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One of the predicted consequences of the depletion of stratospheric ozone is
an increase in the amount of ultra-violet light reaching the surface of the earth,
in particular, UV-B (320-280 nm). Although the real effects are as yet
unknown, this change in radiation could have profound consequences for plant
growth and productivity. The need for information concerning the relationship
between plants and UV-B is therefore pressing. This volume brings together
authoritative contributions from leading experts in UV-B/plant studies and is
unique in considering interactions at various scales, ranging from the level of
the cell through to the level of the community. Information concerning ozone
depletion and physical aspects of UV-B radiation complements the biological
information to provide a thorough and comprehensive review of the present
status of knowledge.
SOCIETY FOR EXPERIMENTAL BIOLOGY
SEMINAR SERIES: 64

PLANTS AND UV-B

RESPONSES TO ENVIRONMENTAL CHANGE
SOCIETY FOR EXPERIMENTAL BIOLOGY SEMINAR SERIES
A series of multi-author volumes developed from seminars held by the Society
for Experimental Biology. Each volume serves not only as an introductory
review of a specific topic, but also introduces the reader to experimental evi-
dence to support the theories and principles discussed, and points the way to
new research.
6. Neurones without impulses: their signifi- 47. Fruit and seed production: aspects of
cance for vertebrate and invertebrate systems. development, environmental physiology and
Edited by A. Roberts and B.M.H. Bush ecology. Edited by C. Marshall and J. Grace
8. Stomatal physiology. Edited by P.C.G. 48. Perspectives in plant cell recognition.
Jarvis and T.A. Mansfield Edited by J.A. Callow and J.R. Green
16. Gills. Edited by D.F. Houlihan, J.C. 49. Inducible plant proteins: their biochemis-
Rankin and TJ. Shuttleworth try and molecular biology. Edited by J.L. Wray
31. Plant canopies: their growth, form and 50. Plant organelles: compartmentation of
function. Edited by G. Russell, B. Marshall metabolism in photosynthetic cells. Edited by
and P.G. Jarvis A.K. Tobin
33. Neurohormones in invertebrates. Edited 51. Oxygen transport in biological systems:
by M. Thorndyke and G. Goldsworthy modelling of pathways from environment to
34. Acid toxicity and aquatic animals. Edited cell. Edited by S. Eggington and H.F. Ross
by R. Morris, E.W. Taylor, D.J.A. Brown and 52. New insights in vertebrate kidney func-
J.A. Brown tion. Edited by J.A. Brown, RJ. Balment and
35. Division and segregation of organelles. J.C. Rankin
Edited by S.A. Boffey and D. Lloyd 53. Post-translational modifications in plants.
36. Biomechanics in evolution. Edited by Edited by N.H. Battey, H.G. Dickinson and
J.M.V. Rayner and RJ. Woottqn A.M. Hetherington
37. Techniques in comparative respiratory 54. Biomechanics and cells. Edited by FJ.
physiology: An experimental approach. Edited Lyall and AJ. El Haj
by C.R. Bridges and P.J. Butler 55. Molecular and cellular aspects of plant
38. Herbicides and plant metabolism. Edited reproduction. Edited by R. Scott and A.D.
by A.D. Dodge Stead
39. Plants under stress. Edited by H.C. Jones, 56. Amino acids and their derivatives in
TJ. Flowers and M.B. Jones plants. Edited by R.M. Wallsgrove
40. In situ hybridisation: application to devel- 57. Toxicology of aquatic pollution: physio-
opmental biology and meoicine. Edited by N. logical, cellular and molecular approaches.
Harris and D.G. Wilkinson Edited by E. W. Taylor
41. Physiological strategies for gas exchange 58. Gene expression and adaptation in aquatic
and metabolism. Edited by AJ. Woakes, M.K. organisms. Edited by S. Ennion and G. Gold-
Grieshaber and C.R. Bridges spink
42. Compartmentation of plant metabolism in 59. Animals and temperature: phenotypic and
non-photosynthesis tissues. Edited by M.J. evolutionary adaptation. Edited by LA. John-
Ernes ston and A.F. Bennett
43. Plant growth: interactions with nutrition 60. Molecular physiology of growth. Edited
and environment. Edited by J.R. Porter and by P.T. Loughna and J.M. Pell
D.W. Lawlor 61. Global warming: implications for fresh-
44. Feeding and texture of foods. Edited by water and marine fish. Edited by CM. Wood
J.F.V. Vincent and P.J. Lillford and G. McDonald
45. Endocytosis, exocytosis and vesicle traffic 62. Fish stress and health in aquaculture.
in plants. Edited by G.R. Hawes, J.O.D. Col- Edited by G.K. Iwama, A.D. Pickering, J.
eman and D.E. Evans Sumpter and C. Schreck
46. Calcium, oxygen radicals and cellular 63. Scaling-up. Edited by P. van Gardingen,
damage. Edited by C.J. Duncan P. Curran ana G. Foody
PLANTS AND UV-B
Responses to Environmental Change

Edited by
P. J. Lumsden
Department of Applied Biology
University of Central Lancashire, Preston, UK

CAMBRIDGE
UNIVERSITY PRESS
CAMBRIDGE UNIVERSITY PRESS
Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao Paulo, Delhi

Cambridge University Press

The Edinburgh Building, Cambridge CB2 8RU, UK

Published in the United States of America by Cambridge University Press, New York

www.cambridge.org
Information on this title: www.cambridge.org/9780521114110
© Cambridge University Press 1997

This publication is in copyright. Subject to statutory exception

and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without the written
permission of Cambridge University Press.

First published 1997

This digitally printed version 2009

A catalogue record for this publication is available from the British Library

Library of Congress Cataloguing in Publication data

Plants and UV-B: responses to environmental change/edited by P. J.
Lumsden
p. cm. - (Society for Experimental Biology seminar series; 64)
Includes index.
ISBN 0 521 57222 3 (hardback)
1. Plants, Effect of ultraviolet radiation on. I. Lumsden, P.J.
II. Series: Seminar series (Society for Experimental Biology (Great Britain));
64.
QK757.P53 1997
571.4'562-dc21 96 30065 CIP
ISBN 978-0-521-57222-4 hardback
ISBN 978-0-521-11411-0 paperback
 Contents

List of contributors ix
Preface xiii

PART I: The ozone layer and UV-B radiation

Global ozone depletion: observations and theory 3

J.A. PYLE

Monitoring changes in UV-B radiation 13

A.R. WEBB

Action spectra for UV-B effects on plants: monochromatic

and polychromatic approaches for analysing plant
responses 31
M.G. HOLMES

PART ii: Effects of UV-B on plants at the cellular level

DNA damage and repair in plants 53

R.M. TAYLOR, A.K. TOBIN and C M . BRAY

Genetic analysis of DNA repair in plants 77

A.B. BRITT

Photosynthesis and photoinhibition 95

N.R. BAKER, S. NOGUES and D.J. ALLEN

UV-B effects on the expression of genes encoding proteins

involved in photosynthesis 113
S. A-H. MACKERNESS, B.R. JORDAN and B. THOMAS
viii Contents
UV-B perception and signal transduction 135
G.I. JENKINS, G. FUGLEVAND and J.M. CHRISTIE

Ultraviolet radiation as a stress factor and the role of

protective pigments 157
J.F. BORNMAN, S. REUBER, Y-P. CEN andG. WEISSENBOCK

PART Hi: Effects of UV-B at the whole plant and community

level

Effects of solar UV-B radiation on aquatic ecosystems 171

D-P. HADER

Assessing the impact of UV-B radiation on the growth and

yield of field crops 195
J.E. CORLETT, J. STEPHEN, H.G. JONES, R. WOODFIN,
R. MEPSTED andN.D. PAUL

Effects of UV-B radiation on plants from agro- and natural

ecosystems 213
J. ROZEMA, J.W.M. VAN DE STAAIJ andM. TOSSERAMS

Effects on subarctic vegetation of enhanced UV-B radiation 233

L.O. BJORN, T. CALLAGHAN, C. GEHRKE, T. GUNNARSSON,
B. HOLMGREN, U. JOHANSON, S. SNOGERUP, M. SONESSON,
O. STERNER and S-G. YU

Impacts of elevated UV-B on forest ecosystems 247

A.R. McLEOD andK.K. NEWSHAM

Effects of elevated UV-B radiation and elevated CO2 on

heathland communities 283
S.A. MOODY, D.J.S. COOP andN.D. PAUL

Alterations in competitive balance 305

M.M. CALDWELL

Interations between trophic levels 317

N.D. PAUL

Index 341
 Contributors

A-H. MACKERNESS, S.
Department of Molecular and Environmental Physiology, Horticulture
Research International, Wellesbourne, Warwick CV35 9EF, UK
ALLEN, D.J.
Department of Biological and Chemical Sciences, University of Essex,
Wivenhoe Park, Colchester, Essex CO4 3SQ, UK
BAKER. N.R.
Department of Biological and Chemical Sciences, University of Essex,
Wivehoe Park, Colchester, Essex CO4 3SQ, UK
BJORN, L.O.
Department of Plant Physiology, University of Lund, Box 117, S-221
00, Sweden
BORNMAN, J.F.
Department of Plant Physiology, University of Lund, Box 117, S-221
00, Sweden
BRAY, C M .
School of Biological Sciences, 3.614 Stopford Building, University of
Manchester, Oxford Road, Manchester Ml3 9PT, UK
BRITT, A.B.
Division of Biological Sciences, Section of Plant Biology, University
of California, Davis, California 95616, USA
CALDWELL, M.M.
Department of Rangeland Resources, Utah State University, Logan,
Utah, UT 84322-5230, USA
CALLAGHAN, T.
Sheffield Centre for Arctic Biology, University of Sheffield, Sheffield,
UK
CEN, Y-P.
APPA Division, IRRI, Manila 1099, Phillippines
CHRISTIE, J.M.
Plant Molecular Science Group, Division of Biochemistry and Molecu-
lar Biology, Institute of Biomedical and Life Sciences, Bower Building,
University of Glasgow, Glasgow G12 8QQ, UK
x Contributors
COOP, D.J.S.
Division of Biological Sciences, University of Lancaster, Bailrigg,
Lancaster LAI 4YQ, UK
CORLETT, J.E.
Annual Crops Department, Horticulture Research International, Welles-
bourne, Warwick CV35 9EF, UK
FUGLEVAND, G.
Plant Molecular Science Group, Division of Biochemistry and Molecu-
lar Biology, Institute of Biomedical and Life Sciences, Bower Building,
University of Glasgow, Glasgow G12 8QQ, UK
GEHRKE, C.
Department of Plant Ecology, University of Lund and Abisko Scientific
Research Station, S-221 00 Lund, Sweden
GUNNARSSON, T.
Department of Chemical Ecology and Ecotoxicology, University of
Lund, S-221 00 Lund, Sweden
HADER, D-P.
Institut fiir Botanik und Pharmazeutische Biologie, Friedrich-
Alexander-Universitat, Staudstr. 5, D91058 Erlangen, Germany
HOLMES, M.G.
Department of Plant Sciences, University of Cambridge, Downing
Street, Cambridge CB2 3EA, UK
HOLMGREN, B.
Department of Meteorology, Uppsala University and Abisko Scientific
Research Station, Uppsala, Sweden
JENKINS, G.I.
Plant Molecular Science Group, Division of Biochemistry and Molecu-
lar Biology, Institute of Biomedical and Life Sciences, Bower Building,
University of Glasgow, Glasgow G12 8QQ, UK
JOHANSON, U.
Department of Plant Physiology, University of Lund, Box 117, S-221 00
Lund, Sweden
JONES, H.G.
Annual Crops Division, Horticulture Research International, Welles-
bourne, Warwick CV35 9EF, UK
JORDAN, B.R.
Department of Crop and Food Research, Levin Research Centre, Private
Bag 4005, Levin, New Zealand
McLEOD, A.R.
Institute of Terrestrial Ecology, Monks Wood, Abbots Ripton, Hunting-
don, Cambridge PE17 2LS, UK
 Contributors xi
MEPSTED, R.
Bath University, Bath, Avon BA2 7AY, UK
MOODY, S.A.
Division of Biological Sciences, University of Lancaster, Bailrigg,
Lancaster LAI 4YQ, UK
NEWSHAM, K.K.
Institute of Terrestrial Ecology, Monks Wood, Abbots Ripton, Hunting-
don, Cambridge PE17 2LS, UK
NOGUES, S.
Department of Biological and Chemical Sciences, University of Essex,
Wivenhoe Park, Colchester, Essex CO4 3SQ, UK. Present address:
Departament de Biologia Vegetal, Facultat de Biologia, Universitat de
Barcelona, Avgda, Diagonal 645, 0828 Barcelona, Spain
PAUL, N.D.
Division of Biological Sciences, University of Lancaster, Bailrigg,
Lancaster LAI 4YQ, UK
PYLE, J.A.
Centre for Atmospheric Science, Department of Chemistry, University
of Cambridge, Lensfield Road, Cambridge CB2 1EW, UK
REUBER, S.
Department of Plant Physiology, University of Lund, Box 117, S-221 00
Lund, Sweden
ROZEMA, J.
Department of Ecology and Ecotoxicology, Vrije University, De
Boelelaan 1087, 1081 HV Amsterdam, The Netherlands
SNOGERUP, S.
Botanical Museum, University of Lund, S-221 00 Lund, Sweden
SONESSON, M.
Department of Plant Ecology, University of Lund, S-221 00 Lund, Sweden
STEPHEN, J.
Annual Crops Department, Horticulture Research International, Welles-
bourne, Warwick CV35 9EF, UK
STERNER, O.
Department of Organic Chemistry 2, University of Lund, S-221 00
Lund, Sweden
TAYLOR, R.M.
School of Biology Sciences, 3.614 Stopford Building, University of
Manchester, Oxford Road, Manchester Ml3 9PT, UK
THOMAS, B.
Department of Molecular and Environmental Physiology, Horticulture
Research International, Wellesbourne, Warwick CV35 9EF, UK
xii Contributors
THOMAS, B.
Department of Molecular and Environmental Physiology, Horticulture
Research International, Wellesbourne, Warwick CV35 9EF, UK
TOBIN, A.K.
Plant Science Laboratory, School of Biological and Medical Sciences,
Sir Harold Mitchell Building, University of St Andrews, Fife, KYI6
9TH, UK
TOSSERAMS, M.
Department of Ecology and Ecotoxicology, Vrije University, De Boele-
laan 1087, 1081 HV Amsterdam, The Netherlands
WEBB, A.R.
Department of Physics, UMIST, PO Box 88, Manchester M60 1QD,
UK
WEISSENBOCK, G.
Botanisches Institut de Universitat zu Koln, Gyrhofstrasse 15, D-50923
Koln, Germany
WOODFIN, R.
Division of Biological Sciences, University of Lancaster, Bailrigg,
Lancaster LAI 4YQ, UK
VAN DE STAAIJ, J.W.M.
Department of Ecology and Ecotoxicology, Vrije University, De Boele-
laan 1987, 1081 HV Amsterdam, The Netherlands
YU, S-G.
Department of Biochemistry, University of Lund, S-221 00 Lund,
Sweden
 Preface

Public awareness of the dangers to health of exposure to ultraviolet

(UV) light has increased in recent years. Although exposure to UV can
have positive effects on humans - sunbathing generally induces a feel-
ing of well-being, partly due to production of natural endorphins, and
stimulation of synthesis of vitamin D - the dangers far outweigh the
benefits. The most noticeable effect of exposure is sunburn, or ery-
thema; more serious is the increase in risk of skin cancer, and of damage
to the eyes, and these symptoms may not surface for several years. At
the same time, the public has also become aware that protection from
solar UV is provided by ozone in the upper atmosphere, the strato-
sphere, but that, over recent years, the ozone layer has suffered
depletion due to the action of man-made chemicals. The predicted result
of this is that more UV radiation from the sun will reach the earth's
surface.
Energy from the sun covers the whole electromagnetic spectrum,
from short gamma rays (10~5 nm) to long radio waves (103 m). UV light
is that region of the spectrum with shorter wavelengths than blue light,
between about 400 nm and 250 nm, and this is divided still further into
UV-A (400-320 nm); UV-B (320-280 nm) and UV-C (280-250 nm).
UV-A does not interact with ozone, since individual photons do not
carry enough energy to carry out the necessary photochemical reactions;
the energy in UV-B is used in breaking the bonds between oxygen
atoms in molecules of ozone, which effectively results in absorption of
the UV-B; UV-C is effectively absorbed by ozone/oxygen, and would
still be so even under high depletions of ozone. Any reduction in the
ozone layer will therefore mean that less UV-B is absorbed, and will
lead to more UV-B reaching the earth's surface.
Until the early 1980s there was no evidence that the ozone in the
stratosphere was actually being depleted; the first recorded evidence for
a thinning in the ozone layer came in 1984 from a British team in
Antarctica, led by Joe Farman. Since then, comprehensive and continu-
ous data have come from the total ozone mapping spectrometer (TOMS)
carried on the Nimbus 7 satellite; together with other instruments, this
xiv Preface
has detected thinning of ozone not just over Antarctica, but over the
entire globe (see chapter by Pyle). By 1987 it was recognised that the
threat to the ozone layer from various gases, particularly man-made
chlorofluorocarbons (CFCs) was real, and as a result, the Montreal Pro-
tocol on Substances that Deplete the Ozone Layer was agreed by rep-
resentatives of 27 of the technologically developed countries. Specified
limits for a number of gases were agreed at Montreal; however, CFCs
are very long-lived, so that, despite limitations being agreed, these were
probably not sufficient to allow recovery of depleted ozone before well
into the twenty-first century.
Although changes in stratospheric ozone would suggest that incident
UV-B will increase, it is clearly vital to have accurate information as
to whether increases in UV-B can actually be detected at ground level,
against a background of other climate variation (see chapter by Webb).
The most recent analyses show that ozone has declined globally by
about 4-5% since 1979, leading to a fairly general assumption that,
over the next three decades, there will be a depletion of the ozone layer
of about 15%, which may result in an increase in effective UV-B of
30% over the current level. It should be noted, however, that within
this range there are significant latitudinal variations in incident UV-B.
For example, the amount of UV-B experienced at tropical latitudes is
much greater than in temperate regions because the angle of the sun is
such that there is less absorption by the atmosphere. In addition, the
ozone layer itself is thinner in equatorial regions. Thus even with sub-
stantial reductions in ozone in temperate regions the effective UV-B
would still not exceed that currently experienced in the tropics. How-
ever, if there were thinning of ozone in tropical regions, the levels of
UV-B would exceed those previously recorded. Conversely, in regions
of very high latitude, the amount of UV-B radiation is relatively low,
but since it is here that thinning of the ozone layer is most marked, the
relative increase in UV-B is potentially greatest.
Over the past few years, research has been carried out to investigate
whether increases in UV-B radiation resulting from ozone depletion
would have a significant impact on plants, in particular, on aspects of
physiology and crop yield, and this volume of the Cambridge University
Press seminar series is intended to provide a comprehensive review of
our current knowledge in this area. It arose partly from a session entitled
UV-B and Plants held at the annual meeting of the Society for Exper-
imental Biology (SEB), Lancaster University, 1996, to which research-
ers from the UK, funded by the Biological Sciences and Biotechnology
Research Council (BBSRC), Natural Environment Research Council
(NERC), Department of the Environment (DOE) and Ministry of Agric-
 Preface xv
ulture Fisheries and Food (MAFF), and researchers from abroad were
invited. All have contributed to the volume. Some chapters provide a
fairly broad review, while others give a more detailed account of recent
experimental work. Some of the current issues relating to research into
UV radiation which were discussed at the meeting are summarised
below, along with some detail of the contents of the chapters.
Experimental work has been carried out in laboratory growth cham-
bers, where plants are grown under artificial white light to which is
added different levels of UV-B, or outdoors, using artificial UV-B to
supplement the UV-B in natural sunlight. From these studies it is now
recognised that there are both direct and indirect effects of UV-B on
plants. Direct effects include radiation-induced changes in photosyn-
thesis, cell division, or other life processes of direct importance to
growth and development. These effects are observed after relatively
short periods of irradiation, hours or days. Damage to DNA has long
been recognised as an important consequence of exposure to UV; this
is discussed in the chapter by Taylor, Tobin and Bray, who describe
the products formed as a result of damage to DNA, and the activity of
the photolyase enzyme(s) involved in repair. Britt then describes a gen-
etic approach of screening for mutants defective in DNA repair as a
way of isolating the genes involved in the repair process. Effects of
UV on photosynthesis are discussed by Baker, Nogues and Allen, the
conclusion being that the primary damaging effect of UV is not on
photosystem II reaction centres, but on some component of the Calvin
cycle. This is demonstrated in more detail by Mackerness, Jordan and
Thomas, who describe the effects of UV on the expression of photosyn-
thetic genes and the levels of photosynthetic proteins. Clearly some of
the UV-B induced down-regulation of photosynthetic genes is not
simply a consequence of non-specific damage to DNA, since other
defence-related genes are up-regulated, and there is developmental vari-
ation in the response to UV-B. Furthermore, protection under high light
appears to be due to some component of photosynthetic activity rather
than to photolyase activity. Direct responses, then, include not only
damage reactions, but also adaptive responses, including the switching
on of a range of defence mechanisms to afford protection against UV
radiation. The best studied is the production of pigments, especially
flavanoids, which will act to screen out the UV-B. Bornman et al.
describe how the production of polyphenols is stimulated, with differen-
tial production of certain types, and that the largest concentration of
pigments is located in the epidermis, effectively reducing the penetra-
tion of UV-B deeper into the mesophyll cells of the leaf. This type
of response involves the stimulation of expression of particular genes,
xvi Preface
implying specific UV-B light detection systems and signal transduction
processes which lead to the regulation of transcription. The question of
perception of UV, and the relationship between perception of UV-A,
UV-B and blue light is discussed by Jenkins, Fuglevand and Christie.
For these sorts of studies, essentially at the molecular and cellular
level, the absolute amount of UV radiation does not need to equate
closely to ambient levels, since the aim is to investigate the individual
mechanisms associated with response to UV. It appears that responses
to UV-B represent a new area of photomorphogenesis that has, to date,
received little attention, and where new questions are consequently aris-
ing. For example, is there a 'simple' UV-B receptor, or are there several
types of receptor, as appears to be the case with blue light responses?
Is it possible to determine whether a response is a consequence of a
'damage' reaction, or is an adaptive response following specific percep-
tion? (Britt suggests that this discrimination might be achieved by treat-
ing a mutant which is defective in recovery; if there is still a response,
then the effect is one of damage, and is not a function of a 'receptor'.)
Understanding the molecular basis of perception and signal transduction
is likely to be of direct relevance to a scenario of global climate change.
Effects seen at the whole-plant level, especially under natural con-
ditions, are likely to involve both direct effects and indirect effects.
Indirect effects are those mediated by radiation-induced changes in the
plant environment, or changes in the plant which are of importance
mainly in relation to other organisms. Examples include effects on other
plants which compete with the plant under consideration (see chapter
by Caldwell), effects on nutrient mobilisation, effects on herbivores and
micro-organisms of importance to the plant. To understand these effects
of UV requires the study of several components of natural ecosystems,
and only recently have such studies been started. Unlike studies of
direct effects, where responses occur quite rapidly, studies of indirect
effects need to be carried out over a long period of time, since effects
are likely to be of a slow, cumulative nature. To date, more effort has
been given to understanding the direct effects, and indeed these are
probably the most important ones in crops, growing as they do in a
partly human-controlled environment, and mostly in monoculture.
Indirect effects, however, may be more important for wild plants in a
natural environment.
Outdoor studies require the construction of suitable irradiation facili-
ties; the UK now has four sites with such facilities, at Lancaster Univer-
sity, Sheffield University, Monks Wood (Institute of Terrestrial
Ecology) and Wellesbourne (Horticulture Research International). At
these sites, supplementary UV irradiation is provided in a modulated
 Preface xvii
form; most researchers carrying out experiments in the field recognise
that modulated systems, where lamp outputs are adjusted to give a sup-
plement which is a constant value above ambient (changing with cloud
cover, for example) are preferable to square wave additions (where
lamps are simply on or off). These outdoor facilities in the UK currently
surpass those elsewhere in the world.
For outdoor studies, supplementary radiation should be related to
realistic ozone depletion scenarios. To achieve this, it is crucial to have
accurate information about the action spectrum of the response being
studied. An action spectrum indicates the relative effectiveness of dif-
ferent wavelengths of radiation in bringing about a particular response;
the relative effectiveness, derived from the action spectrum, can then
be multiplied by the irradiance at each wavelength, and summed over
the appropriate wavelength range to give the important function, bio-
logically effective radiation. This term is most important in calculating
predicted doses of UV resulting from different ozone depletion scen-
arios, but is also important in determining the dose provided by sup-
plementary lamps, the spectrum of which is quite different from that of
sunlight (see chapter by Paul). Throughout this volume the action spec-
trum used to calculate the biologically effective dose of supplementary
UV will be quoted. There are several that can be used, the most
common being derived from the Caldwell generalised plant action spec-
trum, normalised at 300 nm (PAS300). However, this spectrum is a
composite from those available in the early 1970s, and it is quite likely
that particular responses will have action spectra which are slightly or
substantially different from this. The implications of this are discussed
in the chapter by Holmes, where evidence is also presented that, when
UV is given over an extended period of time, the action spectrum for
overall growth has a significant 'tail' in the UV-A region. The reason
for this is that, whereas short-term exposures will give spectra charac-
teristic of absorption by a particular molecule (for example DNA), over
an extended period, a number of processes may be involved, each with
a slightly different action spectrum, added to which the plants will pro-
duce screening pigments which may alter the action spectrum.
The use of appropriate controls for outdoor arrays is a further issue
also now receiving some attention. Tubes used to provide supplemen-
tary UV-B emit some energy at wavelengths below 280 nm, in the
UV-C region. To exclude this, tubes are wrapped with cellulose acetate,
which does not transmit below 290 nm. Control treatments have usually
been unenergised tubes, providing the same shade as operational tubes.
However, the UV-B tubes do emit a certain amount of UV-A, so that
treatments with supplementary UV-B will also have a certain sup-
xviii Preface
plementation of UV-A above ambient. This can be overcome by an
additional control treatment in which tubes are covered with polyester
foil, which excludes wavelengths < 315 nm, thus providing a treatment
which allows the effects of UV-B and UV-A to be separated. Since
there is some evidence that UV-A has biological activity (see chapter
by McLeod & Newsham), such an additional treatment is desirable.
Since there is good evidence that responses to UV-B continue into the
UV-A part of the spectrum, meters used should cover the UV-A as
well. Detailed measurements, calibration of meters against standardised
spectroradiometers and characterisation of the radiometric information,
allowing comparisons to be made between different experimental sys-
tems, are also crucial.
Effects on growth and interactions between ecosystem components
are reviewed in this volume for a range of species and habitats. Aquatic
ecosystems, which are responsible for half of the biomass production
of the planet, are reviewed by Hader, who discusses the penetration of
solar UV radiation into the water column, the biological sensitivity of
aquatic organisms, and the effectiveness of mitigating and protective
measures in aquatic organisms. It is suggested that aquatic systems are
already under UV stress, and that further depletion may result in
changes in species composition, with significant consequences for pro-
ductivity.
Effects on crops are reviewed in the chapter by Corlett et al.\
although glasshouse and controlled environment experiments suggest
that UV causes significant damage, evidence from field studies suggests
that, even with a large ozone depletion, the impact on commercial mono-
cultures may be limted, changes in morphology and pigment concen-
trations being more likely than large changes in productivity. Rozema,
van de Staaij & Tosserams draw similar conclusions with respect to
natural ecosystems, namely that effects on canopy architecture, com-
petitive relationships and litter decomposition are as important as direct
effects on productivity. A detailed description of how changes in spec-
ies balance may come about, owing to slight changes in morphology,
is given in the chapter by Caldwell.
Less research has been carried out into effects on more remote sys-
tems, such as upland moors and Arctic ecosystems. In Arctic regions,
radiation levels are less than at temperate latitudes, but changes in the
ozone layer are greater, giving the possibility of greater relative
increases in UV. Moorlands and Arctic ecosystems are characterised by
vegetation that is slow growing and perennial in nature, allowing effects
to accumulate. Particularly in the Arctic, the low temperature may also
impair repair processes. The chapters by Bjorn et al. and by Moody,
 Preface xix
Coop and Paul review effects on plant growth and on other components
of these ecosystems, such as microbial activity, decomposition and her-
bivory. Moody et al. show that, in UK upland moorlands, the effects of
UV-B on plant growth are generally small in comparison with the
effects of CO2, and that their opposing effects tend to cancel each other.
As a result, biomass under high CO2 plus high UV-B treatments is
almost the same as that for ambient UV-B plus ambient CO2. Effects
of UV-B on microbial-plant interactions are complex; changes in plant
chemical composition can reduce microbial activity, while a direct
effect of UV-B during decomposition is to decrease colonisation by
fungal decomposers. Increased UV-B may therefore lead to a slowing
down of nutrient recycling.
Impacts on forest ecosystems are thoroughly reviewed by McLeod
and Newsham, who consider the distribution of UV through forest can-
opies, direct effects on growth and physiology, where there is more
evidence for stimulation of pigment accumulation than reductions in
growth, and also impacts on leaf decomposition, micro-organisms,
insects and nutrient recycling. Interestingly, it appears that increases in
leaf thickness are due to UV-B, while an increase in lammas shoot
length and some aspects of herbivory may be specifically due to elev-
ated UV-A.
Finally, some specific examples of pathogen/plant interactions are
reviewed in the chapter by Paul. Again, there is significant variation
between species: Septoria tritici appears to be sensitive to UV-B, in
that spore germination is inhibited by elevated UV-B, although strains
from lower latitudes (where ambient UV-B is higher than in the UK)
are more resistant. In other cases, the interaction is more complex;
changes in plant chemical composition may alter the activity of fungal
pathogens. Paul also considers in detail the consequences of using
different action spectra in determining the UV-B doses supplied from
supplementation with artificial lights, highlighting the very large
differences in biologically effective dose that can be derived.
Despite the significant progress made in recent years, or perhaps
more accurately, because of the progress made, a number of questions
arise. At the climate level, is the thinning of the ozone layer having a
real effect on terrestrial levels of UV-B? At the biological level, is it
possible to separate damage and adaptive responses, and further, is it
possible to link responses at the molecular level with those occurring
at the eco-system level? Plant responses to UV-B is an exciting area;
new insights into fundamental mechanisms are being gained, while the
subject has very real significance in the light of changes in climate.
However, many of the studies need to be carried out over longer time
xx Preface
period to provide definitive answers to questions such as cumulative
effects of UV-B, effects of UV-B at the ecosystem level, and interac-
tions of elevated UV-B with other stress factors. Further information
on UV-B, and other aspects of plant photobiology can be found across
the Worldwide Web. A good starting point is the Plant Photobiology
page, the address for which is http://cc.joensuu.fi/photobio/photobio.
html
Peter J. Lumsden
HRI Wellesbourne
Warwick
1996
PART i The ozone layer and UV-B
radiation
 J.A. PYLE

Global ozone depletion: observations

and theory

Introduction
It is now well known that ozone concentrations in the stratosphere have
declined during the last 25 years as a consequence of the emission
into the atmosphere of a variety of chlorine- and bromine-containing
compounds. This decline in the thickness of the ozone layer could have
important consequences. Firstly, ozone is an important climate gas.
Absorption of solar radiation by ozone controls the temperature of the
stratosphere and leads directly to the stable stratification of the strato-
sphere. Changes in ozone can be expected to lead to changes in the
climate of the stratosphere; these changes may also be important for the
circulation of the troposphere and hence for weather. In addition, ozone
is a greenhouse gas, absorbing radiation in the infra-red region of the
spectrum. A decrease of ozone in the lower stratosphere can act to cool
the climate system, counteracting the impact of the growth of carbon
dioxide and other greenhouse gases. Secondly, because ozone absorbs
solar ultra-violet radiation, any reduction in the stratospheric ozone
abundance will lead to enhanced intensity of ultra-violet radiation at
the surface. Biological systems are particularly sensitive to short
wavelength radiation at less than about 300 nm. Increases in the
intensity at these wavelengths may have an influence on the health
of humans, of plants (see later chapters in this volume) and of other
animals.
Ozone change will be a controlling influence on changes in surface
ultra-violet radiation. In this chapter the evidence for ozone change will
first be presented and the causes of the ozone decline will be discussed.
Since the ozone decline is related to the accumulation in the strato-
sphere of man-made chlorine and bromine compounds, the reduction in
the emission of these compounds should lead to an eventual recovery
of the ozone layer. Factors controlling the rate of recovery will be pre-
sented. Finally, some outstanding issues will be raised.
4 J.A. PYLE

Ozone changes in the stratosphere

The possibility that chlorine compounds could significantly perturb the
stratospheric ozone layer was first proposed by Molina and Rowland
(1974). They showed that a build-up of chlorine compounds in the
stratosphere would be the necessary consequence of the substantial
growth during the 1960s and early 1970s in the production and emission
of a number of chlorinated compounds, which were being used as aero-
sol propellants and in foam blowing and refrigeration. As they move
upwards through the stratosphere, these compounds, which are unreact-
ive in the troposphere, would be subject to increasingly intense ener-
getic solar radiation which could dissociate them. This would lead to
the liberation of free chlorine atoms which could then take part in very
efficient catalytic chemical cycles to destroy ozone. In their theory, the
largest ozone depletions would occur in the upper stratosphere at around
40 km.
The first clear evidence for ozone depletion came with the discovery
of the Antarctic 'ozone hole' (Farman, Gardiner & Shanklin, 1985).
Data collected at the British Antarctic Survey base at Halley Bay since
1957 showed that a substantial decline in springtime ozone values had
occurred during the 1980s. The result was surprising in that the details
of the loss were different from the predictions of Molina and Rowland
(1974). Nevertheless, it was soon confirmed that the growth in concen-
trations of chlorine compounds was the cause of the ozone loss (see
next section).
The discovery of the 'ozone hole' prompted a massive research
effort. This has involved detailed studies of the chemical and physical
mechanisms responsible for the depletion. In addition, data sets of the
ozone concentration from both ground-based and satellite instruments
have been carefully analysed to determine trends in ozone not just in
Antarctica but at all latitudes. Figure 1 shows the trends in ozone calcu-
lated during the 1980s from the TOMS satellite instrument (Stolarski et
al., 1991). Analyses with different data sets show the same basic fea-
tures. The most recent analyses were reviewed by WMO (1995) and
SORG (1996). Here, only the salient features will be indicated. While
the largest depletion is evident in Antarctica in the spring, there is also
evidence of a substantial ozone decline in high latitudes of the Northern
Hemisphere in winter and spring. In both hemispheres the data show
that there has been a loss of ozone since the 1970s. Although the Figure
indicates that there has also been a decline in tropical latitudes, the
changes there are small and are not statistically significant.
The most recent analyses (see SORG, 1996) show that ozone has
 Global ozone depletion
80N
NO
DATA

60N -

40N -

20N
LU
Q

1-0 v -.8
-2.0^1.5
I lK"l 3 ' 0 ^\\
J F M A M J J A S O N D
MONTH

Fig. 1. Total ozone trend (% per annum) determined from TOMS

satellite data as a function of latitude and season. The lightly shaded
areas indicate regions where the trends are not statistically significant.
Poleward of the heavy solid lines are the Arctic and Antarctic polar
nights where TOMS was unable to make measurements. (Figure from
Stolarski et al, 1991).

declined globally by about 4-5% since 1979. In middle latitudes, the

annually averaged loss in the same period is about 7%. At northern
mid-latitudes, including the UK, in winter and spring the accumulated
loss since 1979 is now about 11%.
In Antarctica, the 'ozone hole' occurs each spring. Values for the
ozone column (a measure of the sum of all the ozone molecules between
the surface and the top of the atmosphere) in October are now about
one-third of those observed in the 1960s. Each spring, nearly all the
ozone at altitudes between 15 and 20 km is removed in a period of
about six weeks. While there are interannual variations in the depth of
the ozone hole, it is clear that the effect is close to saturation (once all
the ozone is removed, no further depletion can occur).
Evidence for the ozone decline in northern high latitudes has
6 J.A. PYLE
strengthened in the last few years with, for example, record low values
being reported at various stations during the winters of 1994/1995 and
1995/96. The causes of these losses will be investigated further in the
next section.

The causes of ozone depletion

Polar regions
The discovery of the Antarctic ozone hole initially surprised the scien-
tific community. The nature of the ozone loss was quite different to that
suggested by Molina and Rowland (1974). It was occurring in southern
polar latitudes, with the loss predominantly below 20 km altitude. The
loss was mainly confined to the polar spring season and developed very
rapidly each year. None of these details was predicted in Rowland and
Molina's theory.
After a decade of intensive research, the reasons for polar ozone loss
have become reasonably clear. It is certain now that ozone is depleted
by reactions involving chlorine and bromine compounds, present in the
atmosphere following a variety of anthropogenic activities. In the tropo-
sphere the chlorine and bromine are held in stable compounds, the chlo-
rofluorocarbons and halons. In the stratosphere these compounds can
be dissociated. The majority of the chlorine and bromine is then trans-
formed into other compounds ('reservoirs') which themselves do not
destroy ozone. However, it is now known that reactions on surfaces can
turn these reservoirs (for example, HC1 and C1ONO2) into active forms
(such as Cl and CIO) which, in the presence of sunlight, do destroy
ozone. The polar lower stratosphere provides the conditions for these
processes to occur. During winter, a strong westerly circumpolar flow
(the polar vortex) is established. Within the polar vortex temperatures
become very low and polar stratospheric clouds (PSCs) can form. These
PSCs provide the surfaces on which the reservoirs are turned into active
forms. When sunlight returns to the polar regions in springtime, rapid
ozone depletion can occur. Thus the sequence leading to ozone
depletion requires that, first, temperatures are low, so that PSCs can
form and release active chlorine, and, secondly, sunlight is present to
drive the photochemical destruction cycles. (For a more complete
description of the relevant processes see, for example, WMO, 1995.)
The conditions in the Antarctic lower stratosphere are particularly
favourable for ozone depletion. Each winter and spring, temperatures
drop sufficiently for PSCs to form. The low temperatures persist into
the spring when sunlight returns. In contrast, during winter the lower
stratosphere over the Arctic is warmer than its southern hemisphere
 Global ozone depletion 1
counterpart and temperatures for PSC formation are less widespread.
The lowest temperatures may occur during the darkness of polar night.
For these reasons, depletion in the north was not expected to be as
severe as in the south. Nevertheless, in the late 1980s it became clear
that conditions conducive to ozone loss do occur in the north and a
number of detailed research programmes, including the European Arctic
Stratospheric Ozone Experiment (EASOE) in the winter of 1991/92 (see
Pyle et aL, 1994) and the Second European Stratospheric Arctic and
Middle latitude Experiment (SESAME) in the winters of 1993/94 and
1994/95 (see, for example, Pyle et al, 1995), have investigated northern
polar loss.
It is now evident that chemical destruction of ozone has also occurred
in the Arctic lower stratosphere, where a wide variety of measurements
have shown that active chlorine is present following low temperatures.
Studies using, for example, ozone sonde measurements have confirmed
that local losses in the lower stratosphere approaching 2% per day
occurred during 1994/95 (Rex et al., 1996), with an accumulated loss
throughout the winter amounting to about 50% at 20 km inside the polar
vortex. Numerical modelling studies have shown that large interannual
variability can be expected in the magnitude of the ozone depletion.
The model studies confirm that quite significant losses can be expected
in cold stratospheric winters like 1994/95 and 1995/96 (Chipperfield,
Lee & Pyle, 1996).
As discussed above, there are important differences between the
Arctic and Antarctic polar vortices. In the north, the vortex is more
variable and more mobile. In the south, the vortex is usually centred
close to the pole but in the north the location of the vortex is quite
variable and can be influenced strongly by weather systems in the tropo-
sphere. In consequence, the vortex is often located over northern
Europe. On these occasions, the air in the lower stratosphere above
populated regions of Europe can be characteristic of the chemically
perturbed vortex. Thus, in March 1996, record low values of ozone
were reported at the UK measurement sites in Cambourne and Lerwick
when the polar vortex passed overhead. In the context of the middle
latitude decline, discussed below, it is important to realise that these
low ozone events are relatively short-lived and that the ozone-depleted
air will subsequently move away from the UK as the vortex sweeps
back towards more northerly latitudes.

Middle latitudes
The mechanisms leading to losses of ozone in polar latitudes are now
quite well understood. Much more controversial is the cause of the
8 J.A. PYLE

decline in ozone in middle latitudes of the northern hemisphere,

amounting to about 7% (annual average) since 1979. As discussed,
polar vortex air can sometimes be seen over middle latitudes where low
ozone can then be measured. However, it is clear that this cannot be
the main explanation of the annually averaged trends in middle lati-
tudes, and other theories have therefore, been advanced. Most theories
implicate the halogen compounds, but the precise details of the pro-
cesses involved remain in dispute. One possibility is that the ozone
depletion occurs in polar latitudes and this air is then mixed irreversibly
into middle latitudes causing a general 'dilution' of ozone levels there.
A second possibility is that air is primed for ozone depletion by the
reactions on PSCs in polar regions, but is then transported southward,
and possibly mixed, before the depletion occurs. If this process operates
continuously (like a 'flowing processor', see Mclntyre, 1995), then
large ozone loss might occur in mid-latitudes. A further possibility is
that the chlorine is activated in situ in middle latitudes, possibly on
sulphate aerosol, followed by local ozone depletion.
Studies in the last few years suggest that all three mechanisms are
involved. It is clear that polar air can be mixed into middle latitudes
after filaments of air are stripped from the edge of the polar vortex (see,
for example, Pyle et ai, 1995). However, this may not be the major
factor, and increasing evidence is accumulating for the importance of
the in situ reactions on sulphate aerosol which can lead to the initiation
of ozone destruction cycles, similar to those seen in polar latitudes but
operating more slowly in middle latitudes (see SORG, 1996).
What is now clear is that both chlorine and bromine compounds
are involved in the middle latitude decline. However, we only have a
qualitative, and not a quantitative, understanding of the loss. The lack
of quantitative understanding means that we cannot predict accurately
the course of a recovery of ozone amounts in middle latitudes.

Ozone recovery - some outstanding questions

International regulations to control the emissions of certain ozone-
destroying substances have been established since the discovery of the
'ozone hole' and the development of a clear understanding of the mech-
anisms of the ozone loss. Production of the major carriers of chlorine
to the stratosphere, the CFCs, are now phased out with a few exceptions
for developing countries and essential uses. Regulations also control the
emissions of the chlorine-containing transitional compounds which
have replaced the CFCs. Similarly, production of the Halons, which can
carry bromine to the stratosphere, has now ceased and some of the uses
 Global ozone depletion 9
of methyl bromide are to be controlled. The international action began
with the Montreal Protocol in 1987, followed by amendments to the
Protocol in London (1990), Copenhagen (1992) and Vienna (1995). The
consequence is that accumulated chlorine loading of the troposphere
has already reached its maximum; maximum chlorine levels in the
stratosphere are expected within the next few years. Peak concentrations
of bromine in the stratosphere are expected to occur slightly later, per-
haps by about 2010.
Stratospheric ozone levels should start to recover once the concen-
trations of chlorine and bromine begin to fall. Thus, the next decade or
so represents the period of greatest risk when, for example, large ozone
loss could continue to occur in the Arctic vortex. The lifetime of the
CFCs is long, so that their removal from the stratosphere will be slow,
and concentrations of chlorine compounds are expected to remain high
enough in the stratosphere to produce the springtime Antarctic 'ozone
hole' at least until the middle of the next century. Prediction about the
rate of recovery in middle latitudes is made difficult by our lack of a
quantitative understanding of the observed depletion.
Thus, if chlorine and bromine concentrations fall, and all else remains
the same, the ozone layer is expected to recover, albeit slowly. How-
ever, all else may not remain the same. For example, a downward trend
in the temperatures in the lower stratosphere has been reported (see, for
example, Oort & Liu, 1993; SORG, 1996). This could lead to more
widespread conditions for the formation of polar stratospheric clouds
and, hence, to the conditions for chemical destruction of ozone. The
conditions inside the Arctic vortex during the last two winters are par-
ticularly intriguing in this context. Both 1994/95 and 1995/96 saw the
establishment of record low temperatures in the lower polar strato-
sphere. We do not know whether these records were the result of purely
natural variability or whether they represent some kind of trend (for
example, caused by increasing concentrations of greenhouse gases or
reduced concentrations of ozone). The next few winters will provide
the answer. What is quite clear is that if the Arctic lower stratosphere
continues to cool, the conditions will become more like those found in
Antarctica and will favour ozone loss. Any cooling would inevitably
delay the recovery in ozone expected to follow the decreases in chlorine
and bromine loading.

Conclusions
Ozone depletion is widespread across both polar and middle latitudes
and will affect both the climate system and the penetration of ultraviolet
10 J.A. PYLE
radiation to the earth's surface. The causes of polar loss are well under-
stood in terms of a chemical depletion involving chlorine and bromine
compounds. In recent Arctic winters, unequivocal evidence has
emerged for a chemical loss similar to that seen in the Antarctic. For
example, between January and March 1996, about 50% of the ozone in
the Arctic lower stratosphere was destroyed chemically. A quantitative
understanding of the observed decline in ozone amounts in middle lati-
tude is still not available, although it is now clear that, again, chlorine
and bromine compounds play a role.
International regulations, beginning with the Montreal Protocol in
1987, have begun to have an impact on the levels of ozone-destroying
compounds in the atmosphere. However* recovery will be slow. Thus,
large ozone losses in the Arctic, comparable with those seen in the
last two winters, can be expected during the next decade during cold
stratospheric winters. Meanwhile the 'ozone hole' should remain a fea-
ture of the Antarctic springtime stratosphere until the middle of the next
century. Recovery may be made even slower if other conditions in the
stratosphere change. Thus, if the very low temperatures in the last two
Arctic winters represent part of a trend, instead of being purely the
result of natural variability, then continuing large ozone loss can be
expected and the pace of recovery will be slowed.

References
Chipperfield, M.P., Lee, A.M. & Pyle, J.A. (1996). Model calculations
of ozone depletion in the Arctic polar vortex for 1991-92 to 1994-
95. Geophysical Research Letters, 23, 559-62.
Farman, J.C., Gardiner, B.G. & Shanklin, J.D. (1985). Large losses
of total ozone in Antarctica reveal seasonal C1OX-NOX interaction.
Nature, 35, 207-10.
Mclntyre, M.E. (1995). The stratospheric polar vortex and sub-vortex:
fluid dynamics and middle latitude ozone loss. Philosophical Trans-
actions of the Royal Society, London A, 352, 227^0.
Molina, M. & Rowland, F.S. (1974). Stratospheric sink for chloro-
fluoromethanes: chlorine atom catalyzed destruction of ozone.
Nature, 249, 810-12.
Oort, A.H. & Liu, H. (1993). Upper-air temperature trends over the
globe, 1958-1989. Journal of Climate, 6, 292-307.
Pyle, J.A., Chipperfield, M.P., Kilbane-Dawe, L, Lee, A.M., Stimpfle,
R.M., Kohn, D., Renger, W. & Waters, J.W. (1995). Early model-
ling results from the SESAME and ASHOE campaigns. Faraday
Discussions, 100, 371-87.
Pyle, J.A., Harris, N.R.P., Farman, J.C., Arnold, F., Braathen, G.,
Cox, R.A., Faucon, P., Jones, R.L., Megie, G., O'Neill, A., Platt,
Global ozone depletion 11
V., Pommereau, J.-P., Schmidt, V. & Stordal, F. (1994). An over-
view of the EASOE campaign. Geophysical Research Letters, 21,
1191-5.
Rex, M.P., von der Gathen (& 35 co-authors) (1996). Chemical ozone
loss in the Arctic winters 1991/92 and 1994/95 (Match), Proceed-
ings of the Third European Symposium on Polar Ozone Research,
Schlierse, 18-22 September, 1995, European Commission Air Pol-
lution Research Report, 56, 586-9.
SORG. (1996). Stratospheric Ozone 1996, United Kingdom Strato-
spheric Ozone Review Group. Fifth report. HMSO, London.
Stolarski, R.S., Bloomfield, P., McPeters, R.D. & Herman, J.R.
(1991). Total ozone trends deduced from Nimbus 7 TOMS data.
Geophysical Research Letters, 18, 1015-18.
WMO. (1995). Scientific Assessment of Ozone Depletion: 1994,
WMO Global ozone research and monitoring project - report no.
37, Geneva.
 A.R. WEBB

Monitoring changes in UV-B

radiation

Introduction
The biological consequences of ozone depletion, mediated through an
increase in ultraviolet-B (UV-B) radiation, have been cause for concern,
prediction and speculation for many years. Estimating the potential
effects of ozone depletion involves several steps:
1. Estimating the ozone depletion that might realistically be
expected over a given region of the world (this requires
assumptions about, for example, compliance with the Mon-
treal Protocol, or not). Alternatively, observed ozone
depletions to date can be used to assess the changes already
experienced.
2. Calculating changes in UV-B due to changes in ozone. The
assumption is that all else remains unchanged and these
calculations are usually made for clear-sky conditions. If
changes in UV-B irradiances have been observed, then they
may be used instead, but they cannot necessarily be attri-
buted solely to changes in ozone.
3. The exposure of biological systems to the available UV-B
must be assessed. For plants growing at a single location,
this can be assumed to remain unchanged, but for mobile
systems (animals, fish, and especially people) adaptive
behaviour is possible.
4. The biological (or chemical) results of exposure to the
(changed) UV-B must be predicted, based on experiment
and observation. Response may depend upon accumulated
dose, upon reaching some threshold dose, and upon poss-
ible protective mechanisms, for example, the build-up of
UV-absorbing pigments (melanin in humans, flavonoids in
plants).
It is clear that step number 2, assessment of changes in UV radiation,
14 A.R. WEBB

straddles the gap between atmospheric cause and biological effect, and
in doing so becomes the focal point for two different questions:
(a) Atmospheric. What is the expected change in UV-B due to
ozone depletion (and can it be observed, and if not, why
not?), or the corollory of this, can any observed change in
UV-B be attributed solely to ozone depletion?
(b) Biological. What is the real change in available UV-B in
the biosphere, regardless of atmospheric processes?
In search of an answer to both questions, the same data and the same
predictive techniques are used, and as there is not enough information
available in either respect there is still doubt as to whether UV is chang-
ing over much of the earth's surface. This does not contradict the basic
premiss that less ozone in the atmosphere means more UV-B at the
ground, rather it indicates how many other factors have to be considered
in trying to apply this otherwise simple relationship.

Atmospheric factors affecting UV radiation reaching

the biosphere
The solar zenith angle, determined by season and latitude, controls the
underlying diurnal and annual changes in radiation of all wavelengths
of solar radiation reaching the earth's surface. However, zenith angle
and other astronomical factors such as earth-sun distance are considered
constants in considering possible changes in UV-B radiation on a time-
scale of decades and will not be discussed any further.
Ozone is the chief selective absorber of UV-B radiation in the atmos-
phere, but it is by no means the only variable attenuator. Clouds and
aerosols can have a vast effect on UV at the surface on short timescales
(minutes to years) and result in a very noisy long-term (decades) pattern
of surface irradiances from which to try and extract an ozone-related
change which, at its worst, is often small compared to the noise. The
uncertainty is compounded by the fact that ozone itself is highly vari-
able on a day-to-day basis, and dynamics (at least in mid-latitudes)
often conspires to provide low ozone and clear skies together (high
pressure systems) or high ozone and cloud together (low pressure
systems). A sunny 'anticyclonic' summer may thus provide a far higher
dose of UV then a preceding dull summer of passing depressions, while
having nothing at all to do with ozone depletion. Over a sufficiently
long time period (30 years +) this natural variability in the weather can
be treated statistically to produce an expected range of conditions, a
climatology. Thus we have an expected range of ozone column thick-
 Monitoring changes in UV-B radiation 15
nesses for a given location, and excursions outside this normal range
may be single extreme events (the ozone equivalent of a 100-year
storm), or if persistent may represent a changing climatology (attributed
in this case to chemical ozone depletion). Such ozone trends (see chap-
ter by Pyle) might be expected to lead to similar observed changes in
UV-B, if every other aspect of the climate and the environment remains
the same. Should cloud climatology change, one hypothesis associated
with global warming (IPCC, 1990), its effect could be either to enhance
or offset ozone-related changes in UV radiation, depending on how the
cloud increased or decreased. Aerosols and pollution, including low-
level ozone, decrease the UV reaching the surface. Thus, increasingly
poor air quality in urban and industrial areas over several decades may
again disguise the effects of small ozone losses in the stratosphere. As
methods to reduce air pollution become more advanced, declines in
pollution and stratospheric ozone could act in the same direction to
produce an increase in UV radiation.
One further aspect of change which could be significant in some
regions is the land surface or surface use. Surface reflectivity (albedo)
is low for UV wavelengths and most vegetative surfaces. It is somewhat
higher for rocks and concrete, and can be extremely high, over 90%,
for clean snow (Madronich, 1993). From an atmospheric point of view,
changing albedo alters the amount of radiation which is reflected back
to the atmosphere from the ground and is then available to undergo
further back-scattering and return to ground level. Increasing albedo
generally increases the overall surface irradiance. Biologically, the
effect of increasing albedo is likely to be even greater. Not only is an
organism exposed to greater irradiance from above, but it will also
receive directly reflected radiation from below, and at angles which may
enable exposure of otherwise protected areas. The greatest contrast in
albedo is between snow and vegetation from season to season (normal)
or climatologically - another hypothesis of global warming.
To try to predict the outcome of the combination of ozone depletion,
global warming and a cleaner air policy on UV radiation at the surface
would be highly speculative, yet all may have influenced the UV
measurements made to date, while ozone depletion is often the only
factor which can be confidently considered in calculating ozone
depletion effects. Our knowledge of changes in cloud, aerosol, albedo,
and their detailed effects on UV radiative transfer, is so scant that pre-
dictions are almost always restricted to clear-sky calculations where the
only variable allowed to change is ozone. This gives a clear-cut answer
which is not often observed. However, the lack of evidence of an undis-
puted trend in UV-B radiation over much of the globe is not due solely
16 A.R. WEBB
to the confusions wrought by cloud and aerosol, but also to the UV
instrumentation and its very sparse deployment for any significant
length of time.

UV monitoring equipment
The two basic categories of UV monitoring equipment are the broad-
band radiometer and the spectroradiometer. A third category, the multi-
filter instrument lies part-way between the other two categories, provid-
ing data for a discrete number of narrow spectral bands. There is only
one report in the literature from a multi-filter instrument in use for a
significant period of time (Correll et al., 1992), and therefore this type
of instrument will not be discussed in detail.
The broadband instrument is the one that has been in operational use
for the greatest time. It is simpler, cheaper and more robust to operate
than the spectroradiometer, and is therefore also the most widely
deployed type of instrument. There are several different versions of the
broadband instrument, available from different manufacturers, but the
majority of them purport to measure the same quantity - the ery-
themally effective UV radiation incident on a horizontal surface. The
erythemally effective radiation (EER) is defined as the solar spectrum
(10 weighted with the erythemal action spectrum (A^, the effectiveness
of each wavelength in producing erythema or sunburn) and integrated
over the entire solar UV waveband (280-400 nm), thus:
EER = f L A* dX
In reality, each instrument measures the integral of the solar spectrum
and the individual instrument's response spectrum (R0. The response
spectra vary somewhat from manufacturer to manufacturer and even
from instrument to instrument of the same make, and none of them
exactly matches the erythemal action spectrum (of which there are sev-
eral, the McKinlay-Diffey (1987) or CIE response being the one most
commonly used). The response spectrum can also change with age as
the optical elements of the instrument degrade, so the stability must be
checked if long-term monitoring is the intended use of the equipment.
Not all broadband instruments measure EER; some of them have been
designed to match a different action spectrum, or to measure
unweighted UV across a designated waveband, but long-term records
are not generally reported from such instruments in the context of ozone
depletion and will not be discussed.
Spectroradiometers measure the UV irradiance at a series of discrete
wavelengths to provide a solar spectrum showing the change of inten-
 Monitoring changes in UV-B radiation 17
sity with wavelength. As with broadband instruments, there are many
makes of spectroradiometer capable of measuring at different wave-
length intervals (resolution), and with varying degrees of compliance to
the ideal of discrete wavelength measurements. All spectrometers have
a finite slit width through which radiation of a designated wavelength
is directed on its way to the detector. A degree of radiation from neigh-
bouring wavelengths (near straylight) inevitably passes through the slit
at the same time and also reaches the detector, to be falsely attributed
to the nominal wavelength of measurement. The intensity of the ground-
level solar UV radiation drops by several orders of magnitude across
the narrow UV-B part of the spectrum, so reducing this near straylight
becomes vitally important, the more so towards shorter wavelengths.
Random photons bouncing around in the instrument from any of the
incoming radiation (far straylight) must also be suppressed and pre-
vented from reaching the detector. To achieve suitable straylight rejec-
tion, a double monochromator is generally employed.
It is clear that there is no standard instrument for solar UV measure-
ments, and that there is variety even between the types of instrument,
which, even assuming perfect calibrations and other common features
(e.g. cosine response), will give differences in the measurements made
with individual instruments. The importance of these differences
depends upon the way in which the data is to be used.
In looking for a change in UV radiation with time the most important
property of any instrument is its proven stability over a long time
period. This can be achieved by regular calibration of the equipment,
the required frequency depending on experience and the inherent stab-
ility of the components of the instrument. Once internal site-system
stability limits have been determined, the data record from that site can
be used to identify any changes in solar UV which may be greater than
the uncertainty in stability. This holds regardless of the relationship of
the site instrument to any other instruments, or the calibration reference
to other calibration references. So long as there is internal consistency
maintained for the duration of the data record, the possibility to detect
change at a single site exists.
Site stability can only be assessed and maintained by careful and
sufficiently frequent calibrations. The method of calibration, and the
frequency with which it is required, will depend on the type of instru-
ment in use. Broadband instruments are usually calibrated either against
other broadband instruments or against spectroradiometers. Spectro-
radiometers are calibrated against standard lamps, and all absolute
irradiance calibrations should eventually revert back to a National
Standards Laboratory reference. The greater the number of transfer
18 A.R. WEBB
calibrations between the Standards Laboratory and the site calibration,
the greater the uncertainty in the absolute irradiance measurements on
site. For a single site interested only in change (stability) this uncer-
tainty is not an initial problem (Fig. 1): the absolute irradiance may
only be known to ±10%, but a lamp should have much greater stability
at its unknown position within this range. However, when some link in
the calibration chain has to be changed (as inevitably happens when
lamps age and degrade), then great care must be taken that a shift in the
reference irradiance level is not introduced in all following calibration
transfers.
If the data at one site are to be compared with data collected at other
sites, then more attention must be paid to the agreement between the
different monitoring instruments, to ensure that any differences ident-
ified in UV radiation are correctly attributed to the site location and are
not really a consequence of unmatched instruments or their calibrations.
At this point, position on the absolute irradiance scale does become
important (Fig. 1), in addition to stability which should also be main-
tained with the same vigour as for an isolated site. Achieving absolute
agreement between different instruments depends upon both the instru-
ments' characteristics and the reference standards to which their cali-
brations are referred. Calibrated lamps from National Standards Labora-
tories have uncertainties of 2-3% at the short UV-B wavelengths,

Absolute
uncertainty

>

2 4 Relative 1 t
S I it uncertainty ; ^ ^ ^ tj Single site
small
Change in calibration increases uncertainty oi
f complete data set if not rapidly identified

I t ^ Uncertainty
]o •i f• Relative uncertainties (t Absolute I i n total
total
Network
| small discrepancies • network database
I 2 small
o
CO

€ o
1 2 3 4 5 6 7 8 9 10
Time (e.g. months)
Fig. 1. Stability, relative and absolute irradiance standards for single
and multiple monitoring sites.
 Monitoring changes in UV-B radiation 19
reducing to approximately 1% in the UV-A. Each transfer of the absol-
ute standard to another lamp or instrument introduces additional uncer-
tainty. Thus, in the unfortunate situation when uncertainties might be
additive, two well-calibrated instruments may differ in their absolute
UV-B measurements of the same source by 4-5%. Further differences
in broadband response functions, spectroradiometer slit functions, stray-
light, and cosine responses (both types), can add further to the discrep-
ancies. This point has been amply illustrated by a number of inter-
national intercomparisons of both spectroradiometers and broadband
radiometers (Gardiner & Kirsch, 1993, 1994, 1995; Koskela, 1994;
Seckmeyer et al., 1995; Leszczynski et al, 1996). The best agreement
that has been achieved to date is at the 5% level during intercompari-
sons. It has to be hoped that stability with location and with time enables
this level of agreement to be maintained when instruments return to
their home sites.
The easiest comparisons of data from site to site come from assessing
the outputs of instruments of the same type. Most spectroradiometers
take a finite time (minutes) to scan across the UV spectrum, and during
monitoring will usually take a scan at regular designated times or zenith
angles. Broadband meters, by contrast, record the instantaneous EER,
which is usually sampled frequently and integrated over a chosen period
of time to give the total EER dose received, for example, in half-hourly
periods. The two types of data record have different uses and are often
difficult to compare directly unless the conditions of measurement are
very stable (clear skies or uniform, stable overcast). There are also
many ways in which data records can be analysed, depending on the
type of UV instrument used for the monitoring, and the availability of
supporting data from other equipment at the same site, for example,
solarimeters, devices for measuring other solar spectral bands, turbidity
data, ozone, etc.

UV records
There is no coherent, global UV data record from which to assess
whether, and where, there might have been changes in UV radiation
over the past two decades. Instead, data are available from individual
sites and a small number of regional networks, which are unevenly
distributed around the globe (Fig. 2). Many of the sites shown in Fig.
2 did not become operational until after the announcement of the Ant-
arctic ozone hole (Farman, Gardiner & Shanklin, 1985), and monitoring
efforts in place in the decade before this announcement had often ceased
or been scaled down by 1985. Thus there are very few unbroken UV
60 N -

30 N -

30 S -

60 S -

Fig. 2. Global UV monitoring sites (all types of instrument) in November 1995. (Courtesy of Dr E.C. Weatherhead.
Information can be obtained from [email protected])
 Monitoring changes in UV-B radiation 21
records extending from the pre-ozone depletion era to the present day.
This situation automatically precludes any statements about changes in
UV climatology or long-term trends because the data records are simply
not long enough to make such assessments. However, the data records
that are available do provide useful information. It must be realised that
the data is generally site (or region) specific and results cannot be
applied directly to other locations because ozone depletion is not glo-
bally uniform, and neither are the other confounding factors discussed
above. None the less the evidence from different sites can be used to
improve our understanding of UV irradiances at the surface and their
relation to ozone depletion at different locations.
The clearest link between reduced ozone and increased UV-B radi-
ation comes from Antarctica where the springtime appearance of the
ozone hole is so dramatic that the corresponding increases in UV radi-
ation are easily identified. Since 1988 a network of three spectral UV
monitoring instruments have been deployed on the Antarctic continent
by the American National Science Foundation (Booth et aL, 1994). The
UV-B at each of the three sites varies tremendously from year to year
depending on the position of the polar vortex and whether the lowest
ozone values coincide with clear skies and the higher solar elevations
which come as the season progresses. Despite these complications there
is no doubt that lowering ozone by such extreme amounts gives corre-
spondingly huge increases in UV-B. The collection of spectral data
enables the changes in irradiance at UV-B wavelengths to be compared
with changes at UV-A or visible wavelengths (unaffected by ozone)
under the same conditions. If only the UV-B wavelengths change, and
the change increases as wavelength decreases, mirroring the ozone
absorption spectrum, then change in ozone can be identified as the cause
of change in irradiance. If all wavelengths in the UV/visible region
increase or decrease, then cloud, aerosol, the instrument, or a combi-
nation of factors is a more probable explanation for the observations.
This same technique has been used at other locations to show ozone-
related changes in UV-B radiation on a short timescale. The NSF net-
work expanded after 1988, first to Ushuaia in southern Argentina, and
then to Barrow, Alaska and San Diego, California. Southern Argentina
can intermittently come under the influence of the springtime Antarctic
ozone hole as the position of the polar vortex wobbles around the
southern high latitudes, and when under the vortex UV-B radiation
received in Ushuaia can exceed that expected for the latitude by 45%
(Frederick et al., 1993). The year-to-year variability in absolute UV
doses (integrated by month) in Ushuaia is as much a function of the
variability in cloud as changing ozone (WMO, 1995), but if cloud
22 A.R. WEBB

effects are removed then there is an upward trend in UV-B matching

the ozone depletion (WMO, 1995).
Away from the Antarctic region, ozone depletion has been less
severe. In mid-latitudes there has been a general decline in ozone, of
the order of a few per cent per decade, with a seasonality to the change:
it is greatest in winter/spring and least in the summer/autumn.
Extracting evidence of trends in UV-B under these circumstances, with
a short data record and against a background of noise from natural
variability, is impossible. However, short-term UV-B changes can be
clearly associated with periods of low ozone, as, for example, in north-
ern mid-high latitudes during 1992 and 1993. These years represent a
special situation when ozone was lower than previously observed over
this region, and for a prolonged period. Much of this anomaly was due
to a combination of aerosol in the stratosphere following the eruption
of Mount Pinatubo in 1991 (the aerosol acting to increase ozone
destruction), and unusually persistent springtime high pressure regions
over parts of the North American continent and Northern Europe
(tending to give low ozone for dynamic reasons rather than because of
ozone depletion). A four-year record of spectral UV data from Toronto,
Canada showed a significant increase in UV-B radiation in these years
(1989-1993), with the spectral signature associating the change with
ozone (Kerr & McElroy, 1993). The NSF instrument at Barrow, Alaska
provided supporting evidence of this short-term change, reporting elev-
ated springtime UV-B levels in 1993 compared to measurements in the
previous two years (Booth et al, 1993). From 1992 to 1994 low ozone
(as much as 40% depletion) over Finland in the early spring was also
picked up by broadband UV measurements, but it was only in 1993,
when the low ozone extended into April and May, that the increased
absolute irradiances became sufficiently large to appreciably influence
the seasonal and annual doses of UV measured in Finland (Jokela et
al., 1995). Spectral analysis of data from Garmisch-Partenkirchen in
Germany also showed increases at short UV wavelengths during 1993
compared to the preceding year (Seckmeyer et al, 1994). However, in
nearby Innsbruck, broadband measurements of UV dose showed no
increase in the total seasonal doses of UV for 1993 compared to the
average dose for the 1981-1988 period (Blumthaler et al, 1994). This
seeming contradiction is also seen at other locations. For example, in
the UK, spectral measurements made at Reading clearly show that,
when ozone decreases, there is a corresponding increase in UV-B (Fig.
3), yet there is no identifiable change in seasonal or annual UV doses
(EER) measured by a network of broadband instruments spread across
the UK since 1988 (UMIRG, 1996). The explanation is straightforward:
 Monitoring changes in UV-B radiation 23
500 T 500

150 150
3 5 7 9 11 13 15 17 19 21 23 25 27 29 31
Day
Fig. 3. The ratio of erythemally effective UV-B to UV-A radiation
(•) measured at noon at Reading (51.5° N), and the corresponding
ozone (+), for the month of March 1995. Using the ratio of the two
wavebands removes some of the influence of cloud and aerosol
(affects both wavebands) but not the ozone effect (UV-B only).
Inspection of the spectral scans on the 16th and 20th March revealed
that sky conditions had changed significantly during the scan, negat-
ing the analysis, a fact clearly seen in the Figure.

over the UK (and other mid-latitude regions) ozone depletion has not
been severe enough to enable a change in the total UV dose (an average
over all conditions including a large proportion of cloudy days) to be
identified from a short data record which includes great natural varia-
bility. The EER is also less affected by ozone than the shorter UV-B
wavelengths because it includes a UV-A component that does not
respond to changes in ozone. Spectral data, on the other hand, allow
the shortest and most vulnerable UV-B wavelengths to be inspected,
and also enable comparison of different wavelength bands (UV-A and
UV-B) to help remove some of the confusion caused by cloud and other
atmospheric constituents (Fig. 3). If ozone decline is severe enough,
then it can also be picked up by broadband meters on a short timescale:
in the south west of England and Ireland in March 1996, exceptionally
low ozone coincided with clear skies for a few days, giving unpre-
cedented UV doses for the time of year (C. Driscoll, personal
24 A.R. WEBB

communication). Nevertheless this short-lived anomaly is unlikely to

affect the seasonal dose at these locations, and is still lower than sum-
mertime doses.
The existing UV data records which exceed those mentioned above
in duration come from broadband instruments, and one multi-filter
instrument, and many of them have not been maintained to the present
day. The multi-filter instrument located in Maryland, USA, provides
data from 1975 to 1990 (Correll et a/., 1992). From 1980 to 1987, there
is evidence of a substantial increase in UV-B especially for the filter
channels at the shorter wavelengths. After 1987, a decrease in
irradiances was observed following changes to the instrument, although
changes in aerosol, cloud and solar activity are also suggested by the
authors as reasons for the observed decreases.
The much quoted and discussed study of Scotto et al. (1988) reported
broadband measurements from a network of eight radiometers in the
USA for the years 1974-1985. The results showed a downward trend
in EER of 0.5 to 1% per year (depending on the station), and did not
agree with the corresponding figures for a decrease in ozone. There has
since been much investigation and reanalysis of the data from this net-
work, and while the evidence available indicates that the instruments
were stable during the decade in question, there may have been a step
change in the calibration in 1980 which would account for the observed
downward trend (WMO). Other investigations of individual sites in the
network show that, for a subset of the data (clear skies in summer), the
UV-B trend was consistent with the ozone data measured at the same
sites, but the rest of the data were contradictory (Frederick & Weather-
head, 1992). The final interpretation of this US data set is still unclear.
Further analysis of broadband data from Atlanta, Georgia also revives
a previous explanation for the Scotto data, that changes in pollution at
the monitoring sites could be responsible for the downward trend in
UV-B. Justus and Murphy (1994) indicate that changes in aerosol at
some broadband meter sites can mask expected increases in UV-B
because of the response of the instruments to UV-A as well as UV-B.
Elsewhere in the world, long-term broadband UV records are avail-
able from Russia, Switzerland and New Zealand. The Russian data
(Garadzha & Nezval, 1987) comes from city sites and shows the same
sort of downward trend as the US data for a similar time period, and is
open to similar questions. In Switzerland, measurements have been
made at the Jungfraujoch High Altitude Research Station since 1981,
the clean air site avoiding any question of aerosol influences on the data
record. This is also the only broadband data set to be corrected for the
temperature coefficient of the instrument used. The data have not been
 Monitoring changes in UV-B radiation 25
gathered on a continuous basis but for discrete (and changing) periods
each year, giving coverage of every season over the monitoring period.
The UV data, expressed as a ratio of the total solar radiation, showed
an increase of 0.7±0.3% per decade from 1981-1989 (Blumthaler &
Ambach, 1990) calculated for the year as a whole. This trend continued
through 1991, but data for 1992 matched the ratios observed in the early
1980s (WMO, 1995).
Another incomplete broadband UV record is reported form Invercar-
gill, New Zealand by Zheng & Basher (1993). In this case there is a
gap in the record, but extrapolating across the dataless period gives the
expected pattern of UV changes, mirroring the ozone changes at the
same site.
UV records of any duration are sparse in the middle and high lati-
tudes, while in the tropical regions they are non-existent. However,
there has been no statistically significant ozone depletion in the tropics
(WMO, 1995), so no related changes in UV-B would be expected.
Finally, the number of UV monitoring sites has mushroomed tremen-
dously over the past five years, although there is still a significant lack
of sites in tropical regions, Russia, Asia and the Middle East (Fig. 2).
Both broadband and UV spectral monitoring is increasing, as are efforts
to improve the instrumentation and calibration both at and between
individual sites. Some of these efforts are at a national network level,
but regional and international collaborations are also playing a valuable
role in improving UV measurements (Gardiner & Kirsch, 1995; Kos-
kela, 1994; Seckmeyer et aL, 1995). The need to centralise standards
and provide a comprehensive UV database has been recognised by
WMO who have established a Scientific Steering Committee to address
this task, so that in the future there will be more, and more readily
available, UV data.

Sorting out causes and effects

It is clear from the discussion above that, while there is proof that low
ozone means high UV-B, the degree of ozone depletion to date, at all
but high latitudes, is hard to detect in the UV data records available. It
is possible to speculate that a cumulative dose of UV-B over several
years at a mid-latitude site where there has been an average 5% per
decade decline in ozone will be higher than the same cumulative dose
would have been without ozone depletion (regardless of other changes
in the atmosphere). Instantaneous measurements show the ozone-UV
link holds, giving reasonable support to this argument. However, the
variability of the whole atmosphere system prevents any such proof of
26 A.R. WEBB
increasing cumulative dose being obvious in the UV records, and from
the biological standpoint this is the important factor: a UV effect will
only be observed if UV exposure changes, regardless of the cause.
Trying to separate the causes of UV attenuation in the atmosphere helps
to explain the UV observations made to date, and how UV exposures
might have changed subtly, if not in a total dose manner. It also pro-
vides for better predictive models in the future, models being the only
way to estimate what might be happening in the large areas where there
are no data.
Individual causes can be investigated at a single site where the other
variables of interest are also measured, and with sufficient data different
effects may be separated from each other. For example, Bais et al.
(1993) showed that high concentrations of SO2 can significantly influ-
ence UV irradiances. An alternative method of studying different fac-
tors affecting UV irradiances at the surface, and/or the associated
changes in real dose, is to make measurements with matched instru-
ments at different sites at the same or equivalent times, knowing specific
differences between the sites. An example of simultaneous measure-
ments is given by Blumthaler et al. (1994) who used two pairs of spec-
troradiometers to measure UV at sites in the German Alps separated by
1 km vertically but only 5 km horizontally. In cloud-free conditions the
difference in UV irradiances between the sites was then due only to the
aerosol and ozone in the 1 km depth of atmosphere, and this was suf-
ficient to produce a change in UV of 24% at 300 nm, 11% at 320 nm
and 9% at 370 nm (unaffected by ozone). For EER calculated from the
spectral measurements, the 1 km change in altitude produced a 14%
change in UV. These altitude effects were independent of zenith angle
(in the 30-70° range) and were in agreement with the range of model
values calculated using the measured 4 DU (Dobson units) ozone in the
1 km layer, and aerosol profiles which were reasonable estimates for
the region. The total altitude effect was made up of a combination of
Rayleigh scattering (known), ozone (known) and aerosol (unknown)
attenuation throughout the 1 km depth. The influence of the aerosol
could then be assessed from the residual of the total minus the known
(calculated) effects. For a typical continental aerosol the aerosol attenu-
ation was constant for UV-B wavelengths at 1.8% per km, reducing
slightly to 1.5% at 360 nm. For an urban-type aerosol there was rather
more dependency on wavelength, from 4.1% to 3.4%. The actual aero-
sol was probably somewhere between the two types.
Equivalent time measurements are reported by Seckmeyer et al.
(1995) from 12 stations in the Northern and Southern Hemispheres
using spectral (and a few broadband) measurements related through
 Monitoring changes in UV-B radiation 27
calibration to four instruments which had been successfully inter-
compared in Garmisch-Partenkirchen in summer 1993. Six of the sites
were the NSF sites, four were in Australia and run by the Australian
Radiation Laboratory, one was at Lauder in New Zealand, and one at
Garmisch-Partenkirchen in Germany. The three Northern Hemisphere
sites covered latitudes from 32 to 71° N, and the nine Southern Hemi-
sphere sites ranged from 12 to 90° S. The mean daily erythemal dose for
each of the four summer months (May - August, NH, and November -
February, SH) was calculated for each site and then compared as a
function of latitude and hemisphere. The geographical differences in
UV doses were larger than the uncertainties in the measurements and
showed that there was a distinct difference between the two
hemispheres. In mid-latitudes this study reinforces the observations of
Seckmeyer & McKenzie (1992) who compared data from Lauder and
Germany and showed that for clear skies the differences were bigger
than expected from the effects of different sun-earth distances and dif-
ferent ozone amounts. In the early study, the heavier aerosol loading in
the Northern Hemisphere was cited to explain the extra hemispheric
effect. This effect is now shown to hold in cloudy as well as clear
conditions, and at other latitudes. In the Northern Hemisphere the
expected decline in UV dose with latitude is observed, but in the Sou-
thern Hemisphere the latitudinal gradients are much weaker, especially
in the spring, reflecting the influence of the more dramatic ozone
depletions at this time in the Southern Hemisphere. In the summer
months the daily doses at high southern latitudes exceed those at mid-
northern latitudes due to the combined effects of low ozone, daylight
for 24 hours, high albedo, low cloud and aerosol extinction, and at the
south pole high altitude. In the winter months when the poles are in
darkness, latitudinal gradients must become more pronounced, thus
annual integrated doses will also show more latitudinal dependence than
just the summer doses.
The latter study illustrates the importance of knowing what sort of
change in UV irradiances is important for a given biological effect. Is
it the annual dose, a particular seasonal dose, or a threshold maximum
dose that may be reached for a given period of time? It is also important
not to extrapolate results of either absolute irradiances, or change, from
one site to another.

Is there a change at the plant level?

This question cannot be addressed until it is stated in more exact terms,
and even then the answer is often not clear-cut. First, the location where
28 A.R. WEBB
a change is sought must be specified, and then the type of change:
annual, seasonal, dose or threshold.
In the tropics there has been no significant change in stratospheric
ozone, therefore one would not expect any change in UV-B radiation,
although there are no measurements to prove this. In Antarctica and
neighbouring regions, which may periodically come under the influence
of the ozone hole, there are instances of extreme UV-B irradiances when
there is severely depleted ozone overhead. These are highly elevated
threshold doses, and if time beneath the ozone hole is prolonged, and/or
thick cloud is not present, they contribute to elevated seasonal doses and
even annual doses. Similar but less dramatic increases in short-lived
threshold doses and seasonal doses are observed at southern mid-latitudes
as well. In the Northern Hemisphere the evidence is less clear. There have
certainly been instances of high UV doses on a short-term basis, days or
a single season, but these are not always apparent in all types of data
record and the short-lived changes are not sufficient to influence longer-
term doses. The year 1993 produced several reports of unusually high UV
irradiances in mid-high northern latitudes, extending through into the
early summer, but this pattern has not been repeated since and must be
considered an anomaly rather than an impending trend. In general, the
complications of cloud and aerosol, the less dramatic ozone changes, and
the insufficient data records allow only the speculative comments made
at the beginning of the previous section.

References
Bais, A.F., Zerefos, C.S., Meleti, C , Ziomass, I.C., & Tourpali, K.
(1993). Spectral measurements of solar UV-B radiation and its
relations to total ozone, SO2 and clouds. Journal of Geophysical
Research, 98, D3, 5199-204.
Blumthaler, M. & Ambach, W. (1990). Indication of increasing ultra-
violet-B radiation in alpine regions. Science, 248, 206-8.
Blumthaler, M., Webb, A.R., Seckmeyer, G., Bais, A.F., Huber, M. &
Mayer, B. (1994). Simultaneous spectroradiometry: a study of solar
UV irradiance at two altitudes. Geophysical Research Letters, 21,
2805-8.
Booth, C.R., Lucas, T., Morrow, J., Weiler, S. & Penhale, P. (1994).
The United States National Science Foundation/Antarctic Pro-
gram's Network for Monitoring Ultraviolet Radiation. In Ultra-
violet Radiation and Biological Research in Antarctica, AGU Ant-
arctic Research Series. (Weiler, S. & Penhale, P., eds). AGU,
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Other documents randomly have
different content
shell-fish are received into the stomach. In another place
he says there is mutual hostility between the pelican and
the quail. The pelican was known to the Romans under
the name of onocrotalus. Pliny says this bird is like the
swan, except that under the throat there is a sort of
second crop of astonishing capacity. There is, of course,
no doubt that the pelican is here intended. Cicero says
there is a bird called platalea which pursues other birds
and causes them to drop the fish they have caught, which
it devours itself. He then gives the same story as Ælian,
viz., that this bird softens shell-fish in its stomach, &c. The
first part of this account is true of the parasitic gulls
(Lestris). It is uncertain what bird Cicero alludes to by the
name platalea. Pliny gives the same story as Cicero, and
calls the bird platea. The fable, then, is no classical one.
Whence did it originate? Does any pictorial representation
occur on the Egyptian monuments, as Mr. Bartlett has
been informed? I am inclined to think—but I speak under
correction—that such a representation does not occur.
Horapollo (i. 54) tells us that when the ancient Egyptians
want to represent a fool they depict the pelican, because
this bird, instead of laying its eggs on lofty and secure
292
places, merely scratches up the ground and there lays.
The people surround the place with dried cow’s dung, and
set fire to it. The pelican sees the smoke, and endeavours
to extinguish the fire with her wings, the motion of which
only fans the flame. Thus she burns her wings, and falls
an easy prey to the fowlers. Some Egyptian priests,
considering this behaviour evinces great love of its young,
do not eat the bird; others, again, thinking it is a mark of
folly, eat it. The Egyptians, however, did believe in a bird
feeding its young with its blood, and this bird is none
other than a vulture. Horapollo says (i. 11) that a vulture
symbolises a compassionate person (ἐλεήμονα), because
during the 120 days of its nurture of its offspring, if food
cannot be had, ‘it opens its own thigh and permits the
young to partake of the blood, so that they may not perish
from want.’ This is alluded to in the following lines by
Georgius Pisidas:—

Τὸν μηρὸν ἐκτέμοντες, ἡματωμένοις

Γάλακτος ὀλκοῖς ζωπυροῦσι τὰ βρέφη.

Amongst classical authors, the love of the vulture for its

young was proverbial. But when do we first hear of the
fable of the pelican feeding its young with its blood? In
Patristic annotations on the Scriptures. I believe this is the
answer. The ecclesiastical fathers transferred the Egyptian
story from the vulture to the pelican, but magnified the
already sufficiently marvellous fable a hundredfold, for the
293
blood of the parent was not only supposed to serve as
food for the young, but was also able to reanimate the
dead offspring! Augustine, commenting on Psalm cii. 5—‘I
am like a pelican in the wilderness’—says: ‘These birds
[male pelicans] are said to kill their young offspring by
blows of their beaks, and then to bewail their death for
the space of three days. At length, however, it is said the
mother bird inflicts a severe wound on herself, pouring the
flowing blood over the dead young ones, which instantly
brings them to life.’ To the same effect write Eustathius,
Isidorus, Epiphanius, and a host of other writers, except
that sometimes it was the female who killed the young
ones, while the male reanimated them with its blood. This
fable was supposed to be a symbol of Christ’s love to
men. I think, then, that the very interesting fact of the
flamingo feeding the cariama with the red fluid and other
contents of its stomach can hardly be, as Mr. Bartlett
conjectures, the origin of the old fable of the pelican
feeding its young with its blood, because the Egyptian
story of the vulture wounding its thigh has nothing
analogous to the natural-history fact of the flamingo, while
the fable of the pelican pouring from its self-inflicted
wound the life-restoring blood which reanimates its
offspring is still further from the mark.”

In a short criticism upon the subject in the same number

of Land and Water, Mr. H. J. Hancock is inclined to believe
294 some confusion has arisen in the translation from the
that
original Hebrew. “The word ‫( ָקַאת‬Kàh-ath'), which is
rendered πελεκάν in the Septuagint, and Pelican, or
Onocrotalus, in the Vulgate, is derived from the verb ‫ָקא‬
‘to vomit,’ and signifies ‘a vomiter.’ This name, evidently a
general one, may have been intended by the Hebrew
writers to apply either to such birds as, like the pelican
and many others, possess the power of disgorging their
food on being disturbed or alarmed, or to such birds as
are accustomed to nourish their young from their own
crops; and, in the latter case, the curious bloody secretion
of the flamingo may well have given rise to the
superstition concerning the pelican. I may observe, as an
evidence that the translators did not consider the Hebrew
word to be other than a general name, that Kà-ath' is
sometimes rendered ‘cormorant’ (Isa. xxxiv. 11; Zeph. ii.
14). For further information concerning this point, I would
refer your readers to the ‘Hebrew and Chaldee
Concordance,’ p. 1083; Bate’s ‘Hebrew Dictionary,’ p. 538;
and Parkhurst’s ‘Hebrew Dictionary,’ pp. 631, 632.”
Shakespeare, doubtless, had not investigated the subject
so narrowly, but was content to accept the common story
as he found it, and to apply it metaphorically as occasion
required.
IN THE ENGLISH FENS.

The majority of the birds mentioned in this chapter are

not natives of the British Islands, but, strange as it may
295
appear, there is evidence to show that the pelican, or, to
speak more correctly, a species of pelican, once inhabited
the English fens.

The peat-bogs of Cambridgeshire have yielded of late

years a large number of bones of birds, and amongst
these has been discovered the wing-bone of a pelican.
This interesting discovery was made known by M.
Alphonse Milne-Edwards, in an able article in the “Annales
des Sciences Naturelles,” [169] a translation of which
subsequently appeared in The Ibis. [170] The author thus
anticipates the objections of the sceptical:—

“We may be inclined, perhaps, to wonder that a

single bone, belonging (as it does) to a young animal,
and consequently not presenting all its anatomical
characters, should permit the exact recognition of the
genus and species of bird to which it belongs. So
precise a determination would not be always possible,
but in the present case there need be no doubt; for I
have shown, in another work, [171] that the wing-
bone in the genus Pelicanus offers extremely clear
distinctive peculiarities, which do not allow of its
being confounded with that of any other bird.”

THE PELICAN IN ENGLAND.

The only species of pelican which has been recorded to
have occurred in England in recent times, is the great
white pelican, P. onocrotalus.
296
Latham has stated, [172] on the authority of Sir Thomas
Brown, that a pelican of this species was killed in Horsey
Fen in 1663. This statement was copied by Montagu, [173]
and subsequently by Dr. Fleming, [174] but there is no
evidence to show that the bird was a wild one. On the
contrary, it is probable, as suggested by Sir Thomas
Brown, that it may have been one of the King’s pelicans
which was lost about that time from St. James’s Park.

He says [175] :—“An onocrotalus, or pelican, shot upon

Horsey Fen, May 22, 1663, which, stuffed and cleaned, I
yet retain. It was three yards and a half between the
extremities of the wings; the chowle and beak answering
the usual description; the extremities of the wings for a
span deep brown; the rest of the body white; a fowl which
none could remember upon this coast.

“About the same time, I heard one of the king’s pelicans

was lost at St. James’s; perhaps this might be the same.”

Latham was further assured by Dr. Leith, that in the

month of May he saw a brown pelican fly over his head on
Blackheath, in Kent. Montagu, however, suggests that the
bird was an immature swan.

In The Zoologist for 1856 (p. 5321), the Rev. H. B.

297
Tristram has recorded, that on the 25th of August, 1856,
the remains of a pelican were picked up on the shore at
Castle Eden, Durham. Such are the scanty records of the
appearance of a pelican in England in modern times.
The bone found in Cambridgeshire may have belonged to
P. onocrotalus, a native of South and South-Eastern
Europe, and which is stated to be “common on the lakes
and watercourses of Hungary and Russia, and also seen
further south in Asia and in Northern Africa.” M. Milne-
Edwards, however, has not quite determined the species,
for, on comparison with the bones of other recognized and
existing species, it appears to differ rather remarkably in
its greater length.

Enough has probably been said, however, to show the

interest which attaches to the discovery, and to suggest
further research.

With the pelican ends the long list of birds mentioned in

the works of Shakespeare.
CONCLUSION.

The reader who has had the patience or the curiosity to

follow us thus far will, doubtless, ere this have formed a
just estimate of Shakespeare’s qualifications as a
naturalist, and will have drawn the only conclusion which
the evidence justifies.

It is impossible to read all that Shakespeare has written in

connection with ornithology, without being struck with the
extraordinary knowledge which he has displayed for the
298 in which he lived; and our admiration for him as a
age
poet must be increased tenfold on perceiving that the
beauteous thoughts, which he has clothed in such
beauteous language, were dictated by a pure love of
nature, and by a study of those great truths which appeal
at once to the heart and to reason, and which infuse into
the soul of the naturalist the true spirit of poetry.
299

APPENDIX.
A TABLE OF
ORNITHOLOGICAL ALLUSIONS
IN THE ORDER IN WHICH THEY OCCUR:
THE PLAYS AND POEMS BEING ALPHABETICALLY ARRANGED.

All’s Well that Ends Well: PAGE

Act I. Sc. 1 [Hawking-eye] 55
Act I. Sc. 3 Cuckoo 154
Act II. Sc. 5 Lark 136
Act II. Sc. 5 Bunting 136
Act III. Sc. 5 Limed 160
Act IV. Sc. 1 Chough 117
Act IV. Sc. 1 Woodcock 231
Act IV. Sc. 3 Crow 110

Antony and Cleopatra:

Act II. Sc. 2 Eagle 26
Act II. Sc. 3 Cocks 172, 219
Act II. Sc. 3 Quails 219
Act II. Sc. 6 Cuckoo 154
Act III. Sc. 2 [Swan] 201
300 Act III. Sc. 2 [Kite] 44
Act III. Sc. 10 Mallard 238
Act III. Sc. 13 Kite 44
Act III. Sc. 13 Seel 70
Act III. Sc. 13 Dove 195
Act III. Sc. 13 Ostrich 195
Act IV. Sc. 8 [Nightingale] 123
Act IV. Sc. 12 [Swallow] 276
Act V. Sc. 2 Seel 70

As You Like It:

Act I. Sc. 2 Pigeons 180, 185
Act I. Sc. 3 Juno’s Swans 206
Act II. Sc. 3 Ravens 106
Act II. Sc. 3 Sparrow 106, 146
Act II. Sc. 5 Eggs 32
Act II. Sc. 7 [Goose] 197
Act II. Sc. 7 [Cock] 168
Act III. Sc. 3 Falcon 61
Act III. Sc. 3 Bells 61
Act III. Sc. 3 Pigeon 180, 185
Act III. Sc. 4 Goose 197
Act IV. Sc. 1 [Pigeon] 180
Act IV. Sc. 1 Parrot 272
Act IV. Sc. 3 Moss’d 34
Act V. Sc. 4 Stalking-horse 238

Comedy of Errors:
Act II. Sc. 1 [Stale] 245
Act II. Sc. 2 Owls 96
Act III. Sc. 1 Crow 114
Act IV. Sc. 2 Lapwing 221

Coriolanus:
Act I. Sc. 1 Cormorant 260
Act I. Sc. 1 Goose 197
Act I. Sc. 4 Geese 197
 Act III. Sc. 1 [Crow] 110
Act III. Sc. 1 [Eagle] 23
Act III. Sc. 1 Cry havoc (note) 57
Act III. Sc. 1 Quarry 57
301 Act III. Sc. 5 [Kite] 43
Act III. Sc. 5 [Crow] 110
Act IV. Sc. 5 Daw 119
Act IV. Sc. 7 Osprey 42
Act V. Sc. 3 [Dove] 180, 191
Act V. Sc. 3 [Gosling] 197
Act V. Sc. 6 [Eagle] 23
Act V. Sc. 6 [Dovecote] 180

Cymbeline:
Act I. Sc. 2 Eagle 28, 45
Act I. Sc. 2 Puttock 28, 45
Act I. Sc. 3 [Crow] 110
Act I. Sc. 4 Fowl 235
Act II. Sc. 2 Philomel 125
Act II. Sc. 2 [Raven] 99
Act II. Sc. 3 Lark 132
Act II. Sc. 4 [Watching] 45
Act III. Sc. 1 Crows 112
Act III. Sc. 3 Crows 112
Act III. Sc. 3 Eagle 27
Act III. Sc. 4 Jay 121
Act III. Sc. 4 Swan’s nest 206
Act III. Sc. 6 Owl 83
Act III. Sc. 6 Lark 136
Act IV. Sc. 2 Ruddock 141
Act IV. Sc. 2 Wren 144
Act IV. Sc. 2 The Roman Eagle 28
Act V. Sc. 3 Crows 111
 Act V. Sc. 4 Eagle 30
Act V. Sc. 4 Prune 31
Act V. Sc. 4 Cloys 31
Act V. Sc. 5 The Roman Eagle 29

Hamlet:
Act I. Sc. 1 Cock 167
Act I. Sc. 3 Woodcocks 229
Act I. Sc. 5 The falconer’s call 55
Act II. Sc. 2 Aiery 39, 58
Act II. Sc. 2 Kites 43
Act II. Sc. 2 Hawk 75, 223
302 Act II. Sc. 2 Hernshaw 75, 223
Act II. Sc. 2 Pigeon-liver’d 185
Act II. Sc. 2 Kites 43
Act II. Sc. 2 French falconers 56
Act II. Sc. 2 Eyases 58
Act III. Sc. 2 [Raven] 99
Act III. Sc. 2 Recorder (note) 129
Act IV. Sc. 5 Owl 88
Act IV. Sc. 5 Pelican 286
Act IV. Sc. 5 [Dove] 180
Act IV. Sc. 7 Check 60
Act V. Sc. 1 Dove 180
Act V. Sc. 2 [Chough] 115
Act V. Sc. 2 Lapwing 222
Act V. Sc. 2 Bevy 218
Act V. Sc. 2 Sparrow 146
Act V. Sc. 2 [Woodcock] 229
Act V. Sc. 2 Quarry 56

Henry IV.—Part I.:

Act I. Sc. 3 Popinjay 273
 Act I. Sc. 3 Starling 274
Act II. Sc. 1 Turkies 177
Act II. Sc. 2 Chuffs 118
Act II. Sc. 2 Wild-Duck 237
Act II. Sc. 4 [Wild-Geese] 246
Act II. Sc. 4 Sparrow 147
Act II. Sc. 4 [Cuckoo] 147
Act III. Sc. 1 [Raven] 99
Act III. Sc. 1 [Goose] 197
Act III. Sc. 1 Redbreast-teacher 142
Act III. Sc. 2 Cuckoo 155
Act IV. Sc. 1 Estridge 286
Act IV. Sc. 1 Bated 286
Act IV. Sc. 1 Eagles 36, 286
Act IV. Sc. 1 Dove 180
Act IV. Sc. 2 Caliver 240
Act IV. Sc. 2 Wild-Duck 240
Act IV. Sc. 2 Scare-crows 115
Act V. Sc. 1 Gull 148
303 Act V. Sc. 1 Cuckoo’s bird 148
Act V. Sc. 1 Sparrow 148
Act V. Sc. 1 [Vultures] 41

Henry IV.—Part II.:

Act III. Sc. 1 Seel 70
Act III. Sc. 2 Ouzel 139
Act III. Sc. 2 Dove 196
Act V. Sc. 1 Cock and pye 172
Act V. Sc. 1 Pigeons 180, 196
Act V. Sc. 1 Hens 196
Act V. Sc. 1 Wild-Geese 246
Act V. Sc. 4 Vultures 41
 Henry V.:
Act I. Sc. 2 Eagle 32
Act I. Sc. 2 Eggs 32
Act II. Sc. 1 Kite 43
Act II. Sc. 1 Crow 111
Act II. Sc. 2 Cloy 31
Act III. Sc. 6 Gull 149, 266
Act III. Sc. 7 Hawk 73
Act III. Sc. 7 Lark 133
Act III. Sc. 7 Hooded 62
Act III. Sc. 7 Bate 62
Act IV. Prologue Cocks 168
Act IV. Sc. 1 Mounted 63
Act IV. Sc. 1 Stoop 63
Act IV. Sc. 2 Carrions 104
Act IV. Sc. 2 Crows 104

Henry VI.—Part I.:

Act I. Sc. 2 Halcyon days 275
Act I. Sc. 2 Mahomed’s Dove 194
Act I. Sc. 2 [Eagle] 23
Act I. Sc. 4 Scare-crow 115
Act I. Sc. 5 Doves 180
Act II. Sc. 2 Turtle-doves 180, 191
Act II. Sc. 4 Hawks 73
Act II. Sc. 4 Pitch 73
304 Act II. Sc. 4 Daw 119
Act III. Sc. 3 Peacock 175
Act IV. Sc. 2 [Owl] 83
Act IV. Sc. 3 [Vulture] 40
Act V. Sc. 3 Swan 204
Act V. Sc. 3 Cygnets 204
Henry VI.—Part II.:
Act I. Sc. 2 [Hawk] 72
Act I. Sc. 3 Limed 161
Act I. Sc. 4 Screech-Owls 85, 97
Act II. Sc. 1 Flying at the brook 50, 51
Act II. Sc. 1 Old Joan 50
Act II. Sc. 1 Point 50, 51
Act II. Sc. 1 Falcon 50
Act II. Sc. 1 Pitch 50, 51
Act II. Sc. 1 Hawks 50
Act II. Sc. 1 Tower 50, 51
Act II. Sc. 1 Fowl 51
Act II. Sc. 4 Limed 161
Act III. Sc. 1 Dove 180
Act III. Sc. 1 [Raven] 101
Act III. Sc. 1 [Eagle] 23
Act III. Sc. 1 Kite 44
Act III. Sc. 2 Raven 101
Act III. Sc. 2 Wren 101, 144
Act III. Sc. 2 Partridge 44, 216
Act III. Sc. 2 Puttock 44, 216
Act III. Sc. 2 [Kites] 43
Act III. Sc. 2 [Screech-Owl] 85
Act III. Sc. 3 [Lime-twigs] 160
Act IV. Sc. 1 [Eagle] 23
Act IV. Sc. 10 Ostrich 285
Act IV. Sc. 10 Crows 113
Act V. Sc. 2 Kites 43, 112
Act V. Sc. 2 Crows 112

Henry VI.—Part III.:

Act I. Sc. 1 Eagle 38
 Act I. Sc. 1 Tire 38
Act I. Sc. 1 Hawk’s bells 61
305 Act I. Sc. 4 Swan 205
Act I. Sc. 4 Dove 54, 195
Act I. Sc. 4 Falcon 54
Act I. Sc. 4 Woodcock 232
Act II. Sc. 1 Eagle’s bird 25
Act II. Sc. 1 Night-Owl 88, 94
Act II. Sc. 2 Doves 91, 195
Act II. Sc. 6 [Screech-Owl] 85
Act V. Sc. 2 The princely Eagle 33
Act V. Sc. 4 Owl 85
Act V. Sc. 6 Limed 160
Act V. Sc. 6 Owl 86
Act V. Sc. 6 [Raven] 102
Act V. Sc. 6 Night-Crow 102
Act V. Sc. 6 Pies 121

Henry VIII.:
Act II. Sc. 3 [Lark] 136
Act III. Sc. 2 Larks 136
Act IV. Sc. 1 The bird of peace 180

Julius Cæsar:
Act I. Sc. 3 Bird of night 89
Act V. Sc. 1 Eagles 27
Act V. Sc. 1 Raven 99–110
Act V. Sc. 1 Crows 112
Act V. Sc. 1 Kites 43
Act V. Sc. 3 [Eagles] 27
Act V. Sc. 3 [Kites] 43
Act V. Sc. 3 Ravens 104

King John:
 Act I. Sc. 1 Sparrow 145
Act II. Sc. 2 Cry havoc (note) 57
Act IV. Sc. 3 Raven 103
Act V. Sc. 1 [Crow] 110
Act V. Sc. 2 Eagle 38
Act V. Sc. 2 Aiery 38
Act V. Sc. 2 Towers 38
Act V. Sc. 2 Souse 38
Act V. Sc. 7 Cygnet 201
306 Act V. Sc. 7 Swan 201

King Lear:
Act I. Sc. 4 Hedge-Sparrow 147
Act I. Sc. 4 Cuckoo 147
Act I. Sc. 4 Kite 44
Act II. Sc. 2 Wagtail 156
Act II. Sc. 2 Goose 198
Act II. Sc. 2 Halcyon 275
Act II. Sc. 4 Wild-Geese 246
Act II. Sc. 4 Vulture 41
Act II. Sc. 4 Owl 97
Act III. Sc. 4 The five wits 95
Act III. Sc. 4 Pelican 287
Act III. Sc. 6 [Nightingale] 123
Act IV. Sc. 6 Crows 116
Act IV. Sc. 6 Choughs 116
Act IV. Sc. 6 Crow-keeper 114
Act IV. Sc. 6 Wren 144
Act IV. Sc. 6 Lark 135

Loves Labour’s Lost:

Act I. Sc. 1 Cormorant 260
Act I. Sc. 1 Green-Geese 197
 Act III. Sc. 1 Goose 197
Act IV. Sc. 1 Owl 95
Act IV. Sc. 3 Green-Goose 198
Act IV. Sc. 3 Woodcocks 229
Act IV. Sc. 3 Raven 109
Act IV. Sc. 3 [Turtle] 191
Act IV. Sc. 3 Eagle-sighted 25
Act IV. Sc. 3 Bird-bolts 162
Act V. Sc. 1 Pigeon 180
Act V. Sc. 2 Pigeons 180
Act V. Sc. 2 Owl 95
Act V. Sc. 2 [Cuckoo] 147
Act V. Sc. 2 [Lark] 130
Act V. Sc. 2 [Turtle-dove] 191
Act V. Sc. 2 Rook 121
Act V. Sc. 2 Daw 119

Macbeth:
Act I. Sc. 2 Sparrow 147
Act I. Sc. 2 [Eagle] 23
307 Act I. Sc. 5 Raven 102
Act I. Sc. 6 Martlet 277
Act II. Sc. 1 Owl 84
Act II. Sc. 2 “Obscure bird” 85
Act II. Sc. 4 Falcon 39, 51
Act II. Sc. 4 Towering 39, 51
Act II. Sc. 4 Owl 51
Act III. Sc. 2 [Crow] 110–115
Act III. Sc. 4 Maws 46
Act III. Sc. 4 Kites 46
Act III. Sc. 4 Magot-pie 120
Act III. Sc. 4 Choughs 120
Act III. Sc. 4 Rooks 120
 Act IV. Sc. 1 Owlet 84
Act IV. Sc. 2 Wren 91, 143
Act IV. Sc. 2 Owl 91, 143
Act IV. Sc. 3 Vulture 40
Act IV. Sc. 3 [Quarry] 57
Act IV. Sc. 3 [Kite] 43
Act V. Sc. 3 Loon 258
Act V. Sc. 3 [Geese] 197

Measure for Measure:

Act I. Sc. 4 Lapwing 221
Act II. Sc. 1 Scare-crow 115
Act III. Sc. 1 Enmew 64–66
Act III. Sc. 1 Falcon 64
Act III. Sc. 1 Fowl 64
Act III. Sc. 2 Sparrows 146

Merchant of Venice:
Act I. Sc. 2 Throstle 137
Act II. Sc. 2 Doves 196
Act II. Sc. 6 Venus’ Pigeons 190
Act II. Sc. 9 Martlet 278
Act III. Sc. 2 Swan 201
Act V. Sc. 1 Crow 143
Act V. Sc. 1 Lark 135, 143
Act V. Sc. 1 Nightingale 128, 143
Act V. Sc. 1 Goose 128, 143, 197
Act V. Sc. 1 Wren 128, 143
308 Act V. Sc. 1 Cuckoo 150

Merry Wives of Windsor:

Act I. Sc. 1 Cock and pye 171
Act I. Sc. 3 Bully-rook 121
Act I. Sc. 3 [Raven] 99
Act I. Sc. 3 Vultures 41
Act I. Sc. 3 [Dove] 190
Act II. Sc. 1 Cuckoo-birds (note) 148
Act III. Sc. 3 Eyas-musket 74
Act III. Sc. 3 Birding 72
Act III. Sc. 3 [Hawk] 73
Act III. Sc. 4 [Geese] 197
Act III. Sc. 5 Birding 72
Act IV. Sc. 2 Birding 72
Act IV. Sc. 2 Birding-pieces 72, 164
Act V. Sc. 1 Goose 197
Act V. Sc. 5 Swan 207
Act V. Sc. 5 Goose 207

Midsummer Night’s Dream:

Act I. Sc. 1 Doves of Venus 190
Act I. Sc. 1 Lark 133
Act I. Sc. 2 Dove 195
Act I. Sc. 2 Nightingale 195
Act II. Sc. 1 Crows 110
Act II. Sc. 1 [Dove] 180
Act II. Sc. 1 [Bolt] 162
Act II. Sc. 2 Owl 89
Act II. Sc. 2 Philomel 125
Act II. Sc. 2 Raven 108
Act II. Sc. 2 Dove 108
Act III. Sc. 1 [Wild-fowl] 235
Act III. Sc. 1 Ousel-cock 139
Act III. Sc. 1 Throstle 137
Act III. Sc. 1 Wren 142
Act III. Sc. 1 Finch 144
Act III. Sc. 1 Sparrow 147
Act III. Sc. 1 [Lark] 130
 Act III. Sc. 1 Cuckoo 150
Act III. Sc. 2 Wild-Geese 246
Act III. Sc. 2 Fowler 246
Act III. Sc. 2 Choughs 119
309 Act III. Sc. 2 [Crow] 110
Act IV. Sc. 1 Lark 131
Act V. Sc. 1 Recorder 129
Act V. Sc. 1 Goose 197
Act V. Sc. 2 Screech-Owl 86

Much Ado about Nothing:

Act I. Sc. 1 Parrot-teacher 272, 273
Act I. Sc. 1 Bird-bolt 162
Act I. Sc. 1 Crow 114
Act I. Sc. 1 Wise and warm 95
Act II. Sc. 1 Partridge 218
Act II. Sc. 1 Fowl 237
Act II. Sc. 3 Raven 101
Act II. Sc. 3 Fowl 238
Act II. Sc. 3 Daw 119
Act II. Sc. 3 Gull 269
Act III. Sc. 1 Lapwing 221
Act III. Sc. 1 Haggards 59
Act III. Sc. 1 Limed 160
Act III. Sc. 4 [Hawk] 73
Act V. Sc. 1 Woodcock 229

Othello:
Act I. Sc. 1 Daws 120
Act I. Sc. 3 Seel 70
Act I. Sc. 3 Snipe 233
Act II. Sc. 1 Birdlime 161
Act II. Sc. 3 Speak Parrot 272
 Act III. Sc. 3 Watch 45
Act III. Sc. 3 Haggard 57
Act III. Sc. 3 Jesses 57
Act III. Sc. 3 Seel 71
Act IV. Sc. 1 Raven 100
Act V. Sc. 1 “Cry on” (note) 56
Act V. Sc. 2 [Gull] 239, 267
Act V. Sc. 2 Swan 201

Pericles:
Act III. Introd. [Duck] 222–224, 237
Act IV. Introd. [Night-bird] 99
Act IV. Introd. Dove 113, 191
310 Act IV. Introd. Crow 113
Act IV. Sc. 3 Wren 144
Act IV. Sc. 3 [Eagle] 23
Act IV. Sc. 6 Coistrel 74

Richard II.:
Act I. Sc. 1 Pitch 51
Act I. Sc. 3 Falcon 54
Act I. Sc. 3 Cloy 31
Act II. Sc. 1 Cormorant 259
Act II. Sc. 1 Pelican 287
Act II. Sc. 1 Imp 69
Act III. Sc. 3 Eagle 24
Act III. Sc. 3 Night-Owls 85
Act III. Sc. 3 Lark 136

Richard III.:
Act I. Sc. 1 [Eagle] 23, 45
Act I. Sc. 1 Kites 45
Act I. Sc. 1 Buzzards 45, 47
Act I. Sc. 3 Wren 144
 Act I. Sc. 3 [Eagle] 23
Act I. Sc. 3 [Mew’d up] 64
Act I. Sc. 3 Aiery 39
Act IV. Sc. 4 Owls 86
Act V. Sc. 2 Swallow 277
Act V. Sc. 3 Lark 133
Act V. Sc. 3 Cock 167
Act V. Sc. 3 “Cry on” (note) 56

Romeo and Juliet:

Act I. Sc. 2 Swan 114, 206
Act I. Sc. 2 Crow 114, 206
Act I. Sc. 3 Dove-house 180
Act I. Sc. 4 Crow-keeper 114
Act I. Sc. 4 Soar 50, 51
Act I. Sc. 4 Pitch 50, 51
Act I. Sc. 5 Cock-a-hoop 169
Act I. Sc. 5 Dove 113, 194
311 Act I. Sc. 5 Crows 113, 194
Act II. Sc. 2 Falconer 54
Act II. Sc. 2 Lure 54
Act II. Sc. 2 Tassel-gentle 54
Act II. Sc. 4 Goose 197
Act II. Sc. 5 Dove 180
Act III. Sc. 2 Hood 62
Act III. Sc. 2 Unmann’d 62
Act III. Sc. 2 Bating 62
Act III. Sc. 2 Raven 108, 109
Act III. Sc. 4 Mew’d up 64
Act III. Sc. 5 Nightingale 124
Act III. Sc. 5 Lark 124, 131, 134
Act III. Sc. 5 Eagle 25
Act IV. Sc. 4 Watch 46
 Act IV. Sc. 4 Watching 46
Act V. Sc. 1 [Dove] 194
Act V. Sc. 3 Maw 46

Taming of the Shrew:

Induct. Sc. 1 [Nightingale] 123
Induct. Sc. 2 Hawking 72
Induct. Sc. 2 Hawk 72
Induct. Sc. 2 Lark 72
Induct. Sc. 1 Mew 64, 65
Act I. Sc. 2 Woodcock 229
Act II. Sc. 1 Nightingale 124
Act II. Sc. 1 Buzzard 47
Act II. Sc. 1 Turtle 47
Act II. Sc. 1 Wise and warm 95
Act III. Sc. 1 Stale 245
Act III. Sc. 2 Dove 180
Act IV. Sc. 1 Falcon 62
Act IV. Sc. 1 Stoop 62
Act IV. Sc. 1 Lure 55, 62
Act IV. Sc. 1 Man 45, 62
Act IV. Sc. 1 Haggard 45, 62
Act IV. Sc. 1 Watch 45, 62
Act IV. Sc. 1 Kites 45, 62
Act IV. Sc. 1 Bate 45, 63
Act IV. Sc. 1 Peacock (note) 175
312 Act IV. Sc. 2 Haggard 59
Act IV. Sc. 3 Jay 122
Act IV. Sc. 3 Lark 122
Act V. Sc. 2 Hawk 73

The Tempest:
Act I. Sc. 2 Raven’s feather 107
Act II. Sc. 1 Bat-fowling 157
Act II. Sc. 1 Chough 117
Act II. Sc. 2 Duck 238
Act II. Sc. 2 Goose 197
Act II. Sc. 2 Jay’s nest 122
Act II. Sc. 2 Sea-mells 122, 269
Act IV. Sc. 1 Sparrows 146
Act IV. Sc. 1 Barnacles 246
Act IV. Sc. 1 Peacock (note) 175
Act V. Sc. 1 Owls 96

Timon of Athens:
Act I. Sc. 1 Eagle 26
Act II. Sc. 1 [Gull] 267
Act III. Sc. 6 Swallow 277
Act III. Sc. 6 Tiring 38
Act IV. Sc. 3 Eagle 34

Titus Andronicus:
Act II. Sc. 2 Swallows 277
Act II. Sc. 3 Philomel 125
Act II. Sc. 3 Owl 94, 105
Act II. Sc. 3 Raven 105
Act II. Sc. 3 Lark 136
Act III. Sc. 1 [Raven] 99
Act III. Sc. 1 Lark 136
Act IV. Sc. 1 Philomel 125
Act IV. Sc. 1 Swan 205
Act IV. Sc. 2 Swallow 276
Act IV. Sc. 3 Pigeon 180, 183
Act IV. Sc. 4 Pigeons 184
Act IV. Sc. 4 Eagle 33
Act V. Sc. 2 Vulture 40
 Act V. Sc. 2 [Philomel] 125
313 Act V. Sc. 3 Fowl 236

Troilus and Cressida:

Act I. Sc. 1 Cygnet’s down 206
Act I. Sc. 2 [Eagles] 23
Act I. Sc. 2 [Crows] 110
Act I. Sc. 2 Daws 119
Act II. Sc. 1 Sparrows 146
Act II. Sc. 1 [Owl] 83
Act II. Sc. 2 Cormorant 260
Act II. Sc. 3 [Raven] 99
Act III. Sc. 1 Doves 196
Act III. Sc. 2 Sparrow 145
Act III. Sc. 2 Watch’d 45
Act III. Sc. 2 Falcon 54
Act III. Sc. 2 Tercel 54
Act III. Sc. 2 Ducks 54
Act III. Sc. 2 Plantage 192
Act III. Sc. 2 Turtle 180, 192
Act III. Sc. 3 Peacock 175
Act IV. Sc. 2 Lark 131
Act IV. Sc. 2 Crows 131
Act V. Sc. 1 Finch-egg 144
Act V. Sc. 1 Quails 219
Act V. Sc. 1 Owl 83
Act V. Sc. 1 Puttock 44
Act V. Sc. 2 Raven 100
Act V. Sc. 2 Parrot 272
Act V. Sc. 11 [Screech-Owl] 85
Act V. Sc. 11 [Goose] 197

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