reactions of Ox, HOx, NOx and SOx species, Atmos. Chem. Phys., 2004, 4,
1461-1738.
Sander SP, Friedl RR, Ravishankara AR, Golden DM, Kolb CE, Kurylo MJ, Molina MJ,
Moortgat GK, Keller-Rudek H, Finlayson-Pitts BJ, Wine PH, Huie RE, Orkin VL,
Chemical Kinetics and Photochemical Data for Use in Atmospheric Studies. Evaluation
Number 15, Jet Propulsion Laboratory Report No. JPL 06-2, Pasadena, CA, USA, July 10,
2006, p. 522. http://jpldataeval.jpl.nasa.gov/pdf/JPL_15_AllInOne.pdf
Prinn RG, Huang J, Weiss RF, Cunnold DM, Fraser PJ, Simmonds PG, McCulloch A,
Harth C, Reimann S, Salameh P, O'Doherty S, Wang RHJ, Porter LW, Miller BR,
Krummel PB, Evidence for variability of atmospheric hydroxyl radicals over the past
quarter century, Geophys Res Lett, 2005, 32, DOI:10.1029/2004GL022228.
Eckstein E, Perner D, Bruhl C, Trautmann T, A new actinic flux 4 pi-spectroradiometer:
instrument design and application to clear sky and broken cloud conditions, Atmos. Chem.
Phys., 2003, 3, 1965-1979.
The Environmental Effects Assessment Panel Report for 2006
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
25
26
27
28
29
30
31
32
33
34
35
36
Hofzumahaus A, Kraus A, Muller M, Solar actinic flux spectroradiometry: a technique for
measuring photolysis frequencies in the atmosphere, Appl. Optic., 1999, 38, 4443-4460.
Kazadzis S, Topaloglou C, Bais AF, Blumthaler M, Balis D, Kazantzidis A, Schallhart B,
Actinic flux and (O 1D) photolysis frequencies retrieved from spectral measurements of
irradiance at Thessaloniki, Greece, Atmos. Chem. Phys., 2004, 4, 2215-2226.
Schallhart B, Huber A, Blumthaler M, Semi-empirical method for the conversion of
spectral UV global irradiance data into actinic flux, Atmos. Environ., 2004, 38, 4341-4346.
Kylling A, Webb AR, Bais AF, Blumthaler M, Schmitt R, Thiel S, Kazantzidis A, Kift R,
Misslbeck M, Schallhart B, Schreder J, Topaloglou C, Kazadzis S, Rimmer J, Actinic flux
determination from measurements of irradiance, J. Geophys. Res., 2003, 108,
DOI:10.1029/2002JD003236.
Webb AR, Kift R, Thiel S, Blumthaler M, An empirical method for the conversion of
spectral UV irradiance measurements to actinic flux data, Atmos. Environ., 2002, 36, 43974404.
McKenzie R, Johnston P, Hofzumahaus A, Kraus A, Madronich S, Cantrell C, Calvert J,
Shetter R, Relationship between photolysis frequencies derived from spectroscopic
measurements of actinic fluxes and irradiances during the IPMMI campaign, J. Geophys.
Res. Atmos., 2002, 107, DOI:10.1029/2001JD000601.
Topaloglou C, Kazadzis S, Bais AF, Blumthaler M, Schallhart B, Balis D, NO2 and HCHO
photolysis frequencies from irradiance measurements in Thessaloniki, Greece, Atmos.
Chem. Phys., 2005, 5, 1645-1653.
Takahashi K, Hayashi S, Suzuki T, Matsumi Y, Accurate determination of the absolute
quantum yield for O(1D) formation in the photolysis of ozone at 308 nm, J. Phys. Chem. A,
2004, 108, 10497-10501.
Hofzumahaus A, Lefer BL, Monks PS, Hall SR, Kylling A, Mayer B, Shetter RE,
Junkermann W, Bais A, Calvert JG, Cantrell CA, Madronich S, Edwards GD, Kraus A,
Muller M, Bohn B, Schmitt R, Johnston P, McKenzie R, Frost GJ, Griffioen E, Krol M,
Martin T, Pfister G, Roth EP, Ruggaber A, Swartz WH, Lloyd SA, Van Weele M,
Photolysis frequency of O3 to O(1D): Measurements and modeling during the International
Photolysis Frequency Measurement and Modeling Intercomparison (IPMMI), J. Geophys.
Res., 2004, 109, DOI:10.1029/2003JD004333.
Bais AF, Madronich S, Crawford J, Hall SR, Mayer B, van Weele M, Lenoble J, Calvert
JG, Cantrell CA, Shetter RE, Hofzumahaus A, Koepke P, Monks PS, Frost G, McKenzie
R, Krotkov N, Kylling A, Swartz WH, Lloyd S, Pfister G, Martin TJ, Roeth EP, Griffioen
E, Ruggaber A, Krol M, Kraus A, Edwards GD, Mueller M, Lefer BL, Johnston P,
Schwander H, Flittner D, Gardiner BG, Barrick J, Schmitt R, International Photolysis
frequency Measurement and Model Intercomparison (IPMMI): Spectral actinic solar flux
measurements and modeling, J. Geophys. Res. Atmos., 2003, 108,
DOI:10292002JD002891.
Creasey DJ, Evans GE, Heard DE, Lee JD, Measurements of OH and HO2 concentrations
in the Southern Ocean marine boundary layer, J. Geophys. Res., 2003, 108,
DOI:10.1029/2002JD003206.
Olson JR, Crawford JH, Chen G, Fried A, Evans MJ, Jordan CE, Sandholm ST, Davis DD,
Anderson BE, Avery MA, Barrick JD, Blake DR, Brune WH, Eisele FL, Flocke F, Harder
H, Jacob DJ, Kondo Y, Lefer BL, Martinez M, Mauldin RL, Sachse GW, Shetter RE,
Singh HB, Talbot RW, Tan D, Testing fast photochemical theory during TRACE-P based
The Environmental Effects Assessment Panel Report for 2006
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Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
37
38
39
40
41
42
43
44
45
46
47
48
49
50
51
180
on measurements of OH, HO2, and CH2O, J. Geophys. Res. Atmos., 2004, 109,
DOI:10.1029/2003JD004278.
Kylling A, Webb AR, Kift R, Gobbi GP, Ammannato L, Barnaba F, Bais A, Kazadzis S,
Wendisch M, Jakel E, Schmidt S, Kniffka A, Thiel S, Junkermann W, Blumthaler M,
Silbernagl R, Schallhart B, Schmitt R, Kjeldstad B, Thorseth TM, Scheirer R, Mayer B,
Spectral actinic flux in the lower troposphere: measurement and 1-D simulations for
cloudless, broken cloud and overcast situations, Atmos. Chem. Phys., 2005, 5, 1975-1997.
Barnard WF, Saxena VK, Wenny BN, DeLuisi JJ, Daily surface UV exposure and its
relationship to surface pollutant measurements, J Air Waste Manage, 2003, 53, 237-245.
Kleffmann J, Gavriloaiei T, Hofzumahaus A, Holland F, Koppmann R, Rupp L, Schlosser
E, Siese M, Wahner A, Daytime formation of nitrous acid: A major source of OH radicals
in a forest, Geophys Res Lett, 2005, 32, L05818, doi:10.1029/2005GL022524.
Prinn RG, Weiss RF, Miller BR, Huang J, Alyea FN, Cunnold DM, Fraser PJ, Hartley DE,
Simmonds PG, Atmospheric trends and lifetime of CH3CCl3 and global OH concentrations,
Science., 1995, 269, 187-192.
Prinn RG, Huang J, Weiss RF, Cunnold DM, Fraser PJ, Simmonds PG, McCulloch A,
Harth C, Salameh P, O'Doherty S, Wang RHJ, Porter L, Miller BR, Evidence for
substantial variations of atmospheric hydroxyl radicals in the past two decades, Science.,
2001, 292, 1882-1888.
Krol MC, Lelieveld J, Oram DE, Sturrock GA, Penkett SA, Brenninkmeijer CAM, Gros V,
Williams J, Scheeren HA, Continuing emissions of methyl chloroform from Europe,
Nature, 2003, 421, 131-135.
Reimann S, Manning AJ, Simmonds PG, Cunnold DM, Wang RHJ, Li JL, McCulloch A,
Prinn RG, Huang J, Weiss RF, Fraser PJ, O'Doherty S, Greally BR, Stemmler K, Hill M,
Folini D, Low European methyl chloroform emissions inferred from long-term atmospheric
measurements, Nature, 2005, 433, 506-508.
Millet DB, Goldstein AH, Evidence of continuing methylchloroform emissions from the
United States, Geophys Res Lett, 2004, 31, DOI:10.1029/2004GL021932.
Millet DB, Goldstein AH, Correction to "Evidence of continuing methylchloroform
emissions from the United States", Geophys Res Lett, 2004, 31,
DOI:10.1029/2004GL021932.
Wennberg PO, Peacock S, Randerson JT, Bleck R, Recent changes in the air-sea gas
exchange of methyl chloroform, Geophys Res Lett, 2004, 31,
DOI:10.1029/2004GL020476.
Krol M, Lelieveld J, Can the variability in tropospheric OH be deduced from measurements
of 1,1,1-trichloroethane (methyl chloroform)?, J. Geophys. Res. Atmos., 2003, 108,
DOI:10.1029/2002JD002423.
Bekki S, Law KS, Pyle JA, Effect of ozone depletion on atmospheric CH4 and CO
concentrations, Nature, 1994, 371, 595-597.
Fuglestvedt JS, Jonson JE, Isaksen ISA, Effects of reductions in stratospheric ozone on
tropospheric chemistry through changes in photolysis rates, Tellus Series B-Chemical &
Physical Meteorology, 1994, 46, 172-192.
Manning MR, Lowe DC, Moss RC, Bodeker GE, Allan W, Short-term variations in the
oxidizing power of the atmosphere, Nature, 2005, 436, 1001-1004.
Rohrer F, Berresheim H, Strong correlation between level of tropospheric hydroxyl radicals
and solar ultraviolet radiation, Nature, 2006, 442, 184-187.
The Environmental Effects Assessment Panel Report for 2006
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
52
53
54
55
56
57
58
59
60
61
62
63
64
65
Wennberg PO, Radicals follow the sun, Nature, 2006, 442, 145-146.
Heard DE, Free-Radicals in the Troposphere: Their Measurement, Interpretation of FieldData, and Future Directions, in Report of the Leeds Expert Meeting (Ed.: Heard DE),
Devonshire Hall, University of Leeds, Leeds, UK, 2005.
Spivakovsky CM, Logan JA, Montzka SA, Balkanski YJ, Foreman-Fowler M, Jones DBA,
Horowitz LW, Fusco AC, Brenninkmeijer CAM, Prather MJ, Wofsy SC, McElroy MB,
Three-dimensional climatological distribution of tropospheric OH: Update and evaluation,
J. Geophys. Res. Atmos., 2000, 105, 8931-8980.
Bloss WJ, Evans MJ, Lee JD, Sommariva R, Heard DE, Pilling MJ, The oxidative capacity
of the troposphere: Coupling of field measurements of OH and a global chemistry transport
model, Faraday Discussions, 2005, 130, 425-436.
Murazaki K, Hess P, How does climate change contribute to surface ozone change over the
United States?, J. Geophys. Res., 2006, 111, D05301, doi:10.1029/2005JD005873.
Isaksen ISA, Zerefos C, Kourtidis K, Meleti C, Dalsoren SB, Sundet JK, Grini A, Zanis P,
Balis D, Tropospheric ozone changes at unpolluted and semipolluted regions induced by
stratospheric ozone changes, J. Geophys. Res. Atmos., 2005, 110,
DOI:10.1029/2004JD004618.
Kondo Y, Nakamura K, Chen G, Takegawa N, Koike M, Miyazaki Y, Kita K, Crawford J,
Ko M, Blake DR, Kawakami S, Shirai T, Liley B, Wang Y, Ogawa T, Photochemistry of
ozone over the western Pacific from winter to spring, J. Geophys. Res. Atmos., 2004, 109,
DOI:10.1029/2004JD004871.
Lamarque JF, Hess P, Emmons L, Buja L, Washington W, Granier C, Tropospheric ozone
evolution between 1890 and 1990, J. Geophys. Res. Atmos., 2005, 110,
DOI:10.1029/2004JD005537.
Gauss M, Myhre G, Pitari G, Prather MJ, Isaksen ISA, Berntsen TK, Brasseur GP,
Dentener FJ, Derwent RG, Hauglustaine DA, Horowitz LW, Jacob DJ, Johnson M, Law
KS, Mickley LJ, Muller JF, Plantevin PH, Pyle JA, Rogers HL, Stevenson DS, Sundet JK,
van Weele M, Wild O, Radiative forcing in the 21st century due to ozone changes in the
troposphere and the lower stratosphere, J. Geophys. Res. Atmos., 2003, 108,
DOI:10.1029/2002JD002624.
Lary DJ, Shallcross DE, Central role of carbonyl compounds in atmospheric chemistry, J.
Geophys. Res. Atmos., 2000, 105, 19771-19778.
Roberts JM, Flocke F, Chen G, de Gouw J, Holloway JS, Hubler G, Neuman JA, Nicks
DK, Nowak JB, Parrish DD, Ryerson TB, Sueper DT, Warneke C, Fehsenfeld FC,
Measurement of peroxycarboxylic nitric anhydrides (PANs) during the ITCT 2K2 aircraft
intensive experiment, J. Geophys. Res. Atmos., 2004, 109, DOI:10.1029/2004JD004960.
Blitz MA, Heard DE, Pilling MJ, Arnold SR, Chipperfield MP, Pressure and temperaturedependent quantum yields for the photodissociation of acetone between 279 and 327.5 nm,
Geophys Res Lett, 2004, 31, DOI:10.1029/2003GL018793.
Romero MTB, Blitz MA, Heard DE, Pilling MJ, Price B, Seakins PW, Wang LM,
Photolysis of methylethyl, diethyl and methylvinyl ketones and their role in the
atmospheric HOx budget, Faraday Discussions, 2005, 130, 73-88.
Arnold SR, Chipperfield MP, Blitz MA, A three-dimensional model study of the effect of
new temperature-dependent quantum yields for acetone photolysis, J. Geophys. Res., 2005,
110, DOI:10.1029/2005JD005998.
The Environmental Effects Assessment Panel Report for 2006
181
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
66
67
68
69
70
71
72
73
74
75
76
77
78
79
182
Schnell RC, Liu S, Oltmans SJ, Stone RS, Hofmann DJ, Dutton EG, Deshler T, Sturges
WT, Harder JW, Sewell SD, Trainer M, Harris JM, Decrease of summer tropospheric
ozone concentrations in Antarctica, Nature, 1991, 351, 726-729.
Jones AE, Wolff EW, An analysis of the oxidation potential of the South Pole boundary
layer and the influence of stratospheric ozone depletion, J. Geophys. Res. Atmos., 2003,
108, DOI:10.1029/2003JD003379.
Frey MM, Stewart RW, McConnell JR, Bales RC, Atmospheric hydroperoxides in West
Antarctica: Links to stratospheric ozone and atmospheric oxidation capacity, J. Geophys.
Res., 2005, 110, DOI:/10.1029/2005JD006110.
Tie XX, Madronich S, Walters S, Edwards DP, Ginoux P, Mahowald N, Zhang RY, Lou C,
Brasseur G, Assessment of the global impact of aerosols on tropospheric oxidants, J.
Geophys. Res. Atmos., 2005, 110, 10.1029/2004JD005359.
Sulbaek Andersen MP, Nielsen OJ, Hurley MD, Ball JC, Wallington TJ, Stevens JE,
Martin JW, Ellis DA, Mabury SA, Atmospheric chemistry of n-CxF2x+1CHO (x=1, 3, 4):
Reaction with Cl atoms, OH radicals and IR spectra of CxF2x+1C(O)O2NO2, J. Phys. Chem.
A, 2004, 108, 5189-5196.
Wallington TJ, Hurley MD, Xia J, Wuebbles DJ, Sillman S, Ito A, Penner JE, Ellis DA,
Martin J, Mabury SA, Nielsen OJ, P SAM, Formation of C7F15COOH (PFOA) and other
perfluorocarboxylic acids during the atmospheric oxidation of 8:2 fluorotelomer alcohol,
Environ. Sci. Technol., 2006, 40, 924-930.
Houde M, Bujas TAD, Small J, Wells RS, Fair PA, Bossart GD, Solomon KR, Muir DCG,
Biomagnification of perfluoroalkyl compounds in the bottlenose dolphin (Tursiops
truncatus) food web, Environ. Sci. Technol., 2006, 40, 4138-4144.
Houde M, Martin JW, Letcher RJ, Solomon KR, Muir DCG, Biological monitoring of
polyfluoroalkyl compounds: A review, Environ. Sci. Technol., 2006, 40, 3463-3473.
Lau C, Butenhoff JL, Rogers JM, The developmental toxicity of perfluoroalkyl acids and
their derivatives, Toxicol. Appl. Pharmacol., 2004, 198, 231-241.
O'Doherty S, Cunnold DM, Manning A, Miller BR, Wang RHJ, Krummel PB, Fraser PJ,
Simmonds PG, McCulloch A, Weiss RF, Salameh P, Porter LW, Prinn RG, Huang J,
Sturrock G, Ryall D, Derwent RG, Montzka SA, Rapid growth of hydrofluorocarbon 134a
and hydrochlorofluorocarbons 141b, 142b, and 22 from Advanced Global Atmospheric
Gases Experiment (AGAGE) observations at Cape Grim, Tasmania, and Mace Head,
Ireland, J. Geophys. Res., 2004, 109, DOI: 10.1029/2003JD004277.
IPCC, Safeguarding the Ozone Layer and the Global Climate System. Issues Related to
Hydrofluorocarbons and Perfluorocarbons, Intergovernmental Panel on Climate Change
Technology and Economic Assessment Panel Report No., Nairobi, Kenya, April 2005, p.
88. http://www.ipcc.ch/activity/specialrprt05/IPCC_low_en.pdf
Scott BF, Spencer C, Martin JW, Barra R, Bootsma HA, Jones KC, Johnston AE, Muir DC,
Comparison of haloacetic acids in the environment of the Northern and Southern
Hemispheres, Environ. Sci. Technol., 2005, 39, 8664-8670.
Nielsen OJ, Scott BF, Spencer C, Wallington TJ, Ball JC, Trifluoroacetic acid in ancient
freshwater, Atmos. Environ., 2001, 35, 2799-2801.
Scott BF, Macdonald RW, Kannan K, Fisk A, Witter A, Yamashita N, Durham L, Spencer
C, Muir DC, Trifluoroacetate profiles in the Arctic, Atlantic, and Pacific Oceans, Environ.
Sci. Technol., 2005, 39, 6555-6560.
The Environmental Effects Assessment Panel Report for 2006
Changes in tropospheric composition and air quality due to stratospheric ozone depletion and climate change
80
81
82
83
84
85
86
87
88
89
Zehavi D, Seiber JN, An analytical method for trifluoroacetic acid in water and air samples
using headspace gas chromatographic determination of the methyl ester, Anal. Chem.,
1996, 68, 3450–3459.
Hanson ML, Solomon KR, Haloacetic acids in the aquatic environment II: Ecological risk
assessment for aquatic macrophytes, Arch. Environ. Contam. Toxicol., 2004, 130, 385-401.
Zhang J, Zhang Y, Li J, Hu J, Ye P, Zeng Z, Monitoring of trifluoroacetic acid
concentration in environmental waters in China, Water Res, 2005, 39, 1331-9.
Frank H, Christoph EH, Holm- Hansen O, Bullister JL, Trifluoroacetate in ocean waters,
Environ. Sci. Poll. Res., 2002, 36, 12-15.
AFEAS, Production and Sales of Flurorocarbons. Production, Sales, and Atmospheric
Release of Fluorocarbons Through 2003, Alternative Fluorocarbons Environmental
Acceptability Study Report No., Arlington, VA, USA, 2005.
http://www.afeas.org/production_and_sales.html
Berends AG, Boutonnet JC, de Rooij CG, Thompson RS, Toxicity of trifluoroacetate to
aquatic organisms, Environ. Toxicol. Chem., 1999, 18, 1053-1059.
Hanson ML, Solomon KR, Haloacetic acids in the aquatic environment I: Macrophyte
toxicity, Arch. Environ. Contam. Toxicol., 2004, 130, 371-383.
Hanson ML, Solomon KR, New technique for estimating thresholds of toxicity in
ecological risk assessment, Environ. Sci. Technol., 2002, 36, 3257-3264.
Young CJ, Hurley MD, Wallington TJ, Mabury SA, Atmospheric lifetime and global
warming potential of a perfluoropolyether, Environ. Sci. Technol., 2006, 40, 2242-2246.
UNEP, Case Study #16. Preparation of perfluoropolyether diols with high functionality
(difunctional molecules content 99%), UNEP, Process Agents Task Force,
http://www.unep.org/ozone/teap/Reports/PATF/PACS16R0.pdf, accessed September 19,
2005.
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Chapter 7. Effects of stratospheric ozone depletion and climate
change on materials damage.
A. L. Andradya, H. S. Hamidb, A. Torikaic
a
Engineering Technology Division, Research Triangle Institute, 3040 Cornwallis Road, Durham,
NC 27709 USA
b
King Fahd University of Petroleum and Minerals, Dhahran 31261, Saudi Arabia
c
Materials Life Society of Japan, 2-6-8 Kayabacho Chuo-ku, Tokyo, Japan
Summary
Nanoscale inorganic fillers with average particle sizes smaller by an order of magnitude or more
compared to those of conventional fillers are becoming commercially available. The efficacy of
these fillers used in polymer formulations and particularly their effect as photostabilizers are
beginning to be investigated. These may enhance or retard photodegradation depending on the
surface coating of the particles or their chemical nature. Some recent data indicate their use as
effective photostabilizers in some common polymers. However, the potential deleterious
interaction of the nanoscale fillers with other additives in the formulation has also been pointed
out. Depending on the efficiency of stabilization and the economics of their use nanofillers may
provide a useful route to UV-stabilization of plastics and rubber used outdoors. Insufficient data
are available at this time to assess their potential impact on material and coatings stabilization.
Organic fillers such as lignocellulose continue to be investigated for outdoor applications. Their
cost advantage makes them attractive despite the somewhat reduced engineering properties of
their composites. Recent reports, however, suggest the photostability of these composites to
depend on the source of fiber as well as the processing techniques employed in fabricating
products from them. Identification of the key determinants in terms of species, isolation and
processing of polymer/wood composites is critical to developing them for long-term outdoor use.
Efforts are continuing on the synthesis of new light stabilizers, particularly those based on a
hindered amine light stabilizers (HALS), and on identifying synergistic combinations of known
stabilizers for common thermoplastics. Variants of HALS-type stabilizers that reduce the loss of
stabilizer via leaching or migration were recently reported. Studies on the permanence of the
stabilizers themselves when exposed to solar UV wavelengths have also been reported in recent
work. Identification of relevant mechanisms is important not only to understand the interactions
of climate changes and higher UV solar environments with materials damage, but also to guide
future design of light-stabilizers.
Introduction
Most of the naturally-occurring biopolymers such as wood, hair, wool, and proteins as well as
synthetic organic polymers (plastics and rubber) absorb solar UV radiation and consequently
undergo photodegradation. About a third of the plastic produced in North America and in
Europe is used in building applications. These products such as siding, exposed pipes, glazing,
cable coverings, extruded window frames or doors, and in organic protective coatings (See Table
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Effects of stratospheric ozone depletion and climate change on materials damage
7-1). A majority of these polymers (mainly PE, PP, PVC, PC) are inherently photolabile
materials, slowly losing their desirable physical and mechanical properties on routine exposure
to solar UV radiation.
Initially, the photodegradation may result in uneven surface discoloration of the product, but
extended exposure invariably leads to loss in key mechanical properties such as strength or
impact resistance of the material. A large body of research data exists on the types and rates of
light-induced damage suffered by different classes of polymers and their numerous formulations.
Plastics products are almost never made from pure polymer resin; a number of additives
including inorganic reinforcing fillers, thermal stabilizers, antioxidants, flame retardants,
colorants, lubricants, processing aids and even biocides are mixed with the pure polymer to
obtain a formulation used to fabricate a product. The chemical make-up of the formulation is
dictated by the engineering requirements of the product and the environment in which the
product is expected to function. As each of the additives can potentially alter the photosusceptibility of base polymer markedly, the database on the effects of UV radiation on various
polymer materials and their formulations is voluminous. The natural biopolymers, on the other
hand, have fixed chemical compositions and their photodegradation chemistry is less variable
with the source of material.
Table 7-1. Plastics Commonly Used in Outdoor Applications.
Plastic Type
Abbreviation
Outdoor Applications
1. Polyethylene (HighHDPE, LDPE
density and Low-density)
Irrigation pipes, water storage tanks,
greenhouse film, outdoor furniture,
artificial turf.
2. Polypropylene
PP
Artificial turf, outdoor carpet, stadium
seating, outdoor furniture, cable covering,
toys.
3. Poly(vinyl chloride) and
Chlorinated poly(vinyl
chloride)
PVC, CPVC
Rigid pipes for potable and waste water,
Extruded window and door frames,
Siding and gutters, Conduits and cable
covering, Roofing membrane, Roofing
membrane, coated fabric for tents.
4. Polycarbonate
PC
Glazing, outdoor lighting applications.
5. Copolymers of ethylene
and propylene
EPDM
Single-ply membrane roofing.
6. Acrylic polymer
PMMA
Glazing material.
7. Fiber-reinforced plastics
FRP
Roofing panels, water tanks, pipes.
Outdoor applications of most common plastics are possible only because of the commercial
availability of efficient light stabilizers that can be incorporated in their formulations. Light
stabilizers remain the fastest growing segment of the plastics additives market (growing at 611% per year). The most used of these are the hindered amine light stabilizers (HALS), a class
of remarkably efficient radical scavengers that suppress light-induced degradation in polymers.
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A second important group consists of UV absorbers that absorb the damaging UV-B radiation
reaching the surface of material and convert it into thermal energy. Either of these stabilizer
compounds is typically used at very low concentrations (0.5-1.0% w/w) in the polymer
formulation and delivers a defined minimum service life for products regularly exposed to
sunlight during use. As it is often the most expensive component in the polymer formulation,
R&D effort by industry is focused on improving stabilizer effectiveness and on discovering more
potent stabilizer varieties.
An inevitable consequence of stratospheric ozone depletion has been an increase in the UV-B
component in solar radiation reaching the earth’s surface. This would be expected to accelerate
the light-induced degradation reactions in some materials, especially plastics used outdoors
routinely, reducing their service life. The projected average increase in ambient temperatures
from global warming is only 1.5-4.0 °C over the period 1990-20021, too small to cause a
significant increase in materials degradation rates; however, a much larger increase in
temperature that can significantly increase degradation rates is expected in some geographic
regions. In those regions where both higher ambient temperatures and higher UV-B levels occur
together, the degradation rates for materials will be considerably accelerated, further shortening
the useful life of materials. The relationship between the rate of reaction and the absolute
temperature is exponential; a small change in temperature can therefore result in a large increase
in the rate of degradation reactions, for reactions of low activation energy. Other climatic factors
such as rainfall, humidity, tropospheric ozone, and air pollutants further exacerbate the situation
contributing to an even faster rate of degradation of materials exposed outdoors. Some of these
worst-affected geographic regions are likely to include developing countries that rely heavily on
low-cost plastic products in their economy (for instance China is the second largest producer of
plastics in the world). This will also be true of developing countries where wood is extensively
used in housing construction. Table 7-2 summarizes the qualitative impact of these factors on
the light-induced damage to plastics and wood materials.
Table 7-2. The effect of climatic variables on light-induced degradation of materials.
Increase in
Solar UV
Increase in
Temperature
Increase in
Humidity
Increase in
Pollutants**
Polymer
++++
+++
+
+
Wood
+++
++
+++
+
** Particularly sulfur and nitrogen oxides and ground level ozone.
The number of + symbols indicate the availability of publications supporting the effect of the particular
climatic variable in increasing the light-induced degradation of the material. ++++ =Very High. +++ =
High ++ = Moderate + = Low
The challenge to the plastics industry will then be to devise strategies and innovative
technologies that allow the service life of the UV-sensitive materials to be maintained at the
currently accepted levels despite a potential increase in the solar UV-B component. A simple
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Effects of stratospheric ozone depletion and climate change on materials damage
and possibly effective solution assumes that HALS and other stabilizers in use today used at
higher concentrations will turn out to be effective in UV-B-rich solar environments.
Thus, increased concentration of these same stabilizers in polymer formulation or in wood
coatings is likely a practical mitigation strategy. While it is a reasonable strategy, the efficacy of
the existing light stabilizers with UV-rich solar radiation resulting from ozone layer depletion
has not been fully demonstrated. A second feasible response might be to substitute photosusceptible materials currently in use with better UV-resistant polymers or surface-modified
wood products. Either response will add to the cost of the material and the products. Estimates
of the global costs associated with either of these strategies are not available at this time. Such
estimates need to be based on realistic assessments of materials damage and require the use of
advanced damage estimate methodologies as well as the likely efficacy of the various mitigation
options available. The research data that allows a rigorous assessment of either of these is
unfortunately not available at the present time.
Techniques for assessing light-induced degradation
Quantifying the photodamage associated with the exposure of a polymer material to solar
radiation generally requires a knowledge of; a) the wavelength dependence of sensitivity of the
material to the particular type of damage of interest; b) a dose-response relationship that is
applicable to the exposure and deviations from the reciprocity law applicable to that
photodegradation processes; and c) the validity of assumptions of additivity of damage at
different wavelengths and the validity of the reciprocity law for the system of interest. Data for
wavelength dependence of sensitivity (in the form of either plots of sensitivity vs. wavelength2 or
as activation spectra 3 for several key polymer materials have been published. Only very limited
information is available on dose-response relationships of relevant materials for modes of
photodamage of interest. New analyses and findings on any of these critical topics therefore
contribute to better and more complete damage estimates. Recent literature, however, continues
to be sparse on new data on wavelength or dose-response relationships for hitherto
uninvestigated systems.
A critical review was recently published on the reciprocity relationships in materials
photodegradation.4 The reciprocity law is the relationship between irradiance I (photons.cm-2),
exposure duration t (hours) and the resulting photodamage obtained in an exposure experiment.
In instances where the law holds, the quantity (I.t) is directly proportional to extent of damage,
implying that a short exposure at high intensity and a longer exposure at a correspondingly low
intensity to yield the same amount of materials damage. Even where the reciprocity law
generally applies, deviations are expected at both very high and very low irradiance. When
deviation is observed at moderate irradiance, a modified form of the reciprocity rule, extent of
photodamage is proportional to(Ip.t). A compilation of available data on materials
photodegradation reported the value of p~0.9 to 1.0 for a majority of polymers for which data
were available4, confirming that reciprocity is a reasonable assumption for most materials.
Over the years, research on light-induced damage to polymers and wood have consistently relied
on fairly modest analytical techniques, mainly conventional spectroscopy for functional group
analysis, surface color measurements, and mechanical property measurements.5 However, these
continue to provide new insights as illustrated by the Fourier Transform Infrared Spectroscopy
(FTIR) study on acrylic coatings6 for which material in which a square root dependence of
damage on UV irradiance was recently reported.7 Saron and Felsiberti8 demonstrated the use of
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dynamic mechanical analysis (DMA) and FTIR in comparing the surface versus bulk
degradation of polymer blends. While providing valuable information, these techniques have
limited sensitivity, especially in monitoring early stages of photodegradation.
Recent years have seen a trend towards the use of sophisticated techniques for monitoring lightinduced damage. The application of these will allow more accurate damage estimates to be
identified and also help in designing more potent light stabilizers. Several interesting examples
are discussed below; it is the novel application of the techniques for photodamage studies rather
than individual finding from a particular study that is more relevant to the present purpose.
Laser scanning confocal microscopy (LSCM), an ideal technique to study changes in bulk as
well as surface of samples was used in a recent study on photodegradation of acrylic coatings9.
The LSCM technique is likely to be used more commonly in future studies and may allow nondestructive and accurate degradation profile studies via optical sectioning. Infrared attenuated
total reflection methods continue to be used over the years in studying depth profiles resulting
from degradation of polymers. Work by Nagai et al.10 and others11-15 illustrate the value of this
conventional technique in establishing the existence of a layered degradation profiles in plastic
materials. A highly degraded layer just below the surface of the polymer was observed in their
studies.
A second new technique used in analysis of photodegraded materials is atomic force microscopy
(AFM) and the related probe microscopic techniques. AFM nanoindentation technique was
recently used to study changes in surface hardness of fiber-reinforced vinyl ester composites.12
This technique has particular merit in studying the newer nanocomposite materials with
nanoscale fillers that are below the size limit amenable to optical microscopy. Positron
annihilation spectroscopy (PAS), a sensitive technique of analysis for physical defects at a
microscale, has been previously employed to study the photodamge to polymers. In the recent
study on epoxy polymer16 a correlation between physical defects and chemical defects (from
electron spin resonance (ESR) spectroscopy) in the degraded polymer was demonstrated for the
first time. ESR is the more common technique used in recent degradation studies17, 18 and the
observed correlation with PAS suggests that ESR data may have additional value in shedding
some light on degradation induced changes in polymer morphology. Advances are also being
made on ESR methods; 2-D ESR imaging was used by 18 in and other11 studying the depth
profile of degradation in HALS-stabilized polymers.
Also reported recently was a study on surface photooxidation of poly(ether sulfone) under UV-B
irradiation using x-ray photon correlation spectroscopy (XPS) to study the evolution of –SO3H
groups on the polymer surface.19 In general, use of advanced surface spectroscopic methods
(such as XPS) is important as photo-induced changes initiate at the outer surface of the polymer
and propagate inwards. Increased use of these highly sensitive techniques to probe
photodegraded polymer surfaces is an encouraging development.
Effect of fillers on photodegradation
In fabricating building materials and other products where superior and durable mechanical
properties are important, plastic materials are generally compounded with reinforcing fillers such
as carbon, or glass fiber. These polymer composites with inorganic inclusions in the polymer
matrix have dramatically improved properties such as the modulus and compressive strength.
Even with other categories of plastics products, non-reinforcing fillers such as calcium carbonate
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Effects of stratospheric ozone depletion and climate change on materials damage
or rutile titanium dioxide (titania) are typically used either as an opacifier or as a lower-cost filler
(relative to polymer) to reduce overall cost of the product. Fillers account for more than 50
percent of the global plastics additives market. Invariably, it is the UV stability of the plastic
formulation that determines the service lifetime or the cost of maintaining a useful lifetime of a
product used outdoors under increased UV-B levels. Therefore, it is important to review the
impact of novel additives including fillers on the service life of plastic compounds under routine
exposure to solar UV-B radiation.
The use of fillers can significantly affect the UV-induced degradation of a polymer material; for
instance, in rigid PVC compounds, it is the titania (TiO2) added to the formulation that is
responsible for its UV resistance and its outdoor lifetime. Titania is the most widely used white
pigment in coating formulations. A compounded polymer is a mixture of a number of chemical
additives and interaction of fillers with any of these may lead to unexpected effects. Nonpolymer components of the formulation may also be degraded by interaction with an additive.
For instance, with plasticized PVC/TiO2 system exposed to solar radiation, the titania protected
the PVC from degradation but promoted the photodegradation of the phthalate plasticizer in the
formulation. Outdoor lifetime of the formulation was therefore significantly reduced.20 Inert
fillers that do not chemically participate in the photodegradation reactions, tend to improve the
photostability of polymers by shielding underlying polymer from UV exposure.
Experimental data that are in line with the already-established detrimental effect of common
additives such as flame retardants21, recycled plastics 22, copolymers23, and crosslinking agents24
were reported in recent studies. Of particular interest is the better elucidation of the mechanism
involved in the deactivation of hindered amine type light stabilizers (HALS) in polyolefins due
to the presence of an aromatic brominated flame-retardant additive in the same formulation.25
Photodegradation of the retardant liberates hydrogen bromide that, in turn, reacts with the HALS
to convert the active stabilizer into its inactive ammonium salt reducing the service life of the
polymer.
Lignocellulose fillers: The use of wood- or fiber-filled polyolefin composites in outdoor
applications is not a new technology but is presently increasing in popularity26. In 2006 an
estimated 500,000 tonnes of wood-plastic composites will be used in building products in North
American markets.27 Wood fibers in general have mechanical properties that allow the design of
composites for less-demanding applications and often provide a cost advantage compared to the
common inorganic fillers. Recent studies on lingo-cellulose natural fiber fillers suggest that
these fillers can either increase or decrease the photostability of polymer composites containing
them, depending on the origin of the fiber and the weight fraction of filler used. An important
variable in these studies is the processing technique used to fabricate the composite product (i.e.,
injection molding or extrusion) that very significantly influences its weatherability.28 For
instance, wood shavings and kenaf fibers (49% by weight) were found to enhance the
photostability of polyethylene composites.29 A similar result was reported for the
polypropylene/palm-derived fiber composites.30 Lignin filler in natural rubber formulations was
found to exert a stabilizing effect.31 The palm-derived fibers at 10-40% by weight in
unplasticized PVC were reported to increase the light-induced discoloration of the composite but
left the mechanical properties unchanged on extended exposure to laboratory accelerated
weathering.32
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Deglise and Beatrice33, however, reported the wood filler to reduce the photostability of HDPE
composites with the acceleration of photodamage proportional to the volume fraction of wood
used in the composite material. Studies on injection-molded samples of a similar composite also
showed a similar result increasing photodegradability as measured in terms of discoloration as
well as loss in mechanical properties.34 Data reported35 for PP composites with 25 and 50% w/w
wood fiber are also in agreement with the above. This discrepancy in the findings is likely due
to differences in the composition of the fibers (and therefore on source of fiber) used in the
composites. The chromophores in lignin component of wood fibers absorb of solar UV-B
wavelengths making the composites susceptible to photodegradation.36 Photodegradation of
lignin results in the formation of deep yellow degradation products, mainly paraquinone
chromophores, via a series of reactions called the phenoxy quinone redox cycle. The brightness
reversion of mechanical pulps that contain a lignin fraction is well documented37, 38 and recently
reported for bleached chemi-mechanical pulps.39 The energy absorption and transfer
characteristics depend on the chemical make-up of the fiber (especially the lignin and extractives
content. The fraction of fiber in the composite determines the fraction of wood exposed at the
surface layers of polymer where UV-B absorption can take place and may also play a role in
determining photodegradability of a molded product. Composites of PP/cellulose, already
photodegraded by exposure to UV-B was found to enhance the subsequent biodegradability of
the material. This confirms earlier findings of similar effects for other composites and is
possibly due to increased surface hydrophilicity of the photodegraded composites.40
Both wood and wood-plastic composites can be protected from photodegradation by using
HALS and UV absorber additives.41 Muasher and Sain42 studied the efficacy of various such
additives for hardwood powder/HDPE composites and concluded that high molecular weight
diester HALS (used either alone or with a benzotriazole UV absorber for synergistic protective
effect43) was the most effective in controlling fading and yellowing of the material on exposure
to UV radiation.
Nano-scale fillers: There is growing trend in using nanostructured versions of conventional
inorganic fillers in plastic composites. While of similar chemical composition, the nanoscale
fillers have an average particle size of only a several tens of nanometers compared to the particle
size of hundreds of nm in conventional fillers. The surface area of the nanofillers, however, may
be as high a hundred m2 g-1 of material. The higher surface area allows more extensive interface
interactions between the polymer matrix and nanoparticles, resulting in better mechanical
properties in the nanocomposite at much lower filler content (therefore at a lower cost as well).
Therefore, nanopowdered pigments such as rutile TiO2, monmorillonite clays, fullerenes, and
single-walled carbon nanotubes (SWCN) are being explored as the next generation of reinforcing
filler materials. The use of nanofillers in composite applications is expected to grow rapidly in
the coming years. Nanoclay masterbatches (or concentrates) designed for automotive
applications are already on the market and provide significant cost-savings when used in place of
conventional fillers. Nanoclays are also useful in making polymer alloys of normally
incompatible polymers (e.g. PP and PS); these are already being used in automotive interior
applications. In some plastics, such as copolymers of ethyl vinyl acetate or PP compounds, as
little as 3-5% of nanoclay can impart acceptable flame retardancy. This avoids the compounding
problems, environmental issues, and interference with HALS components, encountered with the
use of brominated flame retardant additives referred to earlier. Recent data also suggest
nanoscale pigments may act synergistically with conventional light stabilizers.44 The paucity of
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191
Effects of stratospheric ozone depletion and climate change on materials damage
research literature on UV-induced degradation of nanocomposite at this time allows only an
initial limited assessment of their potential impact on UV-induced degradation of the polymer
composites.
Several studies illustrate the effect of nanofillers in increasing the photodegradability of
polymers. Larger surface area interacting with substrate results in increased generation of free
radical initiator species that in turn increase rates of photoreactions. Qin et al.45 working with
PE/nanoclay MMT composites found the nanofiller to enhance photodegradation of PE as
assessed by spectroscopy. However, the effect depends upon the ionic composition of the filler;
and the ammonium ion associated with the exfoliated nanoclay, and may not be generic to the
nanomaterial itself.46 By selecting a photocatalytic nanofiller a rapidly photodegradable plastic
formulation can be obtained; mixing nanoscale anatase titania (a photocatalyst) with polystyrene
was reported to increase the rate of photodegradation of the polymer.47
Nanofillers as light stabilizers: In general opacifiers such as coated titania filler to enhance the
light stability of polymer such as PVC by shielding the polymer from UV radiation48. Nano-scale
fillers now becoming commercially available have much smaller particle sizes and therefore
considerably larger surface area available for interaction with radiation. Nano-sized TiO2, for
instance, has an average particle size of about 15 nm and an average surface area of ~100 m2g-1
as opposed to conventional TiO2 of particle size of size ~300 nm and surface area of 8 m2 g-1.
Light shielding capability at the same volume fraction of filler increases as the particle size
decreases (See Figure 7-1) provided the filler is well dispersed n the matrix. With nano-anatase
form of titania, large surface area per unit mass lead to rapid catalytic oxidation of coating
formulations (based on alkyd and acrylic polymers) compared to conventional fillers; with the
coated rutile nanoparticles, however, effective light stabilization in acrylic and alkyd paint media
compared to conventional light stabilizers
was observed.49
UV-RADIATION
The opacifier nanoparticle structure of
rutile form of titania consisting of a rutile
core, aluminum oxide surface coating, and
organic top coating was similar to that for
conventional rutile filler. Composite of
polypropylene with ZnO nanoparticles
also showed stabilization against UVinduced degradation with stabilizer
effectiveness increasing with filler
Conventional opacifier
Small-particle opacifier
content50. Model epoxy polymer films
with nano-rutile titania was found to show Figure 7-1. Improved light shielding by the same volume
fraction small particles compared to large particles of an
UV-stability in accelerated laboratory
opacifier in a polymer matrix
exposure46; the protective effect varied
with the volume fraction of nanofiller in the composition. A particularly efficient
photoprotective layer for use as a coating on high-performance textile fibers was made by
dispersing 25-70 nm nanoparticles of ZnO or TiO2 in an acrylic polymer.51 The same can be
achieved with thermoset polymers with ~5 wt percent of ZnO nanoparticles to obtain a coating
that is curable, as recently disclosed in a US patent application. The protective base coat or a
surface clear coat of the polymer containing metal oxide nanoparticles can be used as a
protective coating on a variety of products.52
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Effects of stratospheric ozone depletion and climate change on materials damage
Substituting of nanoscale opacifying fillers for conventional fillers in commercial plastics
formulation should in theory lead to more efficient photostabilization. Adequate data are not
available as yet on the performance of these in commercially relevant formulations. Preliminary
data on weathering of LDPE plastic films by Commonwealth Scientific and Research
Organization, CSIRO , shows synergistic photostabilization by ZnO (1-2 phr) nanoparticles and
HALS (0.3-0.4 phr) in LDPE films.44 This is not unexpected as similar synergism between
HALS and carbon black is known for polyethylenes weathered outdoors. A recent report claimed
ZnO nanoparticlulate fillers can in polyolefins display photostabilizer activity exceeding that of
HALS compounds.53 For model liquid systems (e.g. cumene) undergoing thermal as opposed to
photo-oxidation, however, Zeynalov et.al.54 found the effectiveness of a common phenolic
antioxidant to decrease when nanosized filler particles were used. The mechanism of increased
initiation via catalysis of hydroperoxide decomposition is common in photooxidation of
polymers. Therefore it is not clear whether the nanofiller materials will consistently act as
stabilizers in the presence of other plastics additives. More data are needed before a final
assessment of the value of nanomaterials as photostabilizers can be made.
The preliminary research findings suggest that in some polymer formulations nanoscale filler
materials can yield superior mechanical performance as well as UV-B protection in polymer
composites are particularly relevant to this discussion. Assuming the availability of low-cost
nanofillers with volume production, assuming more efficient photostabilization, this emerging
technology may provide a lower-cost route to maintaining service lifetimes unchanged despite
any possible increase in the solar UV-B fraction.
Recent Developments in HALS
The most effective (and expensive) light stabilizers for common plastics intended for outdoor are
the HALS additives used in concentrations of less that 0.6% (of the polymer). Figure 7-2
illustrates the role of HALS in reacting and removal of free radicals from the oxidizing polymer.
Efficient UV light absorbers are also used where the molecule is able to absorb the high-energy
UV-B wavelengths and convert these into thermal energy. In addition to the light-stabilizers,
plastic compounds generally include a thermal stabilizer package that protects the material from
thermal and thermooxidative degradation
UV-radiation
primarily during processing.
Polymer materials
Oxygen
Potential new light stabilizers continue to be
R55
reported from time to time. Synergistic
combinations of different HALS compounds
R
R
R
as well as HALS/UV absorber combinations
have been reported to obtain even higher
levels of photostabilization43, 56 and
N
N
N
consequently longer service lifetimes.
1
O
R
O
R
Mixed filler system of titania with
conducting carbon black was also reported
ROO
to enhance the photostability of injection
UV-radiation
Polymer materials
molded poly(propylene-co-ethylene)
Oxygen
57
polymer. As they act via different
Figure 7-2. Mechanism of HALS action in removing free
mechanisms and this is to be expected. The radicals from photodegrading plastic materials.
search for better and lower cost light
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193
Effects of stratospheric ozone depletion and climate change on materials damage
stabilizers and polymer types that are inherently photostable in sunlight is an on-going process,58-
60
A particularly important consideration in the selection of light stabilizers for wood or plastic
materials is the permanence of the stabilizer itself especially under higher intensities of UV-B
irradiation. Conceptually, the light stabilizer is slowly depleted on exposure either due to slow
leaching out of the plastic or due to photochemical breakdown by UV-B. Leaching losses are
significant and was recently modeled.61 As light initiated oxidation begins the mechanical
properties of interest deteriorate with further exposure (see Figure 7-3).
Chemical changes
Loss in Property (%)
The most popular stabilizers
belonging to HALS category are not
STABILIZER LOSS
ONSET
DEGRADATION
used up in the stabilization reactions
100
but are regenerated within the
polymer, and an important route to
Useful life of product
their loss is via their own degradation.
Structural changes undergone by
HALS exposed to UV radiation in a PP
matrix were investigated using a new
reactive thermal desorption gas
chromatographic (RTD-GC) method.21
0
The kinetics of HALS loss and the
Duration of Exposure to Solar UV Radiation (Logarithmic Scale)
build up of nitroxyl radical during
exposure to UV were reported and the Figure 7-3. Conceptual representation of the onset of degradation
reaction with the loss of light stabilizer in a photostabilized plastic
data help in better modeling of the
material.
kinetics of HALS depletion or
deactivation on exposure. Chemically affixing the light stabilizer entity on to the polymer chains
to improve their permanence by reducing losses via migration to surface62 has been reported. An
interesting HALS type molecule that is also linked to a blue-emitting fluorophore molecule was
recently claimed to be a ‘one-step’ fluorescent brightner and a light stabilizer compound63 In
specialized applications where brightening is important, as in textile or paper substrates, the
additive may have considerable advantages over conventional technology. Singh et.al.64
Reported the synthesis of a novel HALS-type polymeric stabilizer and demonstrated its
effectiveness on high-impact polystyrene to be superior to that of conventional light stabilizers.
This improvement is likely a result of reduced leaching of stabilizer from the matrix.
An interesting HALS molecule also containing a UV absorber moiety was recently
synthesized.65 In clear-coat formulations this stabilizer was shown to photograft itself onto the
polymer on exposure to UV and result in reduced migration. Pickett et al66 discussed a kinetic
scheme for delamination of coatings stabilized with UV absorbers that allows better prediction of
their service life on outdoor exposure. The approach is superior to the simpler approach of using
zero- or first-order kinetic expressions hitherto used. When used in conjunction with HALS in
UV-cured polyurethane coatings, Decker67 found UV absorbers to maintain their effectiveness
after 4800 h of accelerated exposure in weather-Ometer.
Processing for photostability
A protective cap layer has been used in the past with PVC polymers as an approach to protection
from light-induced damage. A thin adhering surface layer containing high levels of the opacifier
194
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Effects of stratospheric ozone depletion and climate change on materials damage
coextruded on the surface of a PVC product to protect the underlying less-stabilized polymer
from photodamage was reported decades ago. Most of the 23 million tonnes of vinyl plastics
produced globally each year is used in building or other outdoor applications. Any reduction in
the levels of opacifier, rutile titania, used to stabilize the rigid PVC formulations used in building
products is therefore of particular interest. .
A recent patent application68 proposes the use of a cap layer of weather resistant
polyethyleneterphthalate glycol (PETG) coextruded on PVC, CPVC, high-impact polystyrene or
other common plastics. Decker et.al. reported a similar technique for PVC, where a UV-cured
highly-photostabilized protective acrylic layer was adhered to the surface of a vinyl product to
improve its weatherability.69 The acrylic clear coat carried UV absorbers as well as HALS and
the composition showed improved surface properties such as abrasion resistance. The approach
is similar to the use of acrylic surface coatings (stabilized with nanofillers) to coat high-value
industrial fibers to photostabilize them better.51 The same concept, but using a polymerizable
surface coating with a high level of UV absorber (benzotriazoles) intended for protection
products from light-induced damage was disclosed in a recent patent application.70
Conclusions and gaps in knowledge
The recent research findings reviewed here focus primarily on the effects of plastics additives,
particularly the fillers and flame retardants, on the UV stability of the polymers routinely
exposed outdoors during use. Natural fiber-based fillers (lignocelluloses) in polyolefin
composites may either increase or decrease photostability of the resin depending on the origin of
fiber and the processing technique used. As the mechanical properties of these composites appear
to be adequate for some applications, information on which sources of wood fiber enhances
polymer photostability will be useful to the industry, particularly in developing countries. With
future availability of such information, wood-fibers may contribute to low-cost photostable
composites that can function in high-UV solar radiation environments with minimal help from
conventional stabilizers.
Nanoscale fillers where the particle size tends to be <100 nm is seen to be emerging as a
replacement for the conventional fillers. They are effective as reinforcing fillers at lower
concentrations and are therefore cheaper to use. In addition, in early studies some nanoscale
fillers appear to impart antioxidant effects, photostability, and flame retardancy to the composite.
The very high surface area of UV-absorbing nanoparticle oxides, for instance, also delivers
superior photostability to the composites. Only a few publications of preliminary data are
available on the topic at this time, but these novel fillers can evolve into an important class of
polymer additive in the short term. Their superior light stability suggests widespread availability
of nanofillers able to mitigate the effects of increased solar UV at relatively lower levels of use
in plastics formulations (or in wood coatings). However, the interaction of nanoparticle fillers
with plastics additives used in the formulations remain to be elucidated.
Numerous studies using very sensitive analytical techniques (some for the first time) have
contributed to better mechanistic understanding of the chemical and physical changes in surface
and bulk of photodegrading plastics and wood materials. These contribute towards a better
understanding of light stabilizer – additive interactions as well as the mechanisms of
antioxidation in polymers. Such information is invaluable in synthesizing novel photostabilizers
and in designing UV-resistant plastics formulations.
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Effects of stratospheric ozone depletion and climate change on materials damage
The chemistry of interactions between various constituents (including the polymer itself) in
plastic formulations exposed to solar UV radiation is poorly understood. This lack of
quantitative information makes it difficult to predict the photodamage to a given formulation
exposed to solar UV radiation, and therefore does not permit designing new formulations for
specified lifetimes under different UV scenarios. A better understanding of how the different
climatic factors interact with UV environments in modifying photodamage to materials is
needed. Particular important is extending existing mechanistic and predictive models on polymer
photodamage to include the effect of changes in ambient temperature, humidity, and air
pollutants, all known to impact the photodamage process in biopolymers (especially wood) and
plastics.
References
1
2
3
4
5
6
7
8
9
10
11
12
13
196
IPCC, Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the
Third Assessment Report of the Intergovernmental Panel on Climate Change., Cambridge
University Press, Cambridge, UK, 2001.
Torikai A, Wavelength sensitivity of polymers., in Handbook of Polymer Degradation, 2
ed. ed.: Hamid SH, Marcel Dekker, New York, 2000, pp. 573-804.
Searle ND, Activation Spectra of Polymers and Their Application to Stabilization and
Stability Testing, in Handbook of Polymer Degradation, 2 ed. ed.: Hamid SH, Marcel
Dekker, Inc., New York, NY, USA, 2000, pp. 605-643.
Martin JW, Chin JW, Nguyen T, Reciprocity law experiments in polymeric
photodegradation: A critical review, Prog. Org. Coat., 2003, 47, 292-311.
Fechine GJM, Rabello MS, Major RMS, Catalani LH, Surface characterization of
photodegraded poly(ethyleneterephthalate). The effect of UV absorbers, Polymer, 2004,
45, 2303-2308.
Ding SH, Liu DZ, Duan LL, Accelerated aging and aging mechanism of acrylic sealant,
Polymer Deg. Stab., 2006, 91, 1010-1016.
Christensen PA, Dilks A, Egerton TA, Temperley J, Infrared spectroscopic evaluation of he
photodegradation of paint. Part II: The effect of UV intensity and wavelength on the
degradation of acrylic films pigmented with titanium dioxide, J. Material. Sci., 2000, 35,
5353-5358.
Saron C, Felisberti MI, Dynamic mechanical spectroscopy applied to study the thermal and
photodegradation of PPO/high-impact polystyrene blends., Mat. Sci. Eng. A, 2004, 370,
293-301.
Cu X, Jasmin J, Martins JW, Nguyen T, Sung L, Use of laser scanning confocal
microscopy for characterizing changes in film thickness and local surface morphology of
uv-exposed polymer coating, JCT Res., 2004, 1, 267-276.
Nagai N, Matsunobe T, Imai T, Infrared analysis of depth profile in uv-photochemical
degradation of polymers, Polymer Deg. Stab., 2005, 88, 224-233.
Bokria JG, Schilick S, Spatial effects in the photodegradation of poly(acrylonitrilebutadiene-styrene): A study by ATR-FTIR, Polymer, 2002, 43, 3239-3246.
Signor AW, Vanlandingham MR, Chin JW, Effects of ultraviolet radiation exposure on
vinyl ester resins: Characterization of chemical, physical and mechanical damage, Polymer
Deg. Stab., 2003, 79, 359-368.
Pospisil J, Pilar J, Billinbham NC, Marek A, Horak Z, Nespurek S, Factors affecting
accelerated testing of polymer photostability., Polymer Deg. Stab., 2006, 91, 417-422.
The Environmental Effects Assessment Panel Report for 2006
Effects of stratospheric ozone depletion and climate change on materials damage
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
Croll SJ, Skaja AD, Quantitative spectroscopy to determine the effects of photodegradation
on a model polyester-urethane coating, J. Coat. Technol., 2003, 75, 85-94.
Croll SJ, Skaja AD, Spectroscopic absorption and effective dosage in accelerated
weathering of polyester-urethane coating, J. Material. Sci., 2002, 37, 4829-4840.
Zhang R, Gu X, Chen H, Zhang J, Li Y, Nguyen T, Sandreczki T, Jean YC, Study of the
photodegradation of epoxy polymers with slow positron annihilation spectroscopy, J.
Polymer Sci. B-Polymer Phys., 2004, 42, 2441-2459.
Torikai A, Shibata H, Photodegradation of polystyrene: Effect of polymer structre on the
formation of degradation products., Arab. J. Sci. Eng., 2002, 27, 11-24.
Lucarini M, Pedulli GF, Motyakin MV, Schilick S, Electronspin resonance imaging of
polymer degradation and stabilization, Prog. Polymer Sci., 2003, 28, 331-340.
Norrman K, Krebs FC, Photodegradation of poly (ether sulphone) Part 2. Wavelength and
atmosphere dependence, Surf. Inferface Anal., 2004, 36, 1542-1549.
Searle J, Worsely D, Titanium dioxide photocatalysed oxidation of plasticizers in thin
poly(vinyl chloride) films, Plast. Rubber. Composit., 2002, 31, 329-335.
Taguchi Y, Ishida Y, Tsuge S, Ohtani H, Kimura K, Yoshikawa K, Matsubara T, Structural
change of polymeric hindered amine light stabilizer in polypropylene during UVirradiation studied by reactive thermal desorption-gas chromatography, Polymer Deg.
Stab., 2004, 83, 221-227.
Sombatsompop N, Sungsanit K, Structural changes and mechanical performance of
recycled poly(vinyl chloride) bottles exposed to ultraviolet light at 313 nm, J. Appl.
Polymer. Sci., 2004, 92, 84-94.
Chen X, Wang J, Shen J, Effect of UV-irradiation on poly(vinyl chloride) modified by
methylmethacrylate, Polymer Deg. Stab., 2005, 87, 527-533.
Snijders EA, Boersma A, van Baaarle B, Gijsman P, Effect of dicumyl peroxide
crosslinking on the UV stability of ethylene-propylene-diene (EPDM) elastomers
containing 5-ethylene-2-norbornene (ENB), Polymer Deg. Stab., 2005, 89, 484-491.
Antos K, Sedlar J, Influence of aromatic brominated flame retardant on alkane photooxidation: A model and polymer study, Polymer Deg. Stab., 2005, 90, 180-187.
Matuana L, Surface chemistry and mechanical property changes of wood/fiber/high density
polyethylene composites after accelerated weathering, J. Appl. Polymer. Sci., 2004, 94,
2263-2273.
DeFosse F, Additives target wood plastic composite, J. Mod. Plast., 2002, 79, 1.
Stark NM, Matuana LM, Clemons CM, Effect of processing method on surface and
weathering characteristics of wood-flour/HDPE composites, J. Appl. Polymer. Sci., 2004,
93, 1021-1030.
Lundin T, Cramer SM, Falk RH, Felton C, Accelerated weathering of natural fiber-filled
polyethylene composites, J. Material. Civil. Eng., 2004, 16, 547-555.
Abu-Sharkh B, Hamid H, Degradation study of date palm fiber/polypropylene composites
in natural and artificial weathering: mechanical and thermal analysis, Polymer Deg. Stab.,
2004, 85, 967-973.
Gregorova A, Kosikova B, Moravcik R, Stabilization effect of lignin in natural rubber,
Polymer Deg. Stab., 2006, 91, 229-233.
Abu Bakr A, Hassan A, Yusof AFM, Effect of accelerated weathering on the mechanical
properties of oil palm empty fruit filled UPVC composite, Iran. Polymer. J., 2005, 14, 627635.
The Environmental Effects Assessment Panel Report for 2006
197
Effects of stratospheric ozone depletion and climate change on materials damage
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49
50
198
Deglise X, Beatrice F, Photodegradation and photostabilization of woods - The state of art,
Polymer Deg. Stab., 2005, 88, 269-274.
Stark NM, Matuana L, Clemons CM, Effect of processing method on surface and
weathering characteristics of wood-flour/HDPE composite, J. Appl. Polymer. Sci., 2004,
93, 1021-1030.
Seldon R, Nystroem B, Langstroem R, UV aging of poly(propylene)/wood-fiber
composites, Polymer. Comp., 2005, 25, 543-553.
Pandey KK, Study of the effect of photoirradiation on the surface chemistry of wood,
Polymer Deg. Stab., 2005, 90, 9-20.
Li C, Kim DH, Ragouskas AJ, Photostabilization of mechanical pulps by UV absorbers:
Surface photochemical studies using diffuse reflectance techniques, J. Wood. Chem.
Technol., 2004, 20, 30-53.
Li C, Ragauskas AJ, Brightness reversion of mechanical pulps Part XVII: Diffuse
reflectance study on brightness stabilization by additives under various atmospheres,
Cellulose, 2000, 7, 369-385.
Li C, Dong H, Ragauskas AJ, Brightness reversal of mechanical pulp. XIX,
Photostabilization of mechanical pulps by UV absorbers: Surface photochemical studies
using diffuse reflectance technique, J. Wood. Chem. Technol., 2004, 24, 39-53.
Kaczmarek H, Oldak M, Malanowski P, Chaberska H, Effect of short wavelength UVirradiation on aging of polypropylene/cellulose compositions, Polymer Deg. Stab., 2005,
88, 189-198.
George B, Suttie E, Merlin A, Deglise X, Photodegradation and photostabilization of wood,
Polymer Deg. Stab., 2005, 88, 268-274.
Muasher M, Sain M, The efficacy of photostabilizers on the color change of wood filled
plastic composite, Polymer Deg. Stab., 2005, 91, 1156-1165.
Basfar AA, Ali KMI, Natural weathering test for films of various formulations of LDPE
and LLDPE, Polymer Deg. Stab., 2006, 91, 437-443.
CSIRO, Summary of LDPE Film Weathering Allied Trials, CSIRO Report No., Melbourne
Qin H, Zhao C, Zhang S, Chen G, Yang M, Photo-oxidative degradation of
polyethylene/montmorillonite nanocomposite, Polymer Deg. Stab., 2003, 81, 497-500.
Scierka S, Drzal PL, Forster AL, Svetlik S, Nanomechanical properties of UV degraded
TIO2/epoxy nanocomposites, in Material Research Society Symposium, Vol. 841, Material
Research Society., 2005, pp. 217-222.
Shang J, Chai M, Zhu YF, Solid-phase photocatalytic degradation of polystyrene plastic
with TIO2 as photocatalyst, J. Solid State Chem., 2003, 174, 104-110.
Kemp TJ, McIntyre RA, Mechanism of action of titanium dioxide pigment in the
photodegradation of PVC and other polymers, Prog. Reaction Kinet. Mech., 2002, 26, 337374.
Allen NS, Edge M, Ortega A, Sandoval G, Liauw CM, Verran J, Stratton J, McIntyre RB,
Degradation and stabilization of polymers and coatings: Nano versus pigmentary titania
particles, in IUPAC Microsymposium on Degradation, Stabilisation and Recycling and
Polymers No42, Vol. 85, Elsevier Science, Oxford, Prague, 2004, pp. 927-946.
Zhao HX, Li RKY, A study on the photodegradation of zinc oxide filled polypropylene
nanocomposites, Polymer Int., 2006, 47, 3207-3217.
The Environmental Effects Assessment Panel Report for 2006
Effects of stratospheric ozone depletion and climate change on materials damage
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
Katangur P, Warner SB, Patra P, Ultraviolet radiation resistant polymers, in ACS Fall
Meeting - Polymeric Material Science and Engineering, Vol. 89, American Chemical
Society, New York, NY, USA, 2003, p. 723.
Vanier NR, Munro CH, Curable Film-Forming Composition Exhibiting Improved
Resistance To Degradation of Ultraviolet Light, United States Patent Office, 2003, Patent
20030158316.
Ammala A, Hill AJ, Meakin P, Pas SJ, Turney TW, Degradation studies of polyolefins
incorporating transparent nanoparticulate zinc oxide UV stabilizers, J. Nanopart. Res.,
2002, 4, 167-174.
Zeynalov EB, Allen NS, An influence of micron and nano-particles titanium dioxide on the
efficiency of antioxidant Irganox 1010 in a model oxidative reaction, Polymer Deg. Stab.,
2004, 86, 115-120.
Bonda C, O'Rourke S, Pavlovic A, Shah U, Method of decreasing the UV light degradation
of polymers, United States Patent Office, 2005, Patent 123925/11.
Gugumas F, Possibilities and limits of synergism with light stabilizers in polyolefins 2. UV
absorbers in polyolefins, Polymer Deg. Stab., 2002, 75, 309-320.
Maia DRJ, Balbinot L, Popi RJ, De Paoli MA, Effect of conducting carbon black on the
photostabilization of injection molded poly(propylene-co-ethylene) containing TiO2,
Polymer Deg. Stab., 2003, 82, 89-98.
Singh RP, Patwa AN, Desai SM, Pandey JK, Solanky SS, Prasad AV, Synthesis of new
polymeric hindered amine light stabilizers: Performance evaluation in styrenic polymers, J.
Appl. Polymer. Sci., 2003, 90, 1126-1138.
Capocci G, Hubbard M, A radically new UV stabilizer for flexible PVC roofing
membranes, J. Vinyl Addit.Technol., 2005, 11, 91-95.
Seubert CM, Nichols ME, Kucherov AV, Long-term weathering behavior of UV-curable
clearcoats, J. Coat. Technol., 2005, 2, 529-538.
Borsema A, Predicting the efficiency of antioxidants in plastics, Polymer Deg. Stab., 2006,
91, 472-478.
Adamsons K, Cliff N, Kanouni M, Peters C, Yaneff PV, Use of reactable light stabilizers to
prevent migration and to improve durability of coatings on plastic substrate, JCT Res.,
2005, 2, 371-387.
Bojinov VB, Novel adducts of a hindered amine and a blue-emitting fluorophore for "one
step" fluoroscent brightening and stabilization of polymer materials, J. Photochem.
Photobiol. A., 2004, 162, 207-212.
Sing RP, Patwa AN, Desai SM, Pandey JK, Solanky SS, Prasad AV, Synthesis of new
HALS: Performance evaluation in synthetic polymers, J. Appl. Polymer. Sci., 2003, 90,
1126-1138.
Kaci M, Hebal G, Touati N, Rabouhi A, Zaidi L, Djidelli H, Kinetic study of hindered
amine light stabilizer photografting in poly(propylene) films under natural weathering and
accelerated UV conditions: Effect of additive concentration, Macromol. Mat. Eng., 2004,
289.
Pickett JE, UV absorber permanance and coating lifetimes, J. Test. Environ., 2004, 32,
240-245.
Decker C, Weathering resistance of water-based UV-cured polyolefin-acrylate coatings,
Polymer Deg. Stab., 2004, 83, 309-320.
The Environmental Effects Assessment Panel Report for 2006
199
Effects of stratospheric ozone depletion and climate change on materials damage
68
69
70
200
Rabinovitch EB, Summers JW, Weather resistant plastic composites capped with
polyethylene terephthalate glycol (PETG) for outdoor exposure, United States Patent
Office, 2003, Patent 140606/10.
Decker C, Photostabilization of poly(vinyl chloride) by protective coatings, J. Vinyl
Addit.Technol., 2001, 7, 235-243.
McMan SJ, Johnson HA, Jones CL, Nelson EW, Goenner ES, Outdoor weatherable
photopolymerizable coatings, United States Patent Office, 2005, Patent 06974850.
The Environmental Effects Assessment Panel Report for 2006
Environmental Effects Panel Members
ENVIRONMENTAL EFFECTS PANEL MEMBERS AND UNEP REPRESENTATIVES
Dr Anthony Andrady
Engineering Technology Division
RTI International
3040 Cornwallis Road
Durham, NC 27709
USA
Tel. +1-919-541-6713
Fax: +1-919-541-6936
Email: andrady@rti.org
Dr. Pieter J. Aucamp
Ptersa Environmental Consultants
P.O. Box 915751
Faerie Glen, 0043
South Africa
Tel. +27 12 365 1025
Fax: +27 12 365 1025
Email: pjaucamp@iafrica.com
Dr Carlos L. Ballaré
IFEVA, Facultad de Agronomía,
CONICET and Universidad de Buenos
Aires
Avda. San Martin 4453
C1417DSE Buenos Aires
Argentina
Tel. +54 11 4524 8000, ext. 8101
Fax: +54 11 4514 8730
Email: ballare@ifeva.edu.ar
Dr Alkiviadis F. Bais
Aristotle University of Thessaloniki
Laboratory of Atmospheric Physics
Campus Box 149
54124 Thessaloniki
Greece
Tel. +30 2310 998184
Fax: +30 2310 998090
Email: abais@auth.gr
Prof. Lars Olof Björn
Lund University
Department of Cell and Organism
Biology
Sölvegatan 35
223 62 Lund
Sweden
Tel. +46-46-22-27797 or +46-46-133713
Fax: +46-46-22-24113
Email: Lars_Olof.Bjorn@cob.lu.se
Prof. Janet F. Bornman
International Global Change Institute,
IGCI
University of Waikato
Private Bag 3105
Hamilton 3240
New Zealand
Tel. +64 7 8394930 Ext. 718
Mobile: +64 (0)27 26 98 444
Fax +64 7 8395974
Email: JBornman@waikato.ac.nz
Prof. Martyn Caldwell
National Science Foundation
Division of Environmental Biology
Room 635
4201 Wilson Boulevard
Arlington, VA, 22230
USA
Tel. +1-703-292-7866
Fax: +1-703-292-9064
Email: mmc@cc.usu.edu
Dr Anthony P. Cullen
School of Optometry, University of
Waterloo
131 Briarcliffe Crescent
Waterloo
Ontario
Canada N2L 5T6
Tel. +1-519-746-4346
Email: acullen@uwaterloo.ca
The Environmental Effects Assessment Panel Report for 2006
201
Environmental Effects Panel Members
Prof. G. Kulandaivelu
School of Biological Sciences
Madurai Kamaraj University
Madurai 625021
India
Tel. +91-452-245-8485
Fax: +91-452-245-9139
Email: gkplant1@sify.com
Dr. Frank R. de Gruijl
Department of Dermatology
Leiden University Medical Centre
Bldg. 2 POSTAL Zone S2P
P.O. Box 9600
NL-2300 RC Leiden
The Netherlands
Tel. +31-71-526-9363
Fax: +31-71-526-8106
Email: F.R.de_Gruijl@Lumc.nl
Dr David J. Erickson III
Computational Earth Sciences Group
Computer Science and Mathematics
Division
Oak Ridge National Laboratory
P.O. Box 2008
MS 6016 Oak Ridge
TN 37831-6016
USA
Tel: +1-865-574-3136
Fax +1-865-576-5491
Email: ericksondj@ornl.gov
Prof. D.-P. Häder
Institut für Biologie der Universität
Erlangen-Nürnberg
Staudtstrasse 5
D-91058 Erlangen
Germany
Tel. +49-9131-8528216
Fax: +49-9131-8528215
Email: dphaeder@biologie.unierlangen.de
Prof. Mohammad Ilyas
The University College of Engineering
North Malaysia
School of Environmental Engineering
KWS Building 01000 Kangar Perlis
Malaysia
Tel. +604 65 70169
Fax: +604 979 8099
Email: drmij9@yahoo.com
202
Dr H.D. Kumar
Mrigtrishna B32/605 Plot 214,
Saketnagar
Naria
Varanasi - 221 005
India
Tel. +91-542-231-5180 (residence)
Email:: hd_kumar@yahoo.com or
hdkumar@rediffmail.com
Please do not send emails with long
attachments. Hard copies should instead
be sent by airmail
Dr Janice Longstreth
The Institute for Global Risk Research,
LLC
9119 Kirkdale Road, Suite 200
Bethesda, MD 20817
USA
Tel. +1-301-530-8071
Fax: +1-301-530-1646
Email: tigrr98@comcast.net
Dr Richard L. McKenzie
National Institute of Water and
Atmospheric Research
NIWA, Lauder
Private Bag 50061 Omakau
Central Otago 9320
New Zealand
Tel. +64-3-440-0429
Fax: +64-3-447-3348
Email: r.mckenzie@niwa.co.nz
The Environmental Effects Assessment Panel Report for 2006
Environmental Effects Panel Members
Prof. Mary Norval
Medical Microbiology
University of Edinburgh Medical School
Teviot Place, Edinburgh EH8 9AG
UK
Tel. +44-131-650-3167
Fax: +44-131-650-6531
Email: M.Norval@ed.ac.uk
Dr Keith Solomon
Centre for Toxicology
University of Guelph
Guelph, ON
N1G 2W1 Canada
Tel. +1-519-824-4120 x 58792
Fax
+1-519-837-3861
Email: ksolomon@uoguelph.ca
Dr Nigel D Paul,
Department of Biological Sciences,
Lancaster Environment Centre,
Lancaster University,
Lancaster,
LA1 4YQ
UK
Tel:
+44-1524-510208
Fax: +44-1524-510217
Email: n.paul@lancaster.ac.uk
Dr Barbara Sulzberger
Swiss Federal Institution of Aquatic
Science and Technology (Eawag)
Überlandstrasse 133
P.O. Box 611
CH-8600 Dübendorf
Switzerland
Tel. +41-1-823-54-59
Fax: +41-1-823-50-28
Email: sulzberger@eawag.ch
Dr. Halim Hamid Redhwi
King Fahd University of Petroleum &
Minerals (KFUPM)
Dhahran 31261, Saudi Arabia
Tel: +966-3-860-3840 (sec)
Tel: +966-3-860-3810 (direct)
Cell: +966-505-855-071
Fax: +966-3-860-3586 and -2259
Email: hhamid@kfupm.edu.sa
Prof. Yukio Takizawa
National Institute for Minamata Disease
4083-106 Hama, Minamata
Kumamoto 897-0008, Japan
Tel. +81-966-63-6958
Fax ;81-966-63-6958
Email: takizawa-y@sky.plala.or.jp
Prof. Raymond C. Smith
Institute for Computational Earth System
Science (ICESS) and Department of
Geography
University of California
Santa Barbara, California 93106
USA
Tel. +1-805-893-4709
Fax: +1-805-893-2578
Email: ray@icess.ucsb.edu
Dr Xiaoyan Tang
Peking University
Center of Environmental Sciences
Beijing 100871
China
Tel. +86-10-6275-1925
Fax: +86-10-6275-1925 / 27
Email: xytang@pku.edu.cn
Prof. Alan H. Teramura
Department of Botany
University of Hawaii
3190 Maile Way
Honolulu, Hawaii 96822-1180
USA
Tel. +1-808-956-3930
Fax: +1-808-956-3923
Email: teramura@hawaii.edu
The Environmental Effects Assessment Panel Report for 2006
203
Environmental Effects Panel Members
Dr Ayako Torikai
Materials Life Society of Japan
2-6-8 Kayabacho Chuo-ku
Tokyo 103-0025
Japan
Tel./Fax: +81-52-721-8008
Email: torikaia@msj.biglobe.ne.jp
UNEP contact
Mr. Marco Gonzalez
Ozone Secretariat, UNEP
P.O. Box 30552
Nairobi
Kenya
Tel. +254-2-623 885
Fax: +254-2-623 913 or 623 601
Email: Marco.Gonzalez@unep.org
Prof. Jan C. van der Leun
Ecofys
Kanaalweg 16 G
NL-3526 KL Utrecht
The Netherlands
Tel. +31-30-280-8361
Fax:+31-30-280-8301
Email: j.vanderleun@ecofys.nl
Dr Stephen Wilson
Department of Chemistry
University of Wollongong
Northfields Ave.
Wollongong, NSW, 2522
Australia
Tel. +61-2-4221-3505
Fax: +61-2-4221-4287
Email: Stephen_Wilson@uow.edu.au
Dr Robert C. Worrest
CIESIN, Columbia University
12201 Sunrise Valley Drive (MS-302)
Reston, VA, 20192-0002
USA
Tel. + 1-703-648-4074
Fax: + 1-703-648-4224
Email: rworrest@ciesin.columbia.edu
Dr Richard G. Zepp
United States Environmental Protection
Agency
960 College Station Road
Athens, Georgia 30605-2700
USA
Tel. +1-706-355-8117
Fax: +1-706-355-8104
Email: zepp.richard@epa.gov
Spouse: Mary Ann
204
The Environmental Effects Assessment Panel Report for 2006
REVIEWERS OF THE 2006 UNEP EFFECTS ASSESSMENT PANEL
Professor Ayite-Lo Nohende Ajavon
Atmospheric Chemistry Laboratory
FDS/Université de Lome
B.P. 1515 Lome
TOGO
Phone: +228-225 5094
Fax: +228-221 8595
Mobile +228-904-1593/944 9444
Home +228-226-9170
noajavon@tg.refer.org
Dr. Pedro J. Aphalo
Department of Biological and
Environmental Sciences
Plant Biology / Plant Ecology
P.O. Box 65
00014 University of Helsinki
Finland
pedro.aphalo@helsinki.fi
Dr. Joan L. Aron
Science Communication Studies
5457 Marsh Hawk Way
Columbia, Maryland 21045
U.S.A.
Tel: 410-740-0849
Fax: 410-964-3598
JoanAron@mmscnet.org
Dr. Paul Barnes
Department of Biology
Southwest Texas State University
601 University Drive
San Marcos, TX 78666
Phone: 512-245-3753
Fax: 512-245-8713
pb03@swt.edu
Dr. Marianne Berwick
Address: UNM Health Sciences Center
Department of Internal Medicine
MSC 10 5550, 1 University of New Mexico
Albuquerque, NM 87131-0001
Phone: 272-4369
MBerwick@salud.unm.edu
Dr. Mario Blumthaler
Institute of Medical Physics
University of Innsbruck
A-6020, Innsbruck, Austria
Fax +43-512-507-2860
Mario.Blumthaler@uibk.ac.at
Thomas P. Coohill
Siena College
515 Loudon Road
Loudonville, NY, 12211, USA
Tel. +1 518-783-2441
Fax +1 518-783-2986
tcoohill@siena.edu
Prof. Edward DeFabo
Department of Environmental and
Occupational Health
School of Public Health and Health Services
George Washington University Medical
Center
Ross Hall, Room 113
2300 I St., NW
Washington, D.C. 20037, USA
Tel. 1 202 994 3975
FAX: 1 202 994 0409
drmecd@gwumc.edu
Dr. Susana Diaz
CADIC-CONICET
Ruta 3 y Cap.Mutto
C.C. 92
9410 Ushuaia - Tierra del Fuego, Argentina
Tel: +54 2901 422754
Fax: +54 2901 430644
rqdiaz@criba.edu.ar
The Environmental Effects Assessment Panel Report for 2006
205
Reviewers of the 2006 UNEP Effects Assessment Panel
Prof. Nils Ekelund
Department of Natural and Environmental
Sciences
Mid-Sweden University
851 70 Sundsvall, Sweden
Tel. + 46-060-148707
Fax +46-060-148802
nils.ekelund@mh.se
Dr. Ernesto Bernardine Fernández
Faculty of Pharmacy
Valparaiso University
Casilla 5001-V Valparaíso
Gran Bretañaa 1111, Valparaiso, Chile
Tel. +56-32-508106
Fax +56 32-508111
ernesto.fernandez@uv.cl
Dr. W D Grant
Sunlight, Nutrition and Health Research
Centre
San Francisco
CA, USA
wgrant@sunarc.org
Dr. R Elizabeth M Griffin
Herzberg Institute for Astrophysics,
5071 West Saanich Road,
Victoria,
B.C., Canada,
V9E 2E7.
Elizabeth.Griffin@hia-iha.nrc-cnrc.gc.ca
Dr. Walter Helbling
Estación de Fotobiología Playa Unión
Casilla de Correo 15
(9103) Rawson,
Chubut, Argentina
Tel. +54 2965 498 019
Tel/Fax +54 2965 496 269
whelbling@efpu.org.ar
206
Dr, Rainer Hofmann
Lecturer in Plant Biology
Agriculture and Life Sciences Division
Lincoln University
PO Box 84
Canterbury 8150
New Zealand
Ph: ++64 3 325 3838 ext 8202
Fax: ++64 3 325 3851
hofmannr@lincoln.ac.nz
www.lincoln.ac.nz
Andreas Hofzumahaus
Institut fuer Chemie und Dynamik der
Geosphaere
ICG-II: Troposphaere
Forschungszentrum Juelich GmbH
Leo Brandtstr.
D-52425 Juelich Germany
a.hofzumahaus@fz-juelich.de
Dr. Dylan Gwynn-Jones
Institute of Biological Sciences
University of Wales
Aberystwyth
Ceredigion, SY23 3DA, Wales, UK
Tel. +44 (0)1970 622318
Fax +44 (0)1970 622350
dyj@aber.ac.uk
Dr Gareth Jenkins
Plant Science Group
Division of Biochemistry and Molecular
Biology
Institute of Biomedical and Life Sciences
University of Glasgow
Glasgow G12 8QQ
United Kingdom
g.jenkins@bio.gla.ac.uk
The Environmental Effects Assessment Panel Report for 2006
Reviewers of the 2006 UNEP Effects Assessment Panel
Professor Brian R. Jordan
Divisional Director
Agriculture & Life Sciences Division
P.O. Box 84
Lincoln University
New Zealand
Phone +64 3 325 3821
Fax: +64 3 325 3843
jordanb@lincoln.ac.nz
Prof. William Miller
248 Marine Sciences Bldg.
Department of Marine Sciences
University of Georgia
Athens, GA 30602-3636
Office Phone: (706) 542-4299
Lab Phone: (706) 542-0809
FAX Number: (706) 542-5888
bmiller@uga.edu
Kostas Kourtidis
Lab. of Atmospheric Pollution and Pollution
Control Engineering of Atmospheric
Pollutants
Dept. of Environmental Engineering
School of Engineering
Demokritus University of Thrace
12 Vas. Sofias str., 67100 Xanthi, Greece
kourtidi@env.duth.gr
Dr. Patrick J. Neale
Smithsonian Environmental Research
Center
P.O. Box 28
647 Contees Wharf Rd.
Edgewater MD 21037, USA
Tel. +1 443-482-2285 (Office)/+1 443-4822329
Fax +1 443-482-2380
nealep@si.edu
http://www.serc.si.edu/labs/photobiology/in
dex.jsp
Dr. Margaret Kripke
Department of Immunology
Box 178
The University of Texas, M.D. Anderson
Cancer Center
1515 Holcombe Boulevard
Houston, TX, 77030-4095, USA
mripke@mail.mdanderson.org
Prof. Lawrence E. Licht
York University
Department of Biology
4700 Keele Street
Toronto, ON, M3J 1P3, Canada
Fax 1 416 736-5989
lel@YorkU.CA
Dr. Robyn Lucas
The Australian National University
National Centre for Epidemiology and
Population Health
Building 124
Canberra, ACT, 0200, Australia
Tel. +61 2 6125 3448
Fax +61 2 6125 5614
Robyn.Lucas@anu.edu.au
Dr. Jonathan Newman
Department of Environmental Biology,
University of Guelph
Guelph, ON, N1G 2W1, Canada
Tel. 519-824-4120 x 52147
jnewma01@uoguelph.ca
Prof. Frances Noonan
Department of Environmental and
Occupational Health
School of Public Health and Health Services
The George Washington University Medical
Center
Ross Hall, Room 113
2300 Eye St., NW
Washington, DC, 20037
USA
Tel: +1202 994 3970
Fax: +1202 994 0409
drmfpn@gwumc.edu
The Environmental Effects Assessment Panel Report for 2006
207
Reviewers of the 2006 UNEP Effects Assessment Panel
Dr. Masaji Ono
Environmental Health Sciences Division
National Institute for Environmental Studies
Onogawa 16-2, Tsukuba 305-8506, Japan
Tel. +81 298 50 2421
Fax +81 298 50 2588
onomasaj@nies.go.jp
Dr. Rubén D. Piacentini
Instituto de Física Rosario
CONICET-Univ. Nac. de Rosario 9
27 de Febrero 210bis
2000 Rosario, Argentina
Fax +54-341-482 17 72
ruben@ifir.edu.ar
Dr. Norma D. Searle
114 Ventnor F
Deerfield Beach, FL, 33442, USA
Tel./Fax 1 954 480 8938
ndsearle@aol.com.
Prof. Günther Seckmeyer
Institute for Meteorology and Climatology
University of Hannover
Herrenhaeuser Str. 2
30419 Hannover, Germany
Tel. +49-511-762-4022
Fax +49-511-762-4418
Seckmeyer@muk.uni-hannover.de
http://www.muk.unihannover.de/~seckmeyer
Dr. Anna Maria Siani
Universita' di Roma "La Sapienza"
Dipartimento di Fisica
Piazzale Aldo Moro, 5
IT-00185 Roma, Italy
Tel. +39-06-49913479
Fax +39-06-4463158
annamaria.siani@uniroma1.it
http://www.phys.uniroma1.it/DOCS/METE
O/HP_GMET.HTM
208
Dr. Rajeshwar Sinha
Department of Botany
Banares Hindu University
Varanasi, 221005, India
r.p.sinha@gmx.net
Dr. Igor Sobolev
Chemical & Polymer Technology
5 Rita Way
Orinda, CA 94563
USA
Tel. 1 925-376-6402
Fax 1 925 376-6402
i.sobolev@worldnet.att.net
Professor Ruben Sommaruga
Head, Laboratory of Aquatic Photobiology
and Plankton Ecology
Institute of Ecology
University of Innsbruck
Technikerstr. 25
A-6020 Innsbruck
Austria
Phone (office): +43-512-507-6121
Phone (lab): +43-512-507-6145 or 6197
Fax: +43-512-507-2930
Ruben.Sommaruga@uibk.ac.at
Dr. J. Richard Soulen
5333 Hickory Bend
Bloomfield Hills, MI 48304
USA
Tel. +1 248 642 6568
Fax +1 248 258 6769
rsoulen@comcast.net
Dr. Ann Stapleton
Department of Biology,
University of North Carolina, Wilmington,
602 S College
Wilmington, NC, 28403, USA
Stapletona@uncw.edu
The Environmental Effects Assessment Panel Report for 2006
Reviewers of the 2006 UNEP Effects Assessment Panel
Dr. Åke Strid
Department of Natural Sciences
Örebro University
701 82 Örebro
Sweden
ake.strid@nat.oru.se
Prof. Hugh R Taylor
Centre for Eye Research Australia
The University of Melbourne
Department of Ophthalmology
Locked Bag 8, East Melbourne 8002
Australia
Tel. +61 3 9929 8368
Fax +61 3 9662 3859
h.taylor@unimelb.edu.au
Ann R. Webb
University of Manchester
Sackville Street
P.O. Box 88
Manchester
M60 1QD
United Kingdom
ann.webb@manchester.ac.uk
Dr. Hellen West
Agricultural and Environmental Sciences
Nottingham University
Notingham, UK
Phone : +44 (0)115 951 6268
Fax : +44 (0)115 951 6267
helen.west@nottingham.ac.uk
Dr. Craig Williamson
Department of Zoology
212 Pearson Hall
Miami University
Oxford, OH, 45046
Craig.williamson@muohio.edu
Prof. Huixiang Xie
nstitute of Marine Sciences
University of Quebec at Rimouski
Rimouski, QC G5L 3A1 Canada
huixiang_xie@uqar.qc.ca
The Environmental Effects Assessment Panel Report for 2006
209