The ultraviolet history of the terrestrial planets — implications for biological evolution

Planetary and Space Science 48 (2000) 203±214

The ultraviolet history of the terrestrial planets Ð implications for biological evolution Charles S. Cockell*,1 M/S 239-20, NASA Ames Research Center, Mo€ett Field, CA 94035-1000, USA Received 24 June 1999; accepted 27 August 1999

Abstract A radiative transfer model is employed to investigate the comparative surface ultraviolet (UV) radiation histories of Earth, Mars and Venus from 4.5 Ga to the present and thus their comparative theoretical photobiological histories. Earth probably began with a period of higher ultraviolet radiation ¯uxes during the anoxic Archean. During the early Proterozoic UV ¯uxes declined as oxygen partial pressures and thus ozone column abundance rose, but the ozone column became subject to stochastic depletion events caused principally by impact events and possibly large-scale volcanism and less frequently, close cosmic events such as supernovae. In contrast Mars has been subject to a history dominated by a slow increase in solar luminosity and a reduction in partial pressures of CO2, both of which have resulted in an increase in UV ¯ux. The UV radiation history of Venus has been dominated by the greenhouse e€ect through which high partial pressures of CO2 made the surface UV radiation environment clement. These distinct histories in¯uence the potential comparative evolutionary photobiology of the three planets. On Earth, life transitioned from the Archean, when tolerance to UV radiation, particularly for exposed organisms, must have been high to a more photobiologically clement era. In this latter era the predominant evolutionary selection pressure is one that allows for tolerance of sudden and unpredictable increases in UVB radiation above seasonal and diurnal maxima caused by exogenous perturbation of the ozone column. In the case of Mars, the UV radiation ¯ux has increased over time. Today the biologically e€ective irradiances to DNA are not considerably di€erent from those that are calculated for Archean Earth. If the planet su€ered an atmospheric collapse then it may have been subject to an ultraviolet crisis at some point in its past when DNA-weighted irradiance would have increased three to ®ve-fold. Venus transitioned into a photobiologically clement era soon after late bombardment. The lifeless surfaces of Mars and Venus, when in the former case DNA-weighted irradiances are not much greater than Archean Earth and in the latter case, insigni®cant, are testament to the unimportance of UV radiation as an evolutionary selection pressure when other physical factors, particularly lack of liquid water, become limiting to life. Understanding the comparative evolutionary di€erences in surface UV ¯ux of the terrestrial planets can help us understand the in¯uence, and lack of in¯uence, of UV radiation in determining their suitability as abodes for life at di€erent stages in their past. # 2000 Elsevier Science Ltd. All rights reserved.

1. Introduction Ultraviolet (UV) radiation has been a ubiquitous factor in the course of terrestrial biological evolution since the early Archean. Its e€ects on organisms, * Tel.: +1-650-604-5499; fax: +1-650-604-10881 E-mail address: [email protected] (C.S. Cockell). 1 Current address: British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, UK. 0032-0633/00/$20.00 # 2000 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 2 - 0 6 3 3 ( 9 9 ) 0 0 0 8 7 - 2

which are principally detrimental, have been demonstrated with some of the most essential components of the biochemical machinery, particularly DNA (e.g. Harm, 1980; Karentz et al., 1991) and photosystems (e.g. Cockell and Rothschild, 1999; Haeder and Worrest, 1991; Vincent and Roy, 1993). The most damaging wavelengths are the short-wavelength UVC (200± 280 nm) and UVB (280±315 nm) regions. Although UVB wavelengths are the most important on the surface of present-day Earth because of the atmospheric absorption and scattering of UVC radi-

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ation, extraterrestrial UVC radiation has been directly demonstrated to be detrimental to micro-organisms (Horneck, 1993) with implications for terrestrial evolutionary photobiology during the Archean (Rettberg et al., 1998). UVA radiation (315±400 nm) is less damaging, although it can mediate photoxidative damage through reactive oxygen species (Jagger, 1985). As well as deleterious e€ects at the organismal level, UV radiation may also alter inter-species competitiveness and thus ecosystem balance (e.g. Bothwell et al., 1994; Fox and Caldwell, 1978). Thus, understanding how the UV radiation environment of Earth has altered over geologic time periods is essential for understanding the evolutionary history of the Earth and the degree to which UV has contributed as a selection pressure. Ultraviolet histories for Mars and Venus have not been presented previously. However, we do know that Venus and Mars have been subject to quite di€erent atmospheric histories compared to the Earth (Haberle et al., 1994; Kasting et al., 1984; McKay and Davis, 1991). Thus, they provide an opportunity to examine comparative ultraviolet histories and the potential contribution of UV radiation to the biological fate of the planets. Mars is of particular interest since as well as o€ering the greatest hope for the discovery of extraterrestrial life, extinct or extant, the atmospheric and surface conditions of early Mars have been examined in detail, practically and theoretically (e.g. Carr, 1987; Haberle et al., 1994; McKay and Davis, 1991), and so there is a chance of using this data to unravel the ultraviolet history of the planet. In this paper, comparative histories of UV radiation ¯ux on the surface of Earth, Mars and Venus are derived. From this vantage point conclusions are drawn concerning the relative importance of UV radiation as a potential physical evolutionary selection pressure on the three terrestrial planets at di€erent stages in their past. 2. Model for the change in the terrestrial UV ¯ux over time Prior to the generation of oxygen through oxygenic photosynthesis (Collerson and Kamber, 1999; Walker et al., 1983) and geologic processes (DesMarais et al., 1992), the Archean atmosphere was probably anoxic and as a consequence, lacking an e€ective ozone shield. As a result the surface of the Earth was probably exposed to much higher doses of UVC and UVB radiation (Sagan, 1973). Two principal factors would have determined surface UV ¯ux in the anoxic era. First, the solar luminosity. It is estimated that the Sun was 25±30% less luminous during the Archean

era (Gough, 1981; Newman and Rood, 1977). The change in luminosity is accounted for both by changes in radius and temperature. Although the early T-Tauri sun may have emitted more short-wavelength UV radiation than the present-day sun, these wavelengths are generally con®ned to wavelengths <200 nm (Canuto et al., 1982, 1983; Zahnle and Walker, 1982) that do not penetrate a CO2 rich atmosphere, although these emissions were probably important for the photochemistry of the paleoatmosphere (Canuto et al., 1982, 1983; Zahnle and Walker, 1982). In the model presented here, solar luminosity was taken as 75% at 3.5 Ga. Using observations of stars, Zahnle and Walker provide spectra for the sun at 3.5 Ga and present-day. The 25% reduction in luminosity corresponds to an approximately 35% reduction in the biologically important UV range (Zahnle and Walker, 1982). Solar luminosity was assumed to increase linearly over time to present-day values. Second, changes in CO2 partial pressures would have a€ected surface UV ¯uxes. As CO2 partial pressures dropped, so UV penetration increased. A number of models and data sets have been presented for Archean CO2 partial pressures. Between 2.7 and 2.2 Ga, the partial pressure may have been 40 mb based on Precambrian soil weathering data (Rye et al., 1995). However, partial pressures of CO2 in the very early Archean may have been higher and values ranging from 10 bar as the upper limit (Walker, 1986) to a minimum of 0.2 bar to prevent the surface of Archean Earth from freezing (Kasting, 1987) have been proposed. In this model a value of 1 bar was used for a time period 03.5 Ga and a linear decrease to late Archean values (040 mb) was assumed. In all cases the present-day value of pN2 (0.8 bar) was assumed. To calculate the surface UV ¯ux, the solar luminosity and partial pressures of CO2 from 4.5 to 2 Ga for each 100 Myr time period were input into a standard radiative transfer model. The direct term and the diffuse term was calculated using a Delta±Eddington approximation to determine the total UV ¯ux at the surface of the Earth for the three UV wavelength ranges (UVC, 200±280 nm; UVB, 280±315 nm; UVA, 315±400 nm). The radiative transfer model is similar to that described previously (Cockell et al., 2000; Haberle et al. 1993) and is based on a 2-stream model described by Joseph et al. (1976). Irradiance values were calculated with a resolution of 2 nm. The UV spectrum used was that presented by Nicolet (1989) and scaled according to changes in solar luminosity. Here UV ¯ux for Earth, Mars and Venus is calculated for a zenith angle of 08 and cloudless skies. Furthermore, the possible existence of UV screens in the atmosphere such as sulfur (Kasting et al., 1989) or a CH4-generated hydrocarbon smog proposed for early

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Earth (Sagan and Chyba, 1997) are ignored. Thus, the data presented here considers the worse case instantaneous exposure. From a biological survival point of view, this is the most useful calculation since it provides an indication of the upper bounds of biological e€ects. E€ects of day length and obliquity are discussed later. The biologically e€ective irradiance of UV radiation is also a useful term which provides a more meaningful interpretation of the photobiological consequences of changing UV ¯uxes (Cullen et al., 1992). Here a DNA action spectrum, which relates the biological damage to DNA to wavelength was multiplied by the incident radiation and integrated across the UV range to provide a total DNA-weighted biologically e€ective irradiance. The approach used has been described previously (Cockell, 1998; Cockell et al., 2000; Garcia-Pichel, 1998; Rettberg et al., 1998). This value is also calculated as a function of time. Approximately 2.5 Ga oxygen partial pressures began to rise, either directly after the advent of oxygenic photosynthesis or because oxygen already being produced was no longer removed by reducing compounds in the Archean oceans and atmosphere. The rise of O2 partial pressures resulted in the formation of an ozone column abundance sucient to signi®cantly attenuate UVC and UVB wavelengths. At a pO2 of about 10ÿ3 PAL (Present Atmospheric Levels) UVC ¯uxes on the surface of the Earth began to be reduced. At about 0.1 PAL, the ozone shield would have screened UV radiation to an extent similar to today (Kasting 1987). However, DNA-weighted irradiances drop steeply at 10ÿ2 PAL because at this value the wavelengths that are not screened by ozone (200± 220 nm) are quite e€ectively scattered by the atmosphere and biologically damaging wavelengths below 280 are screened. This corresponds to a time 01.5 Ga. Here it is assumed that the ozone shield began to be formed at approximately 2 Ga and had reduced biologically e€ective irradiances to well within an order of magnitude of present-day values by about 1.5 Ga and down to present-day levels by 1 Ga. UV ¯ux at 2, 1.5 and 1 Ga was calculated. The conventional view of the photobiology of Earth has focused on an early period of high UV during the Archean, a rise in ozone column abundance during the early Proterozoic and then the relatively clement UV radiation environment of the Proterozoic and Phanerozoic Earth. However, a number of natural events can cause ozone depletion, including impact events (Toon et al., 1997; Turco et al., 1982) and close cosmic events such as supernovae and neutron star mergers (Aikin et al., 1980; Crutzen and Bruhl, 1996; Ellis and Schramm, 1995; Ruderman, 1974; Thorsett, 1995). Because these events all share the common e€ect of ozone depletion, it is likely that they all share a common evolutionary

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Fig. 1. Photobiological history of Earth. Changes in UVA, B and C radiation from 4.5 Ga to the present. In the case of the Proterozoic and Phanerozoic Earth the increases in UVB radiation and DNAweighted e€ective irradiances associated with a Tunguska-sized impact event and a supernova explosion at a distance of 10 pc (dotted lines) as well as a worse case 85% depletion event for a large impact event are used to illustrate the levels to which stochastic increases in photobiological stress may have occurred as a result of exogenous agents. See text for references.

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signi®cance in subjecting the Earth's biota to stochastic increases in UVB radiation with the subsequent photobiological and ecological consequences (Cockell, 1999a). Because these events will rarely, if ever, cause 100% ozone depletion, DNA-weighted irradiances will not reach Archean levels and surface levels of UVC radiation, even under severe ozone depletion (up to 085%) remain biologically insigni®cant (Fig. 1). Because models that accurately quantify ozone depletion versus energetic scaling for di€erent natural ozone depleting events are not available, proposing a quantitatively accurate ozone depletion versus time frequency graph for the Proterozoic and Phanerozoic biosphere is dicult (Cockell, 1999a). Nevertheless, we do have insights into the relative temporal importance of these di€erent events. Close cosmic events are less common than impact events. For example, a close supernova explosion at a distance of 10 parsecs (32.6 light years) might cause 20% ozone depletion at the equator and 60% depletion at the poles (Crutzen and Bruhl, 1996), but with a frequency of once every 100±500 million years (Ellis and Schramm, 1995). Impact events may, however, achieve these depletions at much greater frequency. The Tunguska meteor explosion in Siberia in 1908 is estimated to have caused 45% ozone depletion over the northern hemisphere and possibly 85% depletion if the NO generated by the impact event was localized to a latitudinal zone between 55 and 658N (Turco et al., 1982). Since events on this scale might occur once every 1000 years (Toon et al., 1997), it is likely that ozone depletion events during the Proterozoic and Phanerozoic have been dominated by impact events interspersed by some cosmic events. Impact events larger than Tunguska will cause greater ozone depletion (Toon et al., 1997). However, because they inject greater quantities of dust and possible smoke from wild®res into the stratosphere, the initial e€ects of ozone depletion may be partly mitigated. E€ects of these events on surface UV ¯ux and DNA weighted irradiance are shown in Fig. 1. Large-scale volcanism might also potentially cause ozone depletion if chlorine is injected into the stratosphere. However, the photochemistry of such events is not clear since the concentrations of ozone-depleting chlorine that would be injected into the atmosphere from magma are not well constrained (Johnston, 1980). If large-scale volcanism does cause ozone depletion, then given the rather high frequency of continental scale volcanism over geologic time Ð there are estimated to have been at least nine major basaltic ¯ood events over the last 250 million years (Rampino et al., 1988) Ð volcanism may also be a signi®cant contributor. The model proposed for the change in UV ¯ux over time is similar to that proposed by Garcia-Pichel

(1998), who calculated a relative increase in UVA, B and C using solar luminosity calculations. There are some di€erences. Here the change in solar luminosity was assumed to be 035% based on Zahnle and Walker (1982) in the early Archean, and not to be entirely due to black-body changes. A radiative transfer model is used to quantify UV ¯ux in W/m2 rather than as a relative change in intensity. Finally, the importance of stochastic increases in UVB ¯ux caused by ozone depletion events during the Proterozoic and Phanerozoic are emphasized. Otherwise the two models are in broad agreement with regards to the amelioration in UVB and C ¯ux at the Archean-Proterozoic transition and the gradual increase in UVA ¯ux resulting from the increase in solar luminosity. 3. Evolutionary photobiology of earth That the high UV ¯uxes of early Earth posed a challenge to life in exposed habitats has been postulated for a considerable period of time (e.g. Margulis et al., 1976; Pierson et al., 1993; Sagan, 1973) and recently (Cockell, 1998; Garcia-Pichel, 1998; Rettberg et al., 1998). Biologically e€ective irradiances to DNA in exposed regions may have been between two and three orders of magnitude higher than present-day Earth (Cockell, 1998; Garcia-Pichel, 1998; Rettberg et al., 1998). The length of time for which these conditions persisted depends upon models for the increase in pO2 resulting from geological and biological factors. The higher UV ¯uxes on Archean Earth would have made e€ective protection and repair processes mandatory responses in exposed habitats. A wide diversity of physical substrates would have allowed life to have persisted in benthic habitats and probably on early Archean cratons. They include iron compounds, rocks and sediments (Cockell, 1998; Garcia-Pichel, 1998; Olson and Pierson, 1986) and maybe even compounds such as sulfur in hydrothermal areas (Cockell, 1998). Later, the intense selection pressure to increase exposure to photosynthetic light, but reduce UV radiation exposure would have led to new innovations in UV screening compounds (Cockell, 1998). Until UV screening compounds had evolved, life would have been limited to regions in which the appropriate physical substrates were available. Even when UV-screening compounds had evolved, it is likely that UV protection strategies such as the matting habitat (Margulis et al., 1976; Pierson et al., 1993) would still have been important for colonization of exposed regions. Using a UV radiative transfer model of the archean oceans, survival of micro-organisms in the photic zone of the Archean oceans can be demonstrated (Cockell, 1999b). At a depth of 030 m DNA-weighted irra-

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diances may have been similar to exposed surfaces on Earth today. During the early Archean dissolved ferrous iron from hydrothermal upwelling would probably have made the surface layers quite photobiologically clement since ferrous iron has a high absorbance in the short wavelength UV range (GarciaPichel, 1998; Olson and Pierson, 1986). After the advent of oxygenic photosynthesis, iron would have been stripped from the ocean surface layers of the Archean oceans (Drever, 1974), just as evidence from Archean sedimentary units suggests it was in shallowwaters (e.g. Lowe, 1994). This would have increased UV penetration. It is likely that the biota in the mixed layer under such conditions was a low diversity, high UV resistant one. But it could have been numerically abundant and thus it is plausible that the surface layers of some Archean water bodies were oligotrophic as they are today. At a depth of greater than 30 m DNA-weighted irradiances and phytoplankton inhibition would have been less than the surface of the present-day Earth, providing a clement deep water environment for life (Cockell, 1999b). The increase in non-stromatolitic micro-fossil abundance in the early Proterozoic (Schopf and Walter, 1983) may be more to do with the increased productivity of upwellings from newly emerged continental blocks or poor preservation of photic zone organisms than a critical photobiological constraint in Earth's Archean oceans. The rise of partial pressures of atmospheric oxygen and thus the rise in ozone column abundance undoubtedly alleviated much of the UV stress (Francois and Gerard, 1988, Garcia-Pichel, 1998) and reduced the requirements for protection and repair that many organisms had (Garcia-Pichel, 1998). Biologically e€ective irradiances generally begin to drop at column abundances above 01  1017 cmÿ2 (Cockell, 1999b). If the delay in the rise of atmospheric oxygen was caused not by a delay in the advent of oxygenic photosynthesis, but by the requirement to deplete ferrous iron and reduced volcanic gases as a sink for oxygen (e.g. Margulis et al., 1976; Veizer et al., 1982), or by a low photosynthetic productivity in the Archean (Knoll, 1979) then it is plausible that UVA-induced photoxidative stress in the micro-environments of oxygenic photosynthetic organisms was already important in the early Archean as well as the UVC and UVB stress (Garcia-Pichel, 1998). The time, however, when oxygenic photosynthesis ®rst arose is still uncertain (Pierson, 1994). Although the period during which oxygenic photosynthesis existed but no ozone shield had formed may have represented a period of great photobiological stress (Garcia-Pichel, 1998), the presence of photoquenching carotenoids in archaea (e.g. Emerson et al., 1994) might suggest that the ability to deal with this UVA-induced stress could have existed before the

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advent of oxygenic photosynthesis, albeit as a result of other early functions of carotenoids. Furthermore, superoxide dismutase may well have evolved in the deepest branches of the phylogenetic tree (Asada et al., 1980), either as a result of localized oxygen production or photochemical production of oxygen radicals in the ocean surface layer, providing organisms with some intrinsic defence against photoxidative stress when oxygenic photosynthesis became more prevalent. After the increase in ozone column abundance, the photic zone of the oceans might have been colonized by a more diverse biota and the land masses would have presented a more photobiologically clement environment for life. It has been suggested that the colonization of the land masses actually required an ameliorated UV radiation environment (Berkner and Marshall, 1965), although for physiological reasons others doubt the importance of the ozone shield and UV radiation as a critical environmental factor for the colonization of land, and even for ancestral plants (Cockell and Knowland, 1999). In one sense, the Archean UV radiation environment was a disadvantage because of the restrictions it might have imposed upon life, but from a photobiological protection point of view, at least it was a constant selection pressure. Furthermore, it is plausible that higher UV ¯uxes can be a motor for generating mutations, thus accelerating the tempo of evolution, which would be dependent on DNA base pair composition (Lesk, 1973). The longer phylogenetic branch length of some phytoplankton taxa has been speculated to be caused by the in¯uence of UV radiation in the photic zone (Pawlowski et al., 1997). However, this concept has not been quantitatively and convincingly demonstrated for the Archean. With the absence of information on the eciency of repair processes in Archean organisms or a substantial Archean fossil record, it may never be possible to convincingly demonstrate that elevated UV radiation compared to today resulted in the potential for elevated evolutionary tempo. After the formation of the ozone column, many more habitats might have been colonized by less UV tolerant taxa, but damage caused by random ozone depletion events would have been unpredictable. For a Tunguska-sized impact event the ozone depletion event may last for about three years (Turco et al., 1982). Although supernovae events have been predicted to cause ozone depletions that might last for many decades or even centuries as a supernova remnant shell sweeps through the solar system (Ellis and Schramm, 1995; Ruderman, 1974), these time scales are still small in the geologic context. In the case of events that occur over a few years, the e€ects might be a random kill or competitive decline of species that are not adapted for high UV radiation well beyond seasonal

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and diurnal maxima. In the case of events that last for decades or longer, changes in ecosystem balance and inter-species competitiveness under the new UV regime may have time to occur. The e€ect might be to contribute towards a subtle biostratigraphic turn-over, particularly if other alterations in the physical environment accompany the change, such as for impact events. In either case, the e€ects are subtle ecosystem alterations and are unlikely to be mass extinctions. None of the major mass extinctions of the Phanerozoic show unequivocal signs of a UV crisis (Cockell, 1999a), although delineating a UV e€ect from other changes is dicult.

Because of the direct coupling between the martian polar caps and the atmospheric CO2 reservoir, the time to reach equilibrium may have been only 0200 years (Leighton and Murray, 1966, Haberle, personal communication). If such a scenario did occur it would have signi®cant consequences for the surface UV ¯ux as discussed in the next section. Since all of the Haberle et al. models give quite

4. Model of the change in Martian UV ¯ux over time Mars does not have a signi®cant ozone shield, although some ozone build-up occurs over the poles in spring and winter (Barth et al., 1973; Barth and Dick, 1974; Lindner, 1991). These levels, although about two orders of magnitude lower than typical terrestrial column abundances, can reduce UVC ¯ux reaching the ground (Cockell et al., 2000; Kuhn and Atreya, 1979). The photobiological history of the planet has almost been exclusively determined by the change in solar luminosity and the atmospheric carbon dioxide reservoir. The postulated changes in solar luminosity as well as the proposed changes in atmospheric CO2 pressures over time can be used to investigate the parameter space of UV ¯ux that may have reached the martian surface over time. Haberle et al. (1994) carried out a detailed modeling study of the evolution of CO2 on Mars. They investigated varying initial CO2 inventories as well as alterations in solar luminosity and the greenhouse e€ect. They ultimately conclude that none of the outcomes is entirely satisfactory. Large initial CO2 inventories tend to predict polar caps that are too large, smaller inventories require low partial pressures of CO2 on early Mars, which may be inconsistent with a warmer, more water rich past (Carr, 1987). In view of the warmer conditions that are proposed for early Mars, Haberle et al. propose a scenario where the initial CO2 inventory may have been between 0.5 and 3 bar. Towards the end of late bombardment at approximately 3.8 Ga, the CO2 inventory may have been 0.5±1 bar. How the CO2 atmospheric reservoir then evolved to current conditions is unknown. Either the CO2 was slowly lost to carbonates through weathering, or the atmosphere may have collapsed. In the latter scenario the build-up of the polar ice caps results in reduced temperatures and a freeze out of more carbon dioxide. A positive feedback process is initiated which leads to a rapid collapse of the atmospheric CO2 reservoir (Haberle et al., 1994).

Fig. 2. Photobiological history of Mars. Changes in UVA, B and C radiation from 4.5 Ga to the present. In the graph of DNA-weighted irradiance the e€ect of an atmospheric collapse is illustrated. An atmospheric collapse causes an ultraviolet crisis (a rapid and permanent increase in DNA-weighted irradiance on a short geologic timescale). Also illustrated is the e€ect of an episodic ¯ood induced CO2 injection into the martian atmosphere as described by Gulick et al. (1997).

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di€erent histories of CO2 change, placing accurate constraints on the change in CO2 is problematic. However, radiative transfer calculations illustrate that the possible parameter space of the initial CO2 pressure may have been less critical to the UV ¯ux on early Mars relative to later stages of atmospheric evolution. For partial pressures that range between 1 bar of CO2 and 3 bar, the UV ¯ux alters by three-fold. More critical alterations occur when lower partial pressures are considered. Proportionally less scattering occurs and more UV reaches the ground for each decrement of CO2 partial pressure. Thus, at the present day atmospheric pressure of 06 mb, the UV ¯ux is ®ve fold more than early Mars with an atmospheric CO2 inventory of 1 bar. In Fig. 2, the ultraviolet history of Mars has been presented for an initial inventory of 2 bar declining to 1 bar in the time corresponding to the early terrestrial Archean (Noachian) with an arbitrary gradual decline to present-day conditions. The rate of decline of CO2 varies with the models used (Haberle et al., 1994; McKay and Davis, 1991). Although improved models may increase the accuracy of the rate of change in UV ¯ux, the qualitative evolutionary conclusions are not critically altered by the assumptions. 5. Theoretical photobiological consequences for Mars Unlike the Earth, whose ultraviolet history during the Proterozoic and Phanerozic has been dominated by an ozone column, Mars has a more simple history and one which has been closely coupled with the changes in atmospheric CO2 inventory. From a biological perspective, the UV ¯ux on Mars has probably presented a steadily increasing challenge to life, regardless of the CO2 evolutionary model that we choose. The rising UV ¯ux over time, although presenting an increasing photobiological challenge, does not represent a critical constraint to life. The present-day DNA-weighted irradiance on the surface of Mars is similar to the weighted irradiance on the surface of Archean Earth, the biological signi®cance of which has been discussed previously (Cockell, 1998). The importance of the photobiological deterioration of Mars is that it could exacerbate the demise of life in synergy with the deterioration in other physical factors (Cockell, 1998). Low temperature extremes and the possible existence of peroxides in the martian soil are two environmental stressors detrimental to life, but the lack of liquid water on the surface is undoubtedly the worst (McKay and Davis, 1991). The drop in temperature of the planet as well as the reduction in CO2 would have reduced habitats in which water was available. A desiccation-UV stress problem became increasingly important on Mars (Cockell et al., 2000). The time over

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which this occurred is dicult to assess, but if the Haberle models are accurate in suggesting a gradual decline in pCO2 over time, then the increase in UV stress has been a continuing problem for Mars from 4.5 Ga until present atmospheric pressures were reached. The availability of liquid water on the surface probably started to become a serious biological problem shortly after 03.8 Ga, when it is presumed that few new valley networks were formed (Carr and Clow, 1981). However, liquid water may have persisted for some 700 million years after this date in ice-covered lakes (McKay and Davis, 1991) which would provide an ecological refugia for any potential surface biota and potentially some UV protection as well. Some hydrothermal regions which may have existed well after late bombardment (e.g. Gulick and Baker, 1989) could theoretically provide an extinction refugia for surface life. This gradualist view of the ultraviolet history of Mars may have been di€erent if the planet did su€er an atmospheric collapse at some point in its history between 4.5 and 3 Ga (Haberle et al., 1994). A planetary atmospheric collapse has the potential to trigger an ultraviolet crisis. A reduction of the martian atmospheric CO2 reservoir from 01 bar to 06 mb would increase DNA-weighted biologically e€ective irradiances by ®ve-fold. A reduction from 0.5 bar to 06 mb would cause a three-fold increase. What would be the e€ect on a theoretical biota? Although these relative percentage increases in DNA-weighted irradiance may occur on present-day Earth for an ozone depletion of 050%, the absolute UV ¯ux is much higher on Mars than Earth. The increase in damage on Earth caused by ozone depletion can be dealt with in some organisms by the induction of UV-screening compounds or repair processes (see Tevini, 1993 and discussions therein). On Mars, if the limits of UV-screening compounds were already employed (for example 99% screening in the subsurface photosynthetic layers of a microbial mat) under a biologically e€ective irradiance some three orders of magnitude higher than on present-day Earth, a substantial amount of the e€ect of the increased UV ¯ux would have to be dealt with by repair processes. A ®ve-fold increase in DNA-weighted irradiance over just two hundred years might be expected to present a substantial selection pressure. Other communities a€ected by such UV radiation changes would be single-celled organisms in the water column. Isolated single-celled organisms cannot make use of the matting habit and in the absence of substantial UV absorption in the water column, can be profoundly a€ected by UV radiation (e.g. Milot-Roy and Vincent, 1994). However, organisms in ice-covered lakes might be protected by the ice covering, which can confer substantial protection against incident UV

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radiation (e.g. Vincent et al., 1998). In the worst case an ultraviolet crisis theoretically might present itself in a paleobiological record as a boundary in the taxonomic diversity and geographic extent of life that is independent of any particular change associated with water availability. Communities una€ected by such a change would be deep-subsurface chemosynthetic communities (Boston et al., 1992) where exposure to UV radiation was irrelevant. Organisms living in substrates such as lithic communities associated with rock, where even a small movement into the rock may reduce light levels by an order of magnitude (Nienow et al., 1988), might also be robust against the photobiological consequences of atmospheric collapse. Organisms with well evolved repair processes would also be robust. For example, the extremely UV tolerant Deinococcus radiodurans, is presumed to have acquired its UV resistance as a result of desiccation selection pressure (Mattimore and Battista, 1996). This is signi®cant since desiccation and increases in UV radiation went hand-in-hand during the atmospheric evolution of Mars. Its repair capabilities exceed the instantaneous DNA-weighted irradiance on present-day Earth at a zenith angle of 08 by approximately three orders of magnitude (Cockell, 1999b) and thus possibly by three-fold the DNAweighted irradiance on early Mars with an atmospheric CO2 inventory of 02 bar. This organism would survive the increase in instantaneous DNA-weighted irradiance associated with the atmospheric collapse considered here. Therefore, for some organisms a planetary ultraviolet crisis brought on by atmospheric collapse need not necessarily precipitate a true biotic crisis. Finally, it should be noted that Mars may also have experienced periods of reduced UV radiation even since 3.5 Ga. Gulick et al. (1997) suggest that episodic CO2 releases of up to 2 bar resulting from catastrophic ¯oods may have resulted in transient hydrothermalism during the last 3.5 Ga. Such episodes would have resulted in an ultraviolet amelioration as illustrated in Fig. 2. The possibility of UV amelioration events concomitant with episodes of surface water availability since 3.5 Ga caused by transient CO2 injections should be noted, since regardless of whether there was life on Mars or not, they represent periods of increased biological potential.

ium (Donahue et al., 1982) suggests that Venus may have had 100 times its current water inventory (Donahue et al., 1982). Others dispute the interpretation of the imbalance, suggesting instead an equilibrium with cometary-derived water (Grinspoon and Lewis, 1988), although revisions in the hydrogen escape rate support the existence of an early ocean on Venus (Donahue and Hodges, 1992). If Venus did have a higher water inventory then a `moist' greenhouse model has been proposed in which Venus may have had early oceans that were close to boiling (Kasting et al., 1984). Eventually, increases in solar luminosity would have set in

6. Model of the change in Venusian UV ¯ux over time The present day atmospheric conditions of Venus as well as the young surface age which may be just a few hundreds of millions of years (Ivanov and Basilevsky, 1987), means that information on the conditions of early Venus is all but lost. However, the deuterium/ hydrogen ratio, which is enriched 100-fold in deuter-

Fig. 3. Photobiological history of Venus. Changes in UVA, B and C radiation from 4.5 Ga to the present. The history is dominated by the greenhouse e€ect, which within the ®rst few hundred million years reduces surface UV ¯ux to insigni®cant levels.

C.S. Cockell / Planetary and Space Science 48 (2000) 203±214

place a runaway greenhouse e€ect. The oceans would have begun to boil away, weathering would have ceased, CO2 locked up in carbonates would have been recycled (this would require subduction of the early Venusian surface which is not known) and the CO2 partial pressures would have rapidly risen to their current value of 90 bar. It has been suggested that such a scheme would have occurred within the ®rst few hundred million years of Venusian history (Kasting et al., 1984). Building a detailed model of UV ¯ux from this data is problematic, but here a tentative scheme is proposed (Fig. 3). A pCO2 similar to early Earth may have been present on early Venus (Kasting et al., 1984). The CO2 in the Venusian atmosphere is believed to be similar to that contained in terrestrial carbonates (Pollack, 1981). In this case the early Venusian atmosphere may have had a pCO2 something in the region of 1 bar. In the model used here a starting inventory of 1 bar is assumed. The radiative transfer model assumes a similar pN2 to present-day Venus, i.e. 03.2 bar. After a few hundred million years the runaway greenhouse e€ect takes over and CO2 partial pressures rapidly rise. After they exceed 10 bar, UV ¯ux on the surface of Venus rapidly begins to be reduced, such that by the time it reaches 90 bar, UV ¯ux is negligible. The lack of UV radiation on present-day Venus is also exacerbated by the presence of a UV absorber in the Venusian clouds (Pollack et al., 1980). 7. Theoretical photobiological consequences for Venus Photobiologically, the environment of the surface of early Venus depends upon the initial gaseous composition of the Venusian atmosphere. If it was similar to early Earth then the Sun±Venus distance dictates that the ¯ux must have been 1.9 times higher than Earth. This UV radiation environment would probably have been tolerable to any potential biota (Cockell, 1999c) and particularly if it inhabited early Venusian oceans where at a depth of 040 m DNA-weighted irradiance may have been similar to the exposed surface of present-day Earth (Cockell, 1999b). Many protection mechanisms that may have been operative on early Earth, are likely to be able to accommodate a two fold increase in UV ¯ux from an evolutionary point of view, since they are already capable of reducing incident biologically e€ective irradiances by two to three orders of magnitude (Cockell, 1998). These include the matting habit, lithic communities and a diversity of other approaches. Thus, from a theoretical point of view the early Venusian photobiological environment was probably not a constraint to life. The runaway greenhouse e€ect would have given rise, in the space of a few hundred million years, to a

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photobiologically completely clement surface, a condition that remains today. However, the increase in temperature associated with the greenhouse e€ect would have exceeded the upper temperature bounds for life as well as removing liquid water at an early stage in the planet's history. From a biological perspective, the temperature and photobiological e€ects of the greenhouse e€ect work in opposite directions, the e€ects of high temperature and lack of liquid water ultimately overwhelming the improved photobiological environment. 8. Comparative evolutionary photobiology The UV history of Mars is dominated by changes in the atmospheric CO2 inventory, likewise for Venus, but in the latter case the greenhouse e€ect has been the overwhelming factor. On Mars, UV ¯ux has increased, and if atmospheric collapse occurred, an ultraviolet crisis could have occurred at some point in its past. In contrast, on Venus, UV ¯ux has decreased and a period of sudden ultraviolet clemency may have occurred early in its history. Thus, when illustrated as a DNA-weighted irradiance, the photobiological history of Venus has been the opposite to Mars. However, like Mars the ultimate biological fate of Venus may be determined by other physical factors. Increases in temperature leading to a loss of liquid water would have rendered the surface unsuitable for life on Venus. In the case of Mars, lack of availability of liquid water driven though reductions in atmospheric pressure and temperature would have made the surface ultimately unsuitable for life. Thus, even though the photobiological environment of Mars is not much worse than Archean Earth and that of Venus is completely clement, the lifelessness of these planets is testament to the relative unimportance of UV radiation as a physical factor in evolution when other parameters become limiting. Because of the Sun±Mars distance, Earth and Mars probably did not start from the same photobiological conditions, particularly if they had similar atmospheric CO2 inventories. The photobiological conditions on Mars may have been more clement than early Earth. However, unlike Mars, life on Earth ultimately controlled the photobiological conditions of the planet. Oxygenic photosynthesis made possible an ozone column so that by 1.5 Ga, the photobiological history of Earth was dominated by the pervasiveness of this column and its perturbation by exogenous agents. The period of photobiological clemency ushered in by the ozone column has some similarities to the dramatic period of ultraviolet clemency that may have occurred on early Venus. However, in the latter case this occurred within the few hundred million years and was

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not associated with the rise of biology as on the Earth, but with the rise of a biologically destructive greenhouse e€ect with increasing CO2 partial pressures. In this paper comparisons are made between instantaneous irradiance since this is more easily constrained. However, rotational period will also in¯uence the comparative photobiology of planetary surfaces. Day length in the early Archean is believed to have been about 14 h (Walker et al., 1983). The increase in day length has principally been caused by lunar tidal drag. If the DNA-weighted irradiance was calculated as a total daily ¯uence for Earth rather than instantaneous dose, the rate of increase of UV ¯ux from 4.5 to 2.5 Ga would be greater since super-imposed upon increase in solar luminosity and reductions in pCO2 would be increasing day length. Because Mars does not su€er a signi®cant tidal drag from a moon, its day length was probably not much shorter than today (Laskar and Robutel, 1993) and so the trends discussed in this paper would not be altered for a daily ¯uence. In the case of Venus, the planet is virtually tidally locked with a slow retrograde motion and so early day length information is lost. However, since the planet rapidly entered a period of ultraviolet clemency, the e€ect of day length on the UV radiation environment became irrelevant, although it could have been signi®cant for a pre-greenhouse Venus. Obliquity will also be signi®cant for total ¯uence. Since the Earth's obliquity is moon stabilized (Laskar et al., 1993) and oscillates 21.38 around the mean of 23.38, which has probably been the case since the Archean, changes have not been a signi®cant photobiological factor for life. The martian obliquity, however, is not primordial and probably chaotically oscillates from 00 to 608 (Laskar and Robutel, 1993). At low obliquities, most of the surface of the planet is subjected to a light/dark cycle. At high obliquities greater proportions of the planet are subjected to long periods of darkness. During such phases habitats for exposed chemosynthetic or heterotrophic life that are protected for 0320 days in darkness could theoretically exist, but during the rest of the year the surface would be exposed to long periods of continuous UV exposure. Biologically, this is analogous to polar microbial communities on Earth which have to repair 24 h of continuous UV damage during summer (e.g. Vincent and Quesada, 1994). Because at higher latitudes the midday zenith angle is higher, then total daily ¯uence may not be much worse than at the equator at vernal equinox, the damage is just spread over the whole day. In the more recent history of Mars it is possible that obliquity alterations would cause changes in pCO2 caused by freeze out of the atmosphere at the poles. Lindner and Jakosky (1985) estimate that at an obliquity of 128, pCO2 may have been as low as 0.1 mbar and 0.02 mbar at an obliquity

of 98. However, even at an obliquity of 98, increases in DNA-weighted irradiances at a zenith angle of 08 amount to less than 10%. Thus, obliquity alterations on Mars have not imposed signi®cant ultraviolet constraints on life although changes in PAR availability at high obliquity could have implications for photosynthetic life at high latitudes. Again, we do not know the obliquity of early Venus, but because of the greenhouse e€ect, UV rapidly insigni®cant for life, although obliquity could conceivably have been important for high latitude early Venusian oceans. Although we do not know if either Venus or Mars possessed life, understanding the theoretical photobiological history of the terrestrial planets can improve our understanding of the role of UV radiation in shaping their suitability as abodes for life. This information may ultimately help improve our understanding of the ultraviolet environments of extrasolar planets (Cockell, 1999d; Kasting et al., 1997) and particularly those with similar conditions to Venus, Earth or Mars. Acknowledgements I would like to express my gratitude to Christopher McKay for the review of the initial draft and to two anonymous reviewers for their comments. References Aikin, A.C., Chandra, S., Stecher, T.P., 1980. Supernovae e€ects on the terrestrial atmosphere. Planetary and Space Science 28, 639± 644. Asada, K., Kanematsu, S., Okaka, S., Hayakawa, T., 1980. Phylogenetic distribution of three types of superoxide dismutase in organisms and in cell organelles. In: Bannister, J.V., Hill, H.A.O. (Eds.), Chemical and Biochemical Aspects of Superoxide and Superoxide Dismutase. Elsevier, pp. 136±153. Barth, C.A., Hord, C.W., Stewart, A.I., Lane, A.L., Dick, M.L., Andersen, G.P., 1973. Mariner 9 ultraviolet spectrometer experiment: seasonal variation of ozone on Mars. Science 179, 797± 798. Barth, C.A., Dick, M.L., 1974. Ozone and the polar hoods of Mars. Icarus 22, 205±211. Berkner, L.V., Marshall, L.C., 1965. History of major atmospheric components. Proceedings of the National Academy of Sciences 53, 1215±1225. Boston, P.J., Ivanov, M.V., McKay, C.P., 1992. On the possibility of chemosynthetic ecosystems in subsurface habitats on Mars. Icarus 95, 300±308. Bothwell, M.L., Sherbot, D.M.J., Pollock, C.M., 1994. Ecosystem response to solar ultraviolet-B radiation: in¯uence of trophic level interactions. Science 265, 97±100. Canuto, V.M., Levine, J.S., Augustsson, T.R., Imho€, C.L., 1982. UV radiation from the young sun and oxygen and ozone levels in the prebiological palaeoatmosphere. Nature 296, 816±820. Canuto, V.M., Levine, J.S., Augustsson, T.R., Imho€, C.L., Giampapa, M.S., 1983. The young sun and the atmosphere and photochemistry of the early Earth. Nature 305, 281±286. Carr, M.H., 1987. Water on Mars. Nature 326, 30±35.

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