© 2001 by The Society for Integrative and Comparative Biology
Influence of Ozone-Related Increases in Ultraviolet Radiation on Antarctic Marine Organisms1
1 Department of Biology, University of San Francisco, San Francisco, California 94117-1080
2 Department of Biology, State University of New York, Geneseo, New York 14454
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Every spring for the past two decades, depletion of stratospheric ozone has caused increases in ultraviolet B radiation (UVB, 280–320 nm) reaching Antarctic terrestrial and aquatic habitats. Research efforts to evaluate the impact of this phenomenon have focused on phytoplankton under the assumption that ecosystem effects will most likely originate through reductions in primary productivity; however, phytoplankton do not represent the only significant component in ecosystem response to elevated UVB. Antarctic bacterioplankton are adversely affected by UVB exposure; and invertebrates and fish, particularly early developmental stages that reside in the plankton, are sensitive to UVB. There is little information available on UV responses of larger Antarctic marine animals (e.g., birds, seals and whales). Understanding the balance between direct biological damage and species-specific potentials for UV tolerance (protection and recovery) relative to trophic dynamics and biogeochemical cycling is a crucial factor in evaluating the overall impact of ozone depletion. After more than a decade of research, much information has been gathered about UV-photobiology in Antarctica; however, a definitive quantitative assessment of the effect of ozone depletion on the Antarctic ecosystem still eludes us. It is only obvious that ozone depletion has not had a catastrophic effect in the Antarctic region. The long-term consequences of possible subtle shifts in species composition and trophic interactions are still uncertain.
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INTRODUCTION |
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Environmental concerns about ozone depletion arise from the fact that the ozone layer in Earth's atmosphere is an effective filter for the biologically harmful ultraviolet B radiation (UVB, 280–320 nm) present in sunlight. Even without ozone depletion, UVB penetrates into surface waters of the oceans and is a daily environmental hazard to many marine organisms. Therefore, increased ultraviolet radiation associated with recorded and predicted decreases in global stratospheric ozone is expected to have ecological consequences in marine communities. The most extensive destruction of ozone occurs over the Antarctic continent and the surrounding Southern Ocean. In this geographic region, over 50% depletion of column ozone has occurred each spring (Sept–Dec) for the past two decades, causing increased amounts of UVB to reach Antarctic marine environments (Frederick et al., 1998
; Schoeberl et al., 1996).
A major obstacle in assessing ecological UVB effects on the Antarctic marine ecosystem is that while ozone depletion has been occurring for over 20 yr, scientists did not accept the possibility of the Antarctic ozone "hole" until nearly a decade after the depletion cycles began (Solomon, 1990). Therefore, the first efforts to examine the biological effects of Antarctic ozone depletion did not commence until after 10 yr of repeated seasonal ozone depletion had already occurred. By this time any ozone-related changes in the marine environment would have been initiated and the ecosystem altered before biological investigations began. Species or individuals within populations that could not tolerate the immediate changes in UVB during the early rounds of ozone depletion would have been eliminated. The organisms present today are those that have survived two decades of increased springtime UVB.
Research conducted over the past decade has yielded a great deal of detailed information on biological responses to UVB exposure and there have been a number of prior reviews related to the effects of ozone depletion in Antarctica (Karentz, 1991, 1992; Marchant, 1997; Vernet and Smith, 1997; Weiler and Penhale, 1994; and others). However, there is still no satisfactory answer to the overriding question of "What is the effect of ozone depletion on the Antarctic ecosystem?". This paper builds on previous reviews and updates our understanding of how increased UVB radiation resulting from ozone depletion affects marine organisms in the Southern Ocean.
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OZONE DEPLETION AND INCIDENT UV IN ANTARCTICA |
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Since the late 1970s, ozone concentrations over the Antarctic and surrounding Southern Ocean have exhibited a seasonal cycle of springtime minima exceeding 50% decline from "normal" ozone levels ("normal"
300 Dobson units, DU) (Farman et al., 1985; Newman, 1994; Schoeberl et al., 1996). This annual phenomenon has been directly attributed to chlorofluorohydrocarbons (CFCs) and other atmospheric anthropogenic pollutants that have been released into the atmosphere over the past 70 yr (Anderson et al., 1991; Jones and Shanklin, 1995). Depletion of ozone over the Antarctic is caused by a combination of chemical and physical features of the springtime Antarctic atmosphere that favor ozone loss. These include 1) the presence of the polar vortex, an atmospheric circumpolar current that effectively isolates a large mass of air over the south polar region from adjacent air masses to the north; 2) extremely cold temperatures; 3) formation of polar stratospheric clouds that provide appropriate substrates for heterogeneous chemistry; and 4) after a long dark winter period, the presence of solar radiation that is required to catalyze ozone dissociation.
During the past two decades the duration of the annual ozone depletion period has increased, minimum levels over the Antarctic have steadily declined and the areal extent of the depletion within the polar vortex has expanded (Jones and Shanklin, 1995) (Fig. 1). Superimposed on these annual trends are short-term changes resulting from the rotation of the polar vortex (Fig. 2). Thus, coastal areas of the Antarctic continent and adjacent ocean waters under the margins of the vortex can be alternately exposed to high and low UVB levels within a period of several days (Fig. 3). The fluctuations in ozone concentrations and concomitant changes in incident UVB result in differences in the intensity of UVB in the water column and the depth of UVB penetration (Fig. 4). It is important to note that ozone depletion does not significantly affect UVA or higher solar wavelengths and UVA attenuation in water is lower than for UVB. Therefore, the incident and in water ratios of UVB to UVA vary with ozone levels and depth.
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With widespread compliance to Montreal Protocol standards for the reduction of CFC usage and release, there is a positive prognosis for recovery from ozone depletion (Hofmann et al., 1997
; Madronich et al., 1998; Montzka et al., 1999). It is expected that within 40–60 yr, global ozone levels will return to "normal" and springtime ozone depletion over the Antarctic will no longer occur. While this is encouraging news, the impact of the past 20 yr of ozone depletion and of the predicted 4–6 decades of continued ozone losses on the Antarctic ecosystem is still uncertain. |
UV PHOTOBIOLOGY OF ANTARCTIC ORGANISMS |
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Bacteria
While there have been a number of investigations of UV effects on freshwater Antarctic cyanobacteria (e.g., Quesada et al., 1995
; Quesada and Vincent, 1997; Roos and Vincent, 1998; Vincent and Quesada, 1994), relatively little has been reported about the impact of ozone depletion on Antarctic marine heterotrophic bacteria. Early studies show that Antarctic bacterioplankton isolates do not possess UV-screening compounds that might protect cells, but they do have capability for recovery from UV-induced damage (Karentz, 1994). A primary cellular target for UVB is DNA. DNA absorbs UVB, altering the molecular structure and potentially impairing DNA function. There are several metabolic pathways that repair DNA damage and an organism can have various combinations of these repair mechanisms. Some Antarctic bacteria have photoreactivation, an enzymatic repair process that requires UVA or higher wavelength radiation (Karentz, 1994).
Another repair pathway in bacteria is the SOS response. The timing of induction of genes involved in the SOS response is an important factor in the level of UV-tolerance within Antarctic microbial populations (Helbling et al., 1995). Initiation of the SOS response before UV exposure occurs can significantly increase bacterial cell survival. Under natural daylight conditions, the SOS response in Antarctic microbial communities exhibits a diel cycle with activation of genes maximized during the early evening to support increased removal of DNA photoproducts during the relatively darker "night" period (Jeffrey et al., 2000).
In Antarctic bacterial communities, UVA (320–400 nm) exposure can contribute to a greater proportion of UV-induced death than UVB wavelengths (Helbling et al., 1995; Marguet et al., 1994). Similar observations are reported from temperate bacteria (Sommaruga et al., 1997) and Antarctic phytoplankton (see below). UVA is not attenuated by ozone, does not cause significant DNA damage by direct absorption and can facilitate DNA repair through photoreactivation. However, both UVB and UVA are involved in a variety of photochemical reactions in seawater and in intracellular fluids that result in the production of reactive species (e.g., peroxide and hydroxyl radicals) that cause oxidative damage to organic molecules (including DNA). Although UVB wavelengths are more harmful on a per photon basis, UVA wavelengths comprise a much greater proportion of the UV radiation present in the solar spectrum; therefore, under ambient sunlight, UVA elicits a stronger biological response.
Two important aspects of the cumulative impact of UV are the intensity and the duration of exposure. For planktonic organisms, vertical mixing of the water column is a key issue in regulating these two factors. On calm days with little wind, UV-induced DNA damage in Antarctic bacterioplankton is greatest at the surface (0–10 m) and then decreases sharply with depth in the stabilized water column (Fig. 5) (Jeffrey et al., 1997). On moderately windy days, turnover of the water column promotes lower damage accumulation and more uniform damage levels with depth. It is presumed that as cells are moved more quickly out of shallow waters with higher UV irradiances, the balance of damage and repair shifts in favor of repair processes and cells experience a more expedient recovery. The issue of vertical mixing is also crucial for the evaluation of UV effects on eukaryotic planktonic organisms (see below).
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Phytoplankton
Research on UVB effects on phytoplankton has been the predominant area of study relative to the biological impact of ozone depletion in Antarctica. The focus on phytoplankton is predicated on the assumption that declines in primary productivity caused by increases in UVB stress will readily translate into ecosystem disruption by reducing trophic energy transfer. The structure of the Antarctic pelagic food web and the location and activity of various predators and consumers is dictated by seasonal changes in phytoplankton abundance and distribution (Ainley et al., 1991
; Barnes and Clarke, 1995; Clarke, 1988; Ross et al., 2000). Moreover, small single-celled organisms with short generation times (<several days) and little control over positioning in the water column would be more exposed and more vulnerable to UVB that larger multicellular organisms with protective surface layers and longer generation times (months to years).
The initial studies of UV effects on Antarctic primary production were undertaken in 1987, ten years after the Antarctic ozone depletion cycle had begun (El-Sayed and Stephens, 1992; El-Sayed et al., 1990; Stephens, 1989). This work was followed by a series of field studies that measured productivity of phytoplankton under ambient ozone depletion (Helbling et al., 1992; Holm-Hansen et al., 1993; Smith et al., 1992; Vernet et al., 1994; and others). These investigations quantified 14C incorporation in whole water samples incubated at various depths under full sunlight and with selective filters to partition the solar spectrum by removing UVB or UVB plus UVA. Biological weighting functions that describe the spectral response of phytoplankton photosynthesis have also been established for Antarctic phytoplankton under ambient and artificial UV radiation (Boucher and Prézelin, 1996a, b; Neale et al., 1994, 1998a).
In general, the quantitative results of various studies are quite similar. Full sunlight conditions that include both UVA and UVB wavelengths support lower rates of primary productivity than partitioned radiation regimes (Fig. 6). Both UVA and UVB cause inhibition of photosynthesis and in the majority of observations, UVA is responsible for a greater proportion of the decrease in carbon fixation than UVB (for the same reasons as discussed above for bacteria) (see also Boucher and Prézelin, 1996a; Davidson and Marchant, 1994). From studies with static depth incubations, the calculated impact of ozone-related changes in UVB on reducing primary productivity has been estimated at 3–15%. When vertical mixing is considered as a means of ameliorating UVB effects by reducing the duration of exposure and allowing time for recovery from UV stress, ozone-dependent reductions in primary productivity are estimated at <1–9% (Arrigo, 1994; Boucher and Prézelin, 1996b; Neale et al., 1998b).
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Observations of short-term (daily) responses and temporal adaptation to UV exposure in natural Antarctic phytoplankton communities suggest that cells respond rapidly to UV and can quickly adjust physiological parameters for greater UV tolerance (Figueroa et al., 1997
; Karentz and Spero, 1995). Species-specific differences in UV sensitivity have been documented and indicate that differential responses occur within the phytoplankton (Davidson et al., 1996; Helbling et al., 1994; Karentz et al., 1991a; Villafañe et al., 1995). The ecological implications of shifts in the taxonomic and size structure of phytoplankton communities may be a significant impact of ozone depletion and require further study and evaluation.
UV can influence a number of other physiological processes in Antarctic phytoplankton including inhibition of dimethyl sulphonium propionate (DMSP) production (Hefu and Kirst, 1997), decreasing rates of uptake of inorganic nitrogen (Döhler, 1997; Döhler et al., 1995), initiating shifts in the size of specific amino acid pools and increasing the concentration of saturated fatty acids (Goes et al., 1997). Changes in nitrogen metabolism can be accompanied by variations in pigments, with UVB causing photo-destruction of chlorophylls (Döhler, 1998a). Phytoplankton can also synthesize heat shock proteins to further ameliorate UV stress (Döhler et al., 1995).
Some Antarctic phytoplankton species contain UV-absorbing compounds, mainly the common mycosporine-like amino acids (MAAs) shinorine and porphyra-334 (Table 1) (Bidigare et al., 1996; Helbling et al., 1996; Lesser et al., 1996; Marchant et al., 1991; Riegger and Robinson, 1997). MAAs are believed to have a photoprotective function with concentrations regulated by solar exposure. However, the induction response in Antarctic phytoplankton is not consistent relative to wavelength nor does the concentration of UV-absorbing compounds always correlate with UV tolerance (Davidson et al., 1994; Helbling et al., 1996; Riegger and Robinson, 1997).
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Sea ice microalgae
During early spring the Antarctic continent is surrounded by sea ice that provides a habitat for a variety of microscopic organisms. The ice and the resident community effectively filter both UV and higher wavelengths used for photosynthesis, greatly attenuating the amount of sunlight in the water column. Low light levels result in low phytoplankton densities and low water column productivity; therefore, primary production by the ice algal community provides a significant contribution to the Antarctic food web during spring. Under a "normal" ozone column 1–5% of incident UV radiation penetrates through the sea ice. With ozone depletion there is an increase in incident UVB, but not higher wavelengths, and consequently UV transmission through the ice increases to 10% (Ryan and Beaglehole, 1994
). Under higher UV exposures, ice algal production is estimated to decrease by 5% (Ryan and Beaglehole, 1994); however, UVB may have stronger effects on standing crop (up to 40% decline) and species successional patterns that depend on the amount of snow cover and initial species composition (McMinn et al., 1999). Detailed studies of photosynthetic responses of the ice community to UVB emphasize the need for more extensive research on UV effects in the sea ice biota (Prézelin et al., 1998; Schofield et al., 1995).
Macroalgae
There are few studies relating to the UV-photobiology of Antarctic macroalgae. These organisms contain UV-absorbing MAAs with Rhodophyta having higher concentrations (400–9,000 µg MAAs g–1 dry weight) than the Phaeophyta and Chlorophyta species examined (20–200 µg MAAs g–1 dry weight) (Table 1) (Karentz et al., 1991b). This phylogenetic pattern is typical for these groups at other latitudes.
The photosynthetic pigments of Antarctic macroalgae have a rapid response to UV exposure and UVB and UVA stress elicit differential responses. Leptosomia simplex (Rhodophyta) responds to artificial UV exposure with declines in chlorophyll pigments; but increases in carotenoids, molecules that have photoprotective anti-oxidant functions (Döhler, 1998b). A comparative study of UV inhibition of photosystem II in nine species of Antarctic macroalgae shows that significant species-specific differences exist, and Chlorophyta and Phaeophyta are more tolerant of UV exposure than the Rhodophyta (Bischof et al., 1998). The authors conclude that increases in UV resulting from ozone depletion might be a factor in establishing the vertical zonation of Antarctic macrophytes.
Zooplankton
Observations in temperate freshwater communities have underscored the importance of understanding the direct effects of UV on consumer populations (Bothwell et al., 1994), but little research has been conducted on the UV-photobiology of Antarctic zooplankton. A limited amount of information is available for Euphausia superba (krill). E. superba contains all seven MAAs that have been identified from Antarctic organisms (Karentz et al., 1991b), suggesting at least a minimum capacity for UV shading of vital cellular targets.
Euphausia superba DNA has a very low (32%) guanine-cytosine base composition (Jarman et al., 1999). Since UV-induced DNA damage is predominantly comprised of adducts formed between adjacent thymine residues (e.g., cyclobutane dimers and pyrimidine-pyrimidone 6–4 photoproducts), the high adenine-thymine complement may predispose krill to higher concentrations of DNA damage than occur in other organisms. Malloy et al. (1997) have observed relatively high levels of DNA repair in E. superba under laboratory conditions; however, ambient levels of DNA damage are not known.
Examination of historical data on krill abundance, westerly wind fluctuations and ozone levels over a 20-yr period (1977–1997) provides the first connection between ozone depletion and variability in krill populations along the Antarctic Peninsula (Naganobu et al., 1999). Correlations are evident between E. superba abundance and ozone levels and the areal extent of ozone depletion. Krill recruitment is not closely correlated to ozone levels, but appears to be affected by sea level pressure (fluctuations in westerly winds). The large annual variability in the estimates of krill abundance and the two-year period required for sexual maturity contribute to the complexity of evaluating the biological impact of large scale environmental variables.
Studies from other latitudes provide evidence of higher sensitivity to UVB in early developmental stages of marine invertebrates than in adults (e.g., Damkaer et al., 1981; Giese, 1939). Similar observations have been reported for fish larvae (Hunter et al., 1981; Vetter et al., 1999). The accelerated developmental activity and minimal morphological complexity of embryos and larvae make them more vulnerable than adult animals. UV exposure during early stages of development can cause developmental delays and/or lethality that will affect recruitment to adult populations.
Many of the most common benthic macroinvertebrate species in the Antarctic reproduce with a planktonic stage during the austral spring when the greatest deterioration of ozone occurs (Bosch et al., 1987; Pearse et al., 1991). These include the sea star Odontaster validus, the sea urchin Sterechinus neumayeri and the ribbon worm Parborlasia corrugatus; all of which produce eggs <0.2 mm diameter and have planktotrophic larval development (Bosch et al., 1987; Pearse et al., 1991; Stanwell-Smith and Peck, 1998). Embryos and larvae of some of these species (e.g., Sterechinus) contain MAAs. MAAs provide a protective sun screening function for urchin embryos in temperate species (Adams and Shick, 1996) and similar observations have been made for Sterechinus neumayeri (DK/IB, unpublished data). However, MAA concentrations are not sufficient to prevent excessive damage to embryos that inhabit shallow surface waters (<5–10 m) (Fig. 7).
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The early development of the Antarctic sea urchin Sterechinus neumayeri has proved to be a reliable model for the study of UV effects on early invertebrate development. In situ measurements of DNA damage, abnormality in development and lethality show that incident UVB is detrimental to development without ozone depletion, and that increased exposure under ozone-depleted conditions exacerbates responses (Fig. 7). UV effects on embryos are generally not observed at incubation depths below 5 m, suggesting that only individuals drifting very near the surface for prolonged periods of time would be adversely affected by UV exposure. Embryos and larvae of Sterechinus and other benthic invertebrates have been found in surface waters (Bosch et al., 1987
; Stanwell-Smith et al., 1999); however, because residence times and mixing rates are not known, it is not possible to assess the vulnerability of these species to ozone-related changes in UV.
The effects of ultraviolet light on the embryos and larvae of the sea star Psilaster charcoti have also been studied. This species represents a second major type of invertebrate developmental strategy with the production of large (0.7 mm diameter) yolk-laden eggs and free-swimming non-feeding larvae (Pearse et al., 1991). Although MAAs are lacking in P. charcoti, the relatively large size and high amounts of carotenoids in eggs and embryos might be expected to provide effective protection against UVB exposure. However, when zygotes and early cleavage embryos are incubated in situ, both UVB and UVA cause considerable damage to embryonic development under "normal" and depleted ozone columns (Fig. 8). The degree of damage and the maximum depth of the UVB effect are comparable to those observed in S. neumayeri; but the implications of these results are quite different. Eggs released by P. charcoti float upwards at rates of 1.5–2.0 m/hr in situ, a velocity that would allow them to move from depths occupied by adults to depths at which they are vulnerable to UV damage in less than 1 day or before the third embryonic cleavage is completed.
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Several other groups of Antarctic organisms have floating eggs that could potentially be exposed to maximum UV fluences during the most crucial stages of early development (Bosch, 1989
; Malloy et al., 1997; Pearse et al., 1991). DNA damage and repair have been examined in Antarctic icthyoplankton (eggs and larvae), including the floating eggs of Chaenocephalus aceratus (icefish) (Malloy et al., 1997). DNA damage levels in icefish eggs collected from surface waters were significantly correlated to total daily incident UVB irradiance and DNA repair rates were correspondingly high. Here again, limited data preclude any substantial evaluation of UV effects on these organisms.
Benthic invertebrates
Coastal areas of the Antarctic have an abundant and diverse benthic faunal component. During spring, sea ice effectively scours most inter- and subtidal areas leaving behind very few organisms with the notable exception of the limpet Nacella concinna. During springtime ozone depletion, the majority of benthic organisms resides in relatively deep water and is well protected from UV exposure by both the sea ice and the overlying water column. Research on UV defenses of these organisms indicates that the majority (
90%) contain UV-absorbing MAAs (Table 1) (Karentz et al., 1991b; McClintock and Karentz, 1997). As found at other latitudes, there is a distinct partitioning of MAAs in different tissues with highest concentrations localized in ovaries and eggs (Karentz, 1994; Karentz et al., 1997). Digestive tissues can also contain appreciable amounts of MAAs, but body walls have low concentrations and sperm have little or non-detectable amounts of MAAs. It is generally accepted that MAAs are bioaccumulated.
MAA concentrations in benthic Antarctic species do not appear to be correlated to ambient UV levels relative to seasonal changes in day length or ozone levels (Karentz et al., 1997). However, along the Antarctic Peninsula there is a consistent vertical gradient of MAA concentration from the intertidal to depths of 30 m. In contrast, there is generally a lower level of MAAs in benthic organisms collected in McMurdo Sound where depths of habitation are deeper and food supply is more likely to be of detrital origin rather than live algal material (McClintock and Karentz, 1997). Other aspects of the UV-photobiology of Antarctic benthic invertebrates have not yet been investigated.
Vertebrates
Aside from a few studies that included fish (mostly larval stages) (Karentz et al., 1991b; Malloy et al., 1997; McClintock and Karentz, 1997), no direct investigations of ozone depletion effects on higher animals have been undertaken. Fish, birds, seals and whales are physically well protected from UV-induced damage by scales, feathers, fur and thick skin layers. The only study relating to the UV-photobiology of Antarctic organisms prior to the inception of ozone depletion examined sensitivity of UV-induced corneal damage in the eyes of Antarctic birds as compared to birds from temperate latitudes (Hemmingsen and Douglas, 1970). Polar birds have higher UV thresholds for damage attributed to their existing adaptation to the higher albedo of snow and ice that creates a high UV environment.
If there is an impact of ozone depletion on larger marine organisms, it is expected to occur through potential limitation of food sources. Evaluation of the UV effects on birds and mammals is confounded by the fact that there are many environmental variables that can be implicated in regulating the size and fitness of a population. The multi-year life histories of these organisms also make it especially difficult to establish cause and effect; therefore, the impact of a single environmental variable is not readily apparent. Consideration of the synergist effects of environmental factors is necessary and this requires careful and consistent long term monitoring on a time scale of decades (e.g., Trivelpiece and Fraser, 1996).
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When the existence of Antarctic ozone depletion was finally accepted, dire predictions were made about the fate of the Antarctic ecosystem (Buckley and Trodahl, 1990
; El-Sayed et al., 1990). Based on the extremely limited information available at the time, these were reasonable assumptions. Today, with the benefit of a larger database on population and community responses to UV, the effect of ozone depletion in the Antarctic does not seem quite so drastic; yet much more complex (Arrigo, 1994; Holm-Hansen et al., 1997; Vernet and Smith, 1997 and others). The focus on phytoplankton has clearly established that primary productivity declines by just a few percent under ozone depletion and that this amount of loss is perhaps insignificant relative to the magnitude of seasonal and annual variability that occurs in the Southern Ocean (Smith et al., 1992). However, this does not imply that ozone depletion may not be a substantial stress to the Antarctic ecosystem.
One of the major conclusions of the 1998 UNEP Assessment of Environmental Effects of Ozone Depletion emphasizes that UV effects on the complex interactions within an ecosystem cannot be reduced to monitoring primary productivity (Häder et al., 1998). Modification of the structure of communities is a more likely response and one that has far-reaching implications. These kinds of changes are also much more difficult to quantify and evaluate, and this presents a great challenge.
Antarctica is the only place on Earth where such large predictable ozone losses occur, and as such it provides a unique location for ozone-related research. Results of studies conducted in the Antarctic have provided invaluable information on the UV-photobiology of organisms and processes that have counterparts at other latitudes. While these data have helped to reduce some of the uncertainty about the risks of ozone depletion, they have also emphasized the importance of more detailed understanding of UV effects in aquatic systems and have stimulated many new avenues of research.
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ACKNOWLEDGMENTS |
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We thank the symposium organizers, J. B. McClintock, B. J. Baker and C. D. Amsler; and O. Holm-Hansen and an anonymous reviewer for helpful comments on this manuscript. This work was supported by NSF Office of Polar Programs grants #9528241 to DK and #9528089 to IB.
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FOOTNOTES |
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1 From the Symposium Antarctic Marine Biology presented at the Annual Meeting of the Society for Comparative and Integrative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: karentzd{at}usfca.edu
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