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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2013) 22, 131–144
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METAA N A LYS IS
Impact of elevated UVB radiation on
marine biota: a meta-analysis
Moira Llabrés1,2*, Susana Agustí1,2,3, Miriam Fernández1,4, Antonio Canepa1,5,
Felipe Maurin1,4, Francisco Vidal1,4 and Carlos M. Duarte1,2,6
1
LINCGlobal, CSIC-PUC, Facultad de
Ciencias Biológicas, Pontificia Universidad
Católica de Chile, Santiago, Chile, 2IMEDEA,
CSIC-UIB, Mallorca, Spain, 3The UWA
Oceans Institute and School of Plant Biology,
University of Western Australia, Crawley,
Australia, 4ECIM, Facultad de Ciencias
Biológicas, Pontificia Universidad Católica de
Chile, Santiago, Chile, 5ICM, CMIMA, CSIC,
Barcelona, Spain, 6The UWA Oceans Institute,
University of Western Australia, Crawley,
Australia
ABSTRACT
Aim The emission of chlorofluorocarbon compounds eroded the ozone layer,
raising incident ultraviolet B radiation to levels that affect biota. However, the role
of UVB radiation (280–315 nm), which remains elevated to date, as a possible
driver of the widespread global deterioration of marine ecosystems has not yet been
fully quantified. In this paper we assess the magnitude of the impacts of elevated
UVB radiation and evaluate the relative sensitivity to UVB across marine taxa and
processes.
Location The analyses presented are based on 1784 experimental assessments of
the impacts of UVB performed with natural radiation and organisms from different geographical areas, as well as with artificial radiation and cultured organisms at
many laboratories around the world.
Methods First we compiled the published literature concerning experimental
evaluation of the impacts of UVB on marine biota. Then a meta-analysis was
conducted with the data set obtained to evaluate the responses of marine organisms
and processes to enhanced and reduced UVB levels.
Results Increased UVB radiation leads to a sharp increase in mortality rates across
marine taxa, with protists, corals, crustaceans and fish eggs and larvae being most
sensitive. A general relationship between relative changes in UVB doses and mortality rates was developed. This relationship can help assess the effects of changes in
incident UVB radiation (past, present or future) on marine organisms.
*Correspondence: Moira Llabrés, LINCGlobal,
CSIC-PUC, Facultad de Ciencias Biológicas,
Pontificia Universidad Católica de Chile,
Almadea 340, Santiago, Chile.
E-mail: [email protected]
Main conclusions This meta-analysis demonstrates that mortality rates of
marine biota increase rapidly in response to elevated UVB radiation. The enhanced
mortality rates associated with currently elevated UVB levels may represent a major
threat to marine biota, possibly underlying recent widespread declines in the abundance of marine organisms ranging from corals to fish and krill.
Keywords
UVB radiation, impact assessment, marine biota, mortality, sensitivity.
I N T RO D U C T I O N
The development of the stratospheric ozone layer (SOL) about
2000 million years ago was a key event in the spread of life on
earth (Holland, 1994). Ozone filters out UVC radiation and also
absorbs some of the UVB radiation so the development of the
SOL attenuated much of the damaging effects of UVB on life. Yet
the incoming UVB levels remained stressful to organisms,
forcing the evolution of a range of strategies to mitigate damage,
including UVB-screening pigments, DNA repair mechanisms
© 2012 Blackwell Publishing Ltd
(Roy, 2000; Sinha & Häder, 2002) and behavioural responses to
avoid damage (Helbling & Zagarese, 2003; Häder et al., 2007).
The recent release of chlorofluorocarbons (CFCs) into the
atmosphere eroded the SOL at rates up to 4 DU (Dobson units)
per decade between 1979 and 1995 (Weatherhead & Andersen,
2006), increasing the incident UVB irradiance at the earth’s
surface accordingly (Madronich et al., 1998). The Montreal Protocol reduced the use and production of CFCs to prevent ozone
depletion, with an expected decrease in UVB irradiance during
the 21st century (UNEP, Environmental Effects Assessment
DOI: 10.1111/j.1466-8238.2012.00784.x
http://wileyonlinelibrary.com/journal/geb
131
M. Llabrés et al.
Panel, 2010). However, the SOL is not likely to recover to 1980
levels within the coming decades (Weatherhead & Andersen,
2006). Indeed, the area of the ozone hole over Antarctica reached
a maximum in 2006 (NASA, 2009) and a record destruction of
ozone over the Arctic was observed in 2011 (Manney et al.,
2011).
The reasons for the slow recovery of the SOL are not yet fully
understood but are believed to include parallel changes in
atmospheric chemistry and temperature as well as the release of
other chemicals that destroy ozone or facilitate ozone depletion
(Weatherhead & Andersen, 2006; UNEP, Environmental Effects
Assessment Panel, 2010) such as N2O, released from heavily
fertilized soils (Bouwman, 1998; Weatherhead & Andersen,
2006). The slow recovery of the SOL can also be explained by the
high stability of CFCs, which can take 40 to 50 years to reach the
stratosphere, leading to the persistence of their effect for
decades. Since enhanced UVB levels will continue to reach the
biosphere for the coming decades (Weatherhead & Andersen,
2006) there is a pressing need to understand the associated
impacts on marine biota. Indeed, increased UVB radiation has
had an impact upon vulnerable groups of terrestrial and aquatic
organisms (Häder et al., 2007), including amphibians (e.g.
Blaustein et al., 1994) and humans (Norval et al., 2007), inducing cancer in human and fish cells (Setlow et al., 1989; Setlow,
2008).
Most of the incoming UVB radiation reaching the biosphere
enters the ocean, which covers two-thirds of the earth’s surface.
Yet the impacts on marine biota were initially assumed to be
limited because of the expected low penetration of damaging
UVB radiation in the ocean (Smith & Baker, 1979; Morel et al.,
2007). Comparison by Morel et al. (2007) of submarine UV
spectral measurements in ultra-oligotrophic waters with earlier
results (Smith & Baker, 1979) showed that the UV penetration in
the clearest ocean waters had been underestimated, as confirmed
by a re-evaluation of laboratory measurements (further discussion in Vasilkov et al., 2002). UVB penetration is relatively low in
coastal waters, where 10% of the incident UVB radiation
(305 nm) reaches between 0.5 m, in turbid estuarine waters, and
12 m in clear coastal waters (Tedetti & Sempéré, 2006). UVB
penetrates much more deeply in clear oceanic waters, where
UVB levels sufficient to cause mortality of photosynthetic
plankton have been reported to penetrate down to 60 m in the
subtropical Atlantic Ocean (Llabrés & Agustí, 2006) and to 26 m
in the Mediterranean Sea (Llabrés et al., 2010). In contrast, the
impacts of UVB on marine benthic communities have been
proposed to be modest (Wahl et al., 2004), although corals
growing in shallow waters may be negatively affected by
enhanced UVB radiation (Shick et al., 1996; Banaszak & Lesser,
2009).
The realization of the potential damaging effects of elevated
UVB prompted research to experimentally assess the vulnerability to UVB of marine organisms ranging from viruses to fish
(Shick et al., 1996; Helbling & Zagarese, 2003; Häder et al., 2007;
Banaszak & Lesser, 2009). These experiments assessed the
impacts of UVB at scales ranging from molecular and cellular
levels to organism and population levels (see Appendix S1 in
132
Supporting Information) and provided ample evidence that
enhanced UVB has a severe impact on aquatic organisms
(Häder et al., 2007). However, a full quantitative assessment of
the magnitude of these impacts across marine taxa is still
pending (Banaszak & Lesser, 2009). Whereas some metaanalyses on the impacts of UV radiation on biota have been
reported (e.g. Searles et al., 2001; Bancroft et al., 2007), these
provide a limited basis for evaluating the impacts of enhanced
UV radiation on marine biota, as only 45% of the 73 reports
analysed by Bancroft et al. (2007) referred to marine organisms,
and none of the organisms in the meta-analysis by Searles et al.
(2001) were marine.
Here we quantify the magnitude of the effect of UVB radiation on marine biota and assess the variability across marine
taxa and processes in their relative sensitivity to UVB radiation.
We base this analysis on a thorough meta-analysis of the published literature focusing on the responses of marine organisms
to experimentally increased and reduced UVB.
METHODS
The published experimental literature on impacts of UV on
marine biota was searched using Web of Science® and Google®
Scholar accessed until August 2011 to find papers that met all of
the following criteria: (1) examine marine organisms growing
under ambient irradiance levels (papers using organisms cultured for generations under artificial light deprived of UV were
not included); (2) report a treatment corresponding to the full
ambient radiation (i.e. controls in this study); and (3) include
additional treatments either removing or enhancing UVB radiation relative to ambient levels. We found 168 papers that met
these requirements. The organisms examined were grouped into
broad operational taxonomic categories (Table 1) and the developmental stage in the case of animals (mature or immature) was
noted. Whereas species-specific differences are likely to be
Table 1 Number of experiments examining responses of marine
organisms to experimental changes in UVB radiation for various
taxa indicating those where UVB radiation was reduced or
increased.
Taxa
Total, n
n (UVB reduced)
n (UVB increased)
Angiospermae
Bacteria
Cnidaria
Crustacea
Echinodermata
Fish
Macroalgae
Microalgae
Mollusca
Protista
Tunicates
Virus
Global
62
161
70
192
180
161
361
429
86
13
8
61
1784
54
129
63
124
137
105
286
313
86
0
5
61
1363
8
32
7
68
43
56
75
116
0
13
3
0
421
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
UVB impact on marine biota
important, the number of species tested and the number of
independent experiments available for any one species was
insufficient to test for species-specific differences with statistical
confidence, so that only differences among phyla could be tested
for. The hemispheric origin (Northern or Southern Hemisphere) and the year when the study was conducted were also
recorded. UV radiation for a given depth was estimated using
the extinction coefficient of UVR with depth, in the area in
which the experiment was performed. Extinction coefficients
vary geographically and were obtained from the literature
(Morel et al., 2007; review of Tedetti & Sempéré, 2006). Experiments that removed UV often considered multiple treatments
including removal of UVB or UVA, removal of both or of all
solar radiation. Whenever multiple treatments were reported,
we extracted information on the response to removal of UVB
alone. The wide range of response traits assessed were broadly
classified as: (1) molecular- or cellular-level responses, such
as production of UV-screening compounds; (2) metabolic
responses, such as photosynthetic and respiration rates; and (3)
individual responses, including behavioural patterns, growth
rate, mortality rate, and other demographic events, such as
reproductive rates, maturation stage and settlement (see Appendix S1 in Supporting Information). Survival data, reported as
percentages (Ps) were converted to specific daily mortality rates
⎛ Ps ⎞ ⎞
⎛
− ln ⎜
⎝ 100 ⎟⎠ ⎟
⎜
μ
=
⎜
⎟ , and mortality rates in the case of viruses
days ⎟
⎜
⎝
⎠
were derived from infectivity decay rates (Noble & Fuhrman,
1997).
The database produced included 1784 individual experimental assessments of the impacts of UVB radiation on marine biota
(see Appendix S1). An experimental assessment is defined here
as the set of the biological processes examined under ambient
irradiance relative to that under each of the altered UVB levels,
whether increased or reduced, imposed experimentally. Each
experimental assessment represents a data point in the metaanalyses conducted here (i.e. 1784 reports of paired control and
treatment data). All experiments on fish focused on planktonic
stages (eggs and larvae) as adult fish can avoid the impacts of
UVB by migrating to deeper layers.
The experiments could be classified into two broad categories:
(1) experiments that partially or totally reduced UVB radiation
relative to that received by the organisms in their habitat, using
either UVB-opaque materials or transplanting the organisms to
deeper layers with reduced incident UVB radiation; and (2)
experiments that increased UVB radiation using artificial illumination with UV lamps or transplanting organisms to shallower depths. Whereas the formal definition of UVB radiation
includes radiation between 280 and 315 nm, some of the experiments used, for operational reasons, filters with a 320 nm cutoff. In either case, the control was defined as the experimental
treatment where the organisms were exposed to the ambient
radiation in their habitats. The information delivered and the
inferences that can be drawn from these two types of experiments differ fundamentally. Increased UVB radiation tells us
about the sensitivity of organisms to UVB levels that they have
not experienced yet. The responses to removal of UVB elucidate
the stress from UVB levels already experienced by marine organisms, estimated by the resulting improvement in performance
upon removal of UVB radiation. The majority of the experiments assessed the response to reduced UVB irradiance (76%)
and fewer studies (24%) evaluated the effects of increased
UVB irradiance (Table 1), which requires more cumbersome
experimental designs.
The first experiment on the impacts of UVB on marine biota
was published in 1979 (an experiment using anchovy eggs and
larvae; Hunter et al., 1979). The first experiment was conducted
in 1976 (Hobson & Hartley, 1983) but most of the experiments
(97%) in the data set were conducted after 1990. Hence, the
experimental assessment of responses to reduced UVB radiation
in the data set refers to control ambient UVB levels already
elevated by anthropogenic erosion of the ozone layer, and serves,
therefore, to assess the associated impacts on marine biota.
The database contained 860 experiments in which artificial
light sources were used, alone or as a supplement to solar radiation, with the remainder using solar radiation. The use of artificial light sources differed depending on the taxa examined, as
most of the experiments with crustaceans used artificial light
(89% of the experiments with crustaceans) whereas none of the
experiments on Cnidaria, Mollusca or viruses used artificial
light sources.
A meta-analysis was conducted to compare the responses to
changes in UVB radiation across organisms and response variables (Gurevitch & Hedges, 1993). A first step to conduct this
meta-analysis involved the development of standardized metrics
for treatments and effects, thereby allowing their comparison.
The standardized metric for treatments is provided by the
relative change in ultraviolet radiation in the experimental
treatments (UVBtreatment) relative to the control representing
the ambient irradiance (UVBcontrol), calculated as the ratio
UVBtreatment
, which allows comparisons across organisms
UVBcontrol
exposed to different incident ambient UVB radiation levels.
Relative UVB values higher and lower than 1 indicate experimental treatments where UVB was higher or lower than the
ambient values, respectively.
A second step in conducting the meta-analysis involved the
standardization of the response variables, allowing comparison
across taxa and traits. Responses across experiments assessing
different traits and different experimental levels of UVB were
compared through the effect ratio. The effect ratio of response
traits that indicate stress (e.g. mortality rates, cellular damage)
was calculated as the ratio of the value in the treatment relative
to the control, and that of response traits that signal improved
organism performance (e.g. growth) was calculated as the
inverse of this ratio (as the ratio of the response value in
the control over that in the experimental treatment; Fig. 1;
Gurevitch & Hedges 1993). The log-effect ratio was used to
analyse responses. A log-effect ratio > 0 signals adverse effects
on the organisms and a log effect ratio < 0 signals improved
organism performance (Fig. 1). Responses were considered an
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
133
M. Llabrés et al.
greater number of parameters and allowed comparison of the
parameters of the equations across taxa and processes. However,
model II regression equations were fitted when the relationships
showed heteroscedasticity.
RESULTS
Figure 1 Description of the interpretation of the relationship
between log effect ratio and relative UVB. The log effect ratio, the
ratio between the response trait under experimental and control
UVB levels (or vice versa), reflects organism performance relative
to that at ambient UVB, with log effect ratio values > 0 indicating
an impact and < 0 indicating improved performance. The relative
UVB index, the ratio of the experimental to ambient UVB
radiation, reflects increased (relative UVB > 1) or reduced
(relative UVB < 1) experimental UVB radiation relative to
control. The marble at the 1,0 coordinate indicates the control
value (i.e. the performance at ambient UVB). The expectation
that increased UVB leads to deteriorated performance while
reduced UVB improves organism performance predicts that there
should be no data points in the quadrants with UV < 1 and log
effect ratio > 0 and that with UV > 1 and log effect ratio < 0.
improvement whenever the trait assessed positively affects the
performance of the organisms by affecting their population size
(e.g. increased life span, reproduction or growth rate) or their
metabolic balance (e.g. increased photosynthetic rates), and
negatively otherwise (see Appendix S2).
We tested the null hypothesis that changes in UVB relative
to ambient values do not change biological performance (logeffect ratio = 0, independently of the increased or decreased
UVB relative to ambient values). The null hypothesis would be
rejected, inferring a consistent effect of UV radiation on the
performance of marine biota, if the log effect ratio is significantly > 0 at relative UVB ratios > 1 and the log effect ratio is
significantly < 0 at relative UVB ratios < 1 (Fig. 1). Possible differences in the relationship between log effect ratio and relative
UVB between experiments where UVB was provided by solar
radiation versus those in which artificial light sources were used
were tested using ANCOVA.
The relationship between responses, as indicated by the logeffect ratio, and UVB doses, as indicated by the relative UVB,
was described using linear regression analysis. Inspection of the
relationships showed linear fits to be as adequate for modelling
this relationship as more complicated equations, so that use of
linear regressions maximized the robustness, as the F-statistic, of
the fitted relationships compared with equations involving a
134
The assessment of experimental responses to increased UVB
radiation showed that only 8.6% of the experiments conducted
yielded unexpected results (i.e. improved conditions at
increased UVB or vice versa; Fig. 1), demonstrating a dominance of consistent UVB impacts on organism performance.
Assessment of the log effect ratio in response to altered UVB
radiation showed that marine organisms responded by greatly
improving their performance when UVB was reduced and
showed evidence of damage when UVB was elevated above
ambient levels (Fig. 2a). Decreasing UVB reduced, on average,
the mortality rates of marine biota by 81% (log effect ratio =
-0.72 ⫾ 0.04; Fig. 2b, Appendix S3) whereas increased UVB led
to mortality rates 2.45 times greater than those under ambient
UVB radiation across experiments (log effect ratio = 0.389 ⫾
0.034; Fig. 2b, Appendix S3). Fish and bacteria showed the
highest average decline in mortality rates to values down to 95 ⫾
6.5% and 85 ⫾ 2% relative to controls when UVB radiation was
reduced, respectively (log effect ratio = -1.282 ⫾ 0.091 and
-0.833 ⫾ 0.118, respectively; Fig. 2c, Appendix S3). The extent
of responses to increased or reduced UVB radiation differed
significantly across taxa (ANOVA; F = 10, P < 0.001, n = 1363 for
reduced UVB; F = 70.3, P < 0.001, n = 421, for increased UVB;
Fig. 3) with fish showing the greatest positive response to
reduced UVB radiation, and protists, cnidarians and fish
showing the strongest impact of increased UVB radiation across
functions (Figs 2a & 3; Appendix S3). Variability among species
within the broad taxonomic groups considered here added to
the unexplained variability in these analyses. The responses to
increased and reduced UVB were generally consistent across
functions, with mortality rates and secondarily cellular and
behavioural traits showing the strongest sensitivity and
metabolic processes being the least sensitive to changes in UVB
radiation (Fig. 2b).
There was a strong relationship between the extent of biological responses and the changes in UVB relative to ambient values
across all taxa and functions (Figs 4 & 5). The slope of the fitted
regression equation between the log-effect ratio and the relative
UVB ratio represents the sensitivity of the processes to UVB
radiation (i.e. the relative change in performance per relative
change in UVB radiation). A slope of 1 indicates that the relative
biological response is proportional to the relative change in
UVB, whereas slopes significantly > 1 and < 1 indicate that the
biological response respectively amplifies or buffers the change
in UVB (Fig. 6). In general, the functional responses varied more
slowly than the rate of UVB increase (slope < 1; Fig. 6). Mortality
rates showed the greatest overall sensitivity to UVB radiation
(Figs 6 & 7; Appendix S3). Since mortality rates were so strongly
affected by UVB radiation, the effects on other functions might
be underestimated as they were of necessity measured on the
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
UVB impact on marine biota
UVB reduced (UVB rel < 1 )
UVB enhanced (1 < UVB rel < 9 )
GLOBAL
Angiosperms
Bacteria
Fish
Chordata
Tunicates
Cnidarians
Crustaceans
Echinoderms
Macroalgae
Microalgae
Molluscs
Protists
Viruses
a
{
-1.2
-0.8
-0.4
0
0.2
0.4
0.6
b
GLOBAL
Mortality
Cellular-Molecular
Demography
Growth
Behaviour
Metabolism
-0.8
Figure 2 The response of marine biota
to experimentally reduced or enhanced
UVB radiation (relative to control).
Mean ⫾ SE log effect ratio for all taxa
across functions (a), for all functions
across taxa (b), and for mortality rates
(c) in response to experimentally
reduced or enhanced UVB radiation.
A log effect ratio < 0 represents an
improvement in the trait examined and
a log effect ratio > 0 represents a
deterioration in performance (Fig. 1).
-0.6
-0.4
-0.2
0
0.2
0.4
GLOBAL
Angiosperms
Bacteria
Fish
Chordata
Tunicates
Cnidarians
Crustaceans
Echinoderms
Macroalgae
Microalgae
Molluscs
Protists
Viruses
0.6
c
{
surviving organisms. The relationships were steepest for fish, the
functional responses of which increased as the 3/2 power of
incident UVB, thereby amplifying changes in incident UVB
across all functions (Figs 4a,c, 6 & 7; Appendix S3).
The mortality response to changes in UVB was steepest for
fish eggs and larvae. Indeed, early life stages were more vulnerable to increased UVB than adult organisms, as the slope of
the relationship between log-effect ratio and the relative UVB
was steeper for early life stages than for adults across taxa (0.23
vs. 0.12, respectively; ANCOVA, t-test, P < 0.001; Table 2a).
ANCOVA showed that there was no difference in the relationship between log effect ratio and relative UVB radiation depending on whether solar radiation or artificial light sources were
used, except for echinoderms, where the log effect ratio was
somewhat smaller for a given relative UV when artificial light
was used, and microalgae, where the slope (sensitivity) of the log
effect ratio versus relative UV was somewhat higher when artificial light was used.
The extensive data set compiled provided evidence for adaptive or selective processes in increasing the resistance of marine
-1.2
-0.8
-0.4
0
0.2
0.4
0.6
Log effect ratio
biota to UVB radiation. Organisms from the Southern Hemisphere, which in general support a greater UVB radiation for
a given latitude than those in the Northern Hemisphere
(Seckmeyer & McKenzie, 1992; Relethford & McKenzie, 1998),
were significantly more resistant to increased UVB radiation
than those from the Northern Hemisphere, as the slope of the
relationship between log-effect ratio and the relative UVB was
significantly steeper for organisms in the Northern Hemisphere
compared with those in the Southern Hemisphere (0.21 vs. 0.17,
respectively; ANCOVA, t-test, P < 0.05; Table 2b). Likewise, we
detected a significant annual decline in the slope of the relationship between log effect ratio and the relative UVB (slope decline
= 0.005 ⫾ 0.0001 year-1; ANCOVA, t-test, P < 0.0007) since 1976
(Table 2c). This change in slope with time suggests that the
relative impact of UVB radiation on marine biota has declined
somewhat since UVB levels first increased in response to the
erosion of the SOL. Elevated UVB is an important driver of
increased mortality, and therefore has great potential to act as a
selective force, as demonstrated for marine viruses (Garza &
Suttle, 1998).
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
135
M. Llabrés et al.
ECHINODERMS
ANGIOSPERMS
GLOBAL
GLOBAL
Mortality
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.3
-0.2
-0.6
0.4
0.2
0
-0.1
-0.4
GLOBAL
GLOBAL
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.8
-0.4
0.4
0.2
0
-0.6
-0.4
GLOBAL
GLOBAL
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.4
0
0.2
0.4
-0.6
0.6
-0.4
-0.2
GLOBAL
GLOBAL
Mortality
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.8
-0.4
0.2
0
0.4
-0.8
0.6
-0.4
0.6
0
0.2
0.4
PROTISTS
GLOBAL
GLOBAL
Mortality
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0
GLOBAL
GLOBAL
Mortality
Mortality
Cellular-Molecular
Cellular-Molecular
Demography
Demography
Growth
Growth
Behaviour
Behaviour
Metabolism
Metabolism
-0.6
-0.4
-0.2
UVB reduced
0
0.2
0.4
0.6
VIRUSES
CRUSTACEANS
-0.8
0.4
0
CNIDARIANS
-0.8
0.2
MOLLUSCS
TUNICATES
-1.2
0.4
MICROALGAE
Mortality
-0.8
0
-0.2
FISH
-1.2
0.2
MACROALGAE
Mortality
-1.2
0
-0.2
BACTERIA
0.2
0.4
-0.6
0.6
-0.4
-0.2
UVB reduced
UVB enhanced
0
UVB enhanced
Log effect ratio
Figure 3 The mean ⫾ SE log effect ratio for individual taxa in response to experimentally reduced or enhanced UV radiation. A log effect
ratio < 0 represents an improvement in the trait examined and a log effect ratio > 0 represents a deterioration in performance (Fig. 1).
136
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
UVB impact on marine biota
2
a
b
1
0
-1
Figure 4 The relationship between
biological responses and the change in
UVB radiation. The relationship between
the responses to experimental UVB
manipulation, as indicated by the log
effect ratio, and the change in UVB
radiation relative to the ambient levels
experienced by the organisms across
functions and taxa. Symbol colours
identify different (a) taxa or (b)
functions, and line colours identify
regression equations fitted for (c)
individual taxa and (d) functions
(Appendix S3). The dotted lines
delineate the quadrants displayed in
Fig. 1, intersecting at the (1,0)
coordinate, thereby helping comparison
with Fig. 1.
Log effect ratio
-2
-3
-4
c
d
1
0
All organisms
Angiosperms
Bacteria
Fish
Tunicates
Cnidarians
Crustaceans
Echinoderms
Macroalgae
Microalgae
Mollusca
Protists
Viruses
-1
-2
-3
-4
0
2
DISCUSSION
The analysis presented here extends previous meta-analyses of
the impacts of UVB radiation on marine biota (e.g. Bancroft
et al., 2007) to encompass a much broader database, a greater
diversity of response variables, and to quantify the relationship
between responses and UVB doses. Yet the analysis provided
here does not represent an exhaustive assessment across all taxa
and processes because there are still only a few studies for some
of them (e.g. tunicates, protists; see Table 1).
The impacts of UVB radiation reported here are restricted to
organisms growing near the sea surface, comprising the top
third to quarter of the photic layer, where UVB radiation levels
may cause impacts. Most marine primary production, both
benthic and planktonic, occurs within this layer and the planktonic eggs and larvae of marine organisms, which are the most
sensitive stages to UVB impacts, are typically buoyant, floating
on the surface where they are exposed to the highest UVB
levels. Moreover, impacts will vary seasonally, and are likely to
be highest in the spring when UVB radiation is typically
highest (e.g. McKenzie et al., 1999). Indeed, spring is a critical
period for the marine ecosystem, when phytoplankton blooms
occur in the temperate and polar oceans and when most
animals reproduce.
The strong responses to reduced UVB radiation relative to
ambient values demonstrate that ambient UVB radiation has a
large effect on organisms at present. Since all experiments
4
6
8
Mortality
Cellular-Molecular
Demography
Growth
Behaviour
Metabolism
0
2
4
6
8
UVB relative
included here were conducted after erosion of the SOL by CFCs
had begun, the results presented imply that the ensuing increase
in UVB may have had a heavy impact on marine biota. Clear
evidence on the impacts of elevated UVB on marine biota is
provided by the 81% reduction in mortality rates across taxa
when UVB radiation is reduced, reaching the maximum expression in the major reduction in mortality of fish larvae and tunicates when UVB radiation is excluded. Whereas differences in
the response to UVB radiation among the broad taxonomic
categories considered here were significant, differences among
species within these categories are likely to be important, due to
differential capacities to photoacclimate and to deploy protective mechanisms, adding to the residual variability unaccounted
for in the analyses conducted. Many other factors affect the
impact of UVB on marine organisms, including concurrent
photosynthetically active radiation (PAR) levels (e.g. Cullen
et al., 1992) and nutrient concentrations (Carrillo et al., 2008).
Ecosystem buffers may include shading by plant canopies and
positive responses resulting from effects of UVB on species
interactions, including the release of predatory pressure. The
role of all these factors (species-specific resistance and photoacclimation capacities, PAR, nutrient levels and species interactions) could not be assessed here and adds to the uncertainty in
evaluating the impacts of elevated UVB radiation on marine
ecosystems.
The analysis presented suggests the operation of adaptive or
selective processes in response to elevated UVB radiation, as the
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
137
M. Llabrés et al.
Angiosperms
Cnidarians
Bacteria
0.4
0.2
1
1
0
0.5
0
0
-1
-0.2
-0.5
-2
-0.4
0
1
2
3
0
2
Crustaceans
4
6
-1
0
1
2
3
Echinoderms
5
4
6
7
Fish
1
1
1
0
0
Log effect ratio
0
-1
-1
-1
-2
-2
0
4
2
6
10
8
0
-2
-3
1
2
Macroalgae
3
4
5
7
6
-4
0
1
0.5
Microalgae
2
2.5
Protists
1
1
1
1.5
0
0
0.6
-1
-1
0.2
0
1
2
3
4
5
6
-2
1
2
3
4
5
0
1
2
3
Tunicates
0.4
0
-0.4
-0.8
0
1
2
3
4
5
UVB relative
Figure 5 The relationship between log effect ratio and relative UVB for the different taxa examined here. Solid lines show the fitted
regression equations (Appendix S3).
138
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
UVB impact on marine biota
Mortality
GLOBAL
Cellular-Molecular
Growth
Demography
Metabolism
a
Behaviour
0.2
0.4
0.6
GLOBAL
Fish
Protists
Echinoderms
Crustaceans
Microalgae
Macroalgae
Tunicates
Angiosperms
Bacteria
Cnidarians
b
0
0.5
1
1.5
Sensitivity
Figure 6 Sensitivity of marine biota to changes in UVB
radiation. Slope ⫾ SE of the fitted relationships between log effect
ratio and relative UVB radiation for various responses (a) and
taxa (b), describing their sensitivity to changes in UVB radiation.
biota in the Southern Hemisphere was more resistant to UVB
radiation than that in the Northern Hemisphere and the
response of marine biota to enhanced UV levels declined from
1976 to 2009. Extrapolation of the rate of reduction in biological
effects over time (Table 2c) suggests that the impact of enhanced
UV radiation may dissipate in two decades, although this may
differ for individual taxa or processes. Given the sensitivity of
mortality rates to enhanced UVB, these results suggest that
enhanced UVB may have acted as an evolutionary driver, genetically sieving marine biota to select more resistant organisms, a
suggestion that needs be tested.
The decline in ozone levels was greatest in the Southern
Hemisphere, with a decline in total column ozone of as much
as 18% from 1979 to 1995 over the Southern Ocean compared
with a decline of 10% over the Arctic for the same period
(Weatherhead & Andersen, 2006), although an unprecedented
decline in Arctic ozone in the spring of 2011 has just been
detected (Manney et al., 2011). Subtropical regions supported
more modest declines of ozone – about 4% from 1979 to 1995
(Weatherhead & Andersen, 2006). As a consequence, incident
UVB radiation increased greatly relative to baselines following
the erosion of the ozone layer. For instance, the incident UVB
radiation at 45° S in New Zealand increased by 15–20% in
1998–99 relative to 1970 levels, with an overall increase rate in
DNA-damaging UV radiation of 1.78% year-1 at that latitude
(McKenzie et al., 1999).
The relationships between log effect ratio and relative UVB
levels derived here can be used to evaluate the expected impacts
of the increased UVB on marine biota. Elevated UVB doses with
depletion of the SOL were not reported for the individual
locations where experiments were conducted, so the evaluation
cannot be done for specific studies. This evaluation can be based
on the use of the general relationship between the responses to
increased UVB and reported regional or local rates of increase in
UVB with depletion of the SOL. For instance, these relationships
predict that an increase in UVB radiation of 15%, comparable to
that expected for the Southern Ocean between 1979 and 1995, is
expected to result in a deterioration in organism performance
across marine taxa by 59%, and a deterioration in performance
of 38% with an increase in UVB radiation of 5%, comparable to
that expected between 1979 and 1995 for subtropical regions.
We emphasize that these calculations are only indicative of the
possible magnitude of the impacts resulting from the observed
UVB increase.
The increase in mortality rates resulting from the observed
UVB increase is expected to be even greater for fish larvae and
eggs, protists and corals, the taxa which are most sensitive to
UVB. The greater sensitivity of eggs and larvae detected here is
consistent with results from meta-analysis of UVB impacts on
amphibian species (Bancroft et al., 2008) and aquatic species
(Bancroft et al., 2007), which concluded that early life stages are
more sensitive than adult animals. Hence, our results suggest
that the marine biota has been greatly affected by the realized
elevated levels of UVB since the 1970s, particularly at high latitudes in the Southern Hemisphere where the UVB increase has
been greatest.
Although the impact of increased UVB ranks only second to
warming in terms of potential stressors in the ocean surface
(Halpern et al., 2008), elevated UVB radiation has been
neglected in evaluations of possible anthropogenic stresses
accounting for the current widespread demise of marine
biota (Lotze et al., 2006; Worm et al., 2006; Jackson, 2008).
The emphasis on global warming, eutrophication and, more
recently, ocean acidification, all of which increased in parallel to
elevated UVB levels (Duarte et al., 2009), may have precluded
the formal exploration of elevated UVB radiation as a possible
cause of the accelerated declines in marine biota, despite evidence that UVB may induce coral bleaching (Gleason & Wellington, 1993) and significant phytoplankton mortality in the
ocean (Llabrés & Agustí, 2006; Agustí & Llabrés, 2007; Llabrés
et al., 2010). We believe that this neglect stems from the widespread misconception that the Montreal Protocol, considered as
an example of a success story in environmental legislation,
solved the problem of elevated UV radiation (Weatherhead &
Andersen, 2006). Indeed the Montreal Protocol was successful in
avoiding further deterioration of the SOL and laying the foundations for its recovery, but this recovery has not yet occurred
(UNEP, Environmental Effects Assessment Panel, 2010). This
misconception is particularly surprising, given the wealth of
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
139
M. Llabrés et al.
Bacteria
1
Fish
Cnidarians
0.2
1
0
0
0
-0.2
-1
-0.4
-1
-2
Log effect ratio
-0.6
-3
-2
0
1
2
3
4
5
6
0
-0.8
0.5
Crustaceans
1
1.5
2
0
2.5
1
2
3
4
5
6
7
Microalgae
Echinoderms
1
1
0
0
-0.2
-1
-0.4
-2
-0.6
0
2
4
6
8
10
0
-1
0
0.5
1
1.5
-2
1
2
3
4
5
UVB relative
Figure 7 Relationship between mortality response of marine biota and changes in UVB radiation. The relationship between the changes in
mortality, as the log effect ratio, in response to changes in UVB radiation, as the relative UVB radiation for different taxa. Solid lines show
the fitted regression equations (Appendix S3).
evidence that elevated UV levels continue to have an impact on
human health (Norval et al., 2007; Setlow, 2008).
Evidence of accelerated decline of marine biota has accumulated since the 1970s (Gardner et al., 2003; Myers & Worm, 2003;
Atkinson et al., 2004; Bruno & Selig, 2007; Jackson, 2008;
Waycott et al., 2009). Our analysis shows that the levels of
increase in UVB as result of anthropogenic damage to the SOL
are sufficient to cause a significantly increased mortality rate in
marine biota. Indeed, elevated UVB levels must be included
among the possible drivers, together with other stresses, of the
parallel decline in marine biota. For instance, krill, which have
been shown to be highly vulnerable to increased UVB radiation
(Damkaer et al., 1980), declined 60-fold in abundance in the
Southern Ocean between 1970 and 2003 (Atkinson et al., 2004).
While reduced ice cover was proposed as the driver of this
decline (Atkinson et al., 2004), this effect may have been
enhanced further by the greatly increased UVB radiation over
the Southern Ocean during this time interval. Indeed, both
factors may act together, as reduced sea ice increases exposure to
UVB radiation. The Canadian cod stock, the eggs and larvae of
which float near the sea surface (Vallin & Nissling, 2000), collapsed in the late 1980s as a result of overfishing and failed to
140
recover despite a moratorium (Fu et al., 2001). The high vulnerability of cod eggs and larvae to increased UVB levels (Béland
et al., 1999; Lesser et al., 2001) may have played a role in delaying
their recovery. The decline of corals in the tropics and subtropics
is also consistent with increased UVB levels, as the results presented here show that they rank amongst the organisms most
vulnerable to UVB. Moreover, corals experienced widespread
mortality in 1997–98 (Wilkinson, 1998), an event that was
attributable to the effects of elevated temperature during El
Niño (Glynn, 1988), but which may have also involved elevated
UVB levels since the summer of 1998–99 experienced one of the
highest levels of UV radiation so far recorded over the Southern
Hemisphere (McKenzie et al., 1999). Indeed, Banaszak & Lesser
(2009) suggested that UVB radiation may enhance the impacts
of warming on corals, as loss of photoprotective pigments following warming-induced bleaching events renders corals more
vulnerable to UVB radiation. Oceanic primary production has
also declined (Behrenfeld & Falkowski, 1997; Boyce et al., 2010)
and the least productive areas of the ocean expanded (Polovina
et al., 2008; Boyce et al., 2010), consistent with the high mortality induced by UV radiation on Prochlorococcus, the dominant
autotroph in the clear waters of the oligotrophic ocean (Gleason
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
UVB impact on marine biota
Cellular-Molecular
Mortality
Demography
1
1
1
0
0
-1
Log effect ratio
-1
-3
-1
-2
0
2
4
8
6
0
1
2
3
4
5
6
-2
7
1
0
0
0
-1
-1
-1
2
3
4
4
5
6
-2
0
2
6
4
6
8
10
Metabolism
1
1
2
Behaviour
Growth
1
-2
0
8
-2
1
2
3
4
5
UVB relative
Figure 8 The relationships between log effect ratio and relative UVB for the various biological functions examined here. Solid lines show
the fitted regression equations (Appendix S3).
Table 2 General linear models showing
the effect of the interaction between the
relative UVB radiation and (a) the stage
of the organism (immature = 0, adult =
1, (b) the hemisphere of provenance of
the organism (South = 1, North = 0,
on the response to changes to UVB,
as log effect ratio; and (c) the effect of
the year when the experiment was
conducted. Parameter estimates for the
individual taxa not shown.
Response
(a) Effect of life stage
Variable
Intercept
UVB relative
Mature/immature
UVB relative ¥ mature/
immature
ANOVA
(b) Effect of hemisphere
Variable
Intercept
UVB relative
UVB relative ¥ Southern
(1)/immature(0)
ANOVA
(c) Effect of year
Variable
Intercept
UVB relative
Year
UVB relative ¥ year
ANOVA
Log effect ratio
Parameter
-0.44
0.23
0.23
-0.11
SE
0.02
0.01
0.03
0.02
t
-22.9
19.0
8.3
-4.8
R2 = 0.28
F-ratio = 290
P < 0.001
Parameter
-0.33
0.21
-0.04
SE
0.01
0.01
0.02
t
-24.6
23.2
-2.0
R2 = 0.23
F-ratio = 179
P < 0.0001
Parameter
-12.5
0.22
0.006
-0.01
R2 = 0.33
SE
2.99
0.01
0.001
0.001
F-ratio = 72.7
t
-4.2
24.9
4.1
-8.6
P < 0.0001
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd
P
< 0.0001
< 0.0001
< 0.0001
< 0.0001
P
< 0.0001
< 0.0001
0.04
P
< 0.0001
< 0.0001
< 0.001
< 0.0001
141
M. Llabrés et al.
& Wellington, 1993; Llabrés & Agustí, 2006; Llabrés et al., 2010).
Again, oligotrophication increases UVB penetration and,
accordingly, the doses received by autotrophs, thereby possibly
leading to a positive feedback. Reduced nutrient supply as oligotrophic areas expand may further weaken the capacity of
autotrophs to develop protective mechanisms against UVB
radiation (e.g. photoprotective pigments, DNA repair).
The relationship presented here between the performance of
marine biota, particularly mortality rates, and elevated UVB
radiation is not solely applicable to understanding the impacts
from SOL depletion, as elevated – or reduced – UVB radiation
can also derive from other local or global changes. For instance,
UVB levels depend on atmospheric aerosol loads and cloud
cover, and the underwater UVB penetration reaching the organisms depends on dissolved organic carbon and particle loads in
the water column (Zepp et al., 2007). Hence, the results provided here can also be used to estimate the effects of altered UVB
levels incident on the organisms resulting from changes in these
processes, such as the global reduction in oceanic chlorophyll a,
that may result in increased penetration of UVB (Boyce et al.,
2010).
The impacts on marine biota derived from synergies between
elevated UVB and other stresses should be explored further
(Banaszak & Lesser, 2009). Indeed, Bancroft et al. (2008) conducted a meta-analysis of the impacts of UVB on amphibian
species and concluded that these impacts are greater than
expected from additive considerations whenever the organisms
are exposed to additional stressors. We suggest that elevated
UVB may have played a role in enhancing biological declines in
the ocean by inducing synergies with the more proximal drivers.
Elevated UVB radiation must be considered, together with overfishing and climate change, among the candidate drivers for the
recent widespread decline of biota in the ocean.
ACKNOWLEDGEMENTS
This research is a contribution to the LINCGlobal programme
(CSIC-PUC) and was partially funded by the Malaspina-2010
project of the CONSOLIDER programme (ref. CSD200800077) and the project MEDEICG (ref. CTM2009-07013) of the
Spanish Ministry of Science and Innovation.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
Appendix S1 Database of experimental assessments of the
impacts of UVB radiation on marine biota used in this study.
Appendix S2 Consideration of response traits when UVB and
responses increase.
Appendix S3 Summary of meta-analysis results derived from
the data set of experimental responses of marine biota to
increased or reduced UVB levels.
As a service to our authors and readers, this journal provides
supporting information supplied by the authors. Such materials
are peer-reviewed and may be re-organized for online delivery,
but are not copy-edited or typeset. Technical support issues
arising from supporting information (other than missing files)
should be addressed to the authors.
BIOSKETCH
Moira Llabrés is a post-doctoral researcher at the
Laboratorio Internacional de Cambio Global
(LINCGlobal, CSIC-PUC). Her doctoral research was
carried out at Mediterranean Institute of Advanced
Studies (IMEDEA, Spain) and focused on the
importance of ultraviolet radiation as a factor inducing
cell death in marine phytoplankton. Her work focuses
on the effect of UV radiation on phytoplankton with
most of her experiments being performed with natural
phytoplankton populations in different areas of the
Atlantic Ocean, Indian Ocean, the Southern Ocean and
the Mediterranean Sea.
Editor: Michael Rex
Global Ecology and Biogeography, 22, 131–144, © 2012 Blackwell Publishing Ltd