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Keywords:

  • UVB radiation;
  • impact assessment;
  • marine biota;
  • mortality;
  • sensitivity

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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.

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.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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 (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 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 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 meta-analyses 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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 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 inline image, and mortality rates in the case of viruses were derived from infectivity decay rates (Noble & Fuhrman, 1997).

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
TaxaTotal, n n (UVB reduced) n (UVB increased)
Angiospermae62548
Bacteria16112932
Cnidaria70637
Crustacea19212468
Echinodermata18013743
Fish16110556
Macroalgae36128675
Microalgae429313116
Mollusca86860
Protista13013
Tunicates853
Virus61610
Global17841363421

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 meta-analyses 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 cut-off. 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 inline image, which allows comparisons across organisms 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 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).

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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.

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We tested the null hypothesis that changes in UVB relative to ambient values do not change biological performance (log-effect 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 log-effect 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 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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).

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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).

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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).

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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 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 4, 6 & 4, 8; Appendix S3).

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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.

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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).

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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.

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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).

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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).

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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.

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
ResponseLog effect ratio   
(a) Effect of life stage    
VariableParameterSE t P
Intercept−0.440.02−22.9< 0.0001
UVB relative0.230.0119.0< 0.0001
Mature/immature0.230.038.3< 0.0001
UVB relative × mature/immature−0.110.02−4.8< 0.0001
ANOVA R 2 = 0.28 F-ratio = 290 P < 0.001 
(b) Effect of hemisphere    
VariableParameterSE t P
Intercept−0.330.01−24.6< 0.0001
UVB relative0.210.0123.2< 0.0001
UVB relative × Southern (1)/immature(0)−0.040.02−2.00.04
ANOVA R 2 = 0.23 F-ratio = 179 P < 0.0001 
(c) Effect of year    
VariableParameterSE t P
Intercept−12.52.99−4.2< 0.0001
UVB relative0.220.0124.9< 0.0001
Year0.0060.0014.1< 0.001
UVB relative × year−0.010.001−8.6< 0.0001
ANOVA R 2 = 0.33 F-ratio = 72.7 P < 0.0001 

The extensive data set compiled provided evidence for adaptive or selective processes in increasing the resistance of marine 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).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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 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 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 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 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 & 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

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information

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. CSD2008-00077) and the project MEDEICG (ref. CTM2009-07013) of the Spanish Ministry of Science and Innovation.

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  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
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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.

Supporting Information

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  9. Supporting Information
FilenameFormatSizeDescription
geb784-sup-0001-si.pdf330K Appendix S1 Database of experimental assessments of the impacts of UVB radiation on marine biota used in this study.
geb784-sup-0002-si.pdf49K Appendix S2 Consideration of response traits when UVB and responses increase.
geb784-sup-0003-si.pdf39K Appendix S3 Summary of meta-analysis results derived from the data set of experimental responses of marine biota to increased or reduced UVB levels.

Please note: Wiley Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.