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Crises and extinction in the fossil record—a role for ultraviolet radiation?

Published online by Cambridge University Press:  20 May 2016

Charles S. Cockell
Charles S. Cockell*
Affiliation:
Department of Plant Biology, Carnegie Institution, 290 Panama Street, Stanford, California 94305–1297.
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Abstract

A number of natural events can cause ozone depletion, including asteroid and comet impacts, large-scale volcanism involving the stratospheric injection of chlorine, and close cosmic events such as supernovae. These events have previously been postulated to have been sole or contributory causes of mass extinctions. Following such events, UV-B radiation would have been elevated at the surface of the earth. The possibilities for detecting elevated UV-B as a kill mechanism in the fossil record are discussed. In the case of impact events and large-scale volcanism, the taxa affected by increases in UV-B radiation are likely to be similar to those affected by cooling and by the initial drop in irradiance caused by stratospheric dust injection. Thus UV-B may synergistically exacerbate the effects of these other environmental changes and contribute to stress in the biosphere, although UV-B alone is unlikely to cause a mass extinction. By the same token, however, this similarity in affected taxa is likely to make delineating the involvement of UV-B radiation in the fossil record more difficult. Cosmic events such as supernovae may produce smaller extinction events, but ones that are “cleaner” UV catastrophes without the involvement of other environmental changes.

Type
Articles
Information
Paleobiology , Volume 25 , Issue 2 , Spring 1999 , pp. 212 - 225
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Aikin, A. C., Chandra, S., and Stecher, T. P. 1980. Supernovae effects on the terrestrial atmosphere. Planetary and Space Science 28: 639–644.Google Scholar
Alvarez, L. W., Alvarez, W., Asaro, F., and Michel, H. V. 1980. Extraterrestrial cause for the Cretaceous-Tertiary extinction: experimental results and theoretical interpretation. Science 208: 1095–1108.Google Scholar
Angell, J. K. and Korshover, J. 1973. Quasi-biennial and long-term fluctuations in total ozone. Monthly Weather Reviews 101: 426–443.Google Scholar
Antia, N. J. and Cheng, J. Y. 1970. The survival of axenic cultures of marine planktonic algae from prolonged exposure to darkness at 20°C. Phycologia 9: 179–183.Google Scholar
Avery, J. A., Bowmaker, J. K., Djamgoz, M. B. A., and Downing, J. E. G. 1983. Ultraviolet sensitive receptor in a freshwater fish. Journal of Physiology 334: 23–24.Google Scholar
Benton, M. J. 1989. Mass extinctions amongst tetrapods and quality of the fossil record. Philosophical Transactions of the Royal Society of London B. 325: 369–386.Google Scholar
Benton, M. J. 1993. The fossil record 2. Chapman and Hall, London.Google Scholar
Berger, A. 1984. Accuracy and frequency stability of the earth's orbital elements during the Quaternary. Pp. 3–39. in Berger, A. I. eds. Milankovitch and climate, Part 1.Google Scholar
Blaustein, A. R., Hoffman, P. D., Hokit, D. G., Keisecker, J. M., Walls, S. C., and Hays, J. B. 1994. UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines. Proceedings of the National Academy of Sciences USA. 91: 1791–1795.Google Scholar
Bless, M. J. M., Becker, R. T., Higgs, K. T., Paproth, E., and Streel, M. 1992. Eustatic cycles around the Devonian-Carboniferous boundary and the sedimentary and fossil record in Saurland (Federal Republic of Germany). Annales de la Société Géologique de Belgique 115: 689–702.Google Scholar
Booth, C. R. and Morrow, J. R. 1997. The penetration of UV into natural waters. Photochemistry and Photobiology 65: 254–257.Google Scholar
Boucher, N. P. and Prezelin, B. B. 1996. An in situ biological weighting function for UV inhibition of phytoplankton carbon fixation in the southern ocean. Marine Ecology Progress Series 144: 223–236.Google Scholar
Boulter, M. C., Spicer, R. A., and Thomas, B. A. 1988. Patterns of plant extinction from some paleobiological evidence. In Larwood, G. P. ed. Extinction and survival in the fossil record. Systematics Association Special Volume 34: 1–36. Clarendon Oxford.Google Scholar
Bowmaker, J. K. and Kunz, Y. W. 1987. Ultraviolet receptors tetrachromatic color vision and retinal mosaics in the brown trout (Salmo trutta): age-dependent changes. Vision Research 27: 2101–2108.Google Scholar
Brasier, M. D. 1988. Foraminiferal extinction and ecological collapse during global biological events. In Larwood, G. P. ed. Extinction and survival in the fossil record. Systematics Association Special Volume 34: 37–64. Clarendon Oxford.Google Scholar
Bricaud, A., Morel, A., and Peieur, L. 1981. Absorption by dissolved organic matter of the sea (yellow substance) in the UV and visible domains. Limnology and Oceanography 26: 43–53.Google Scholar
Casey, R. E., Wigley, C. R., and Perez-Guzman, A. M. 1983. Biogeographic and ecologic perspective on polycystine radiolarian evolution. Paleobiology 9: 363–376.Google Scholar
Cockell, C. S. and Stokes, D. M. 1999. Polar winter: a biological model for impact events and related dark/cold climatic changes. Climatic Change (in press).Google Scholar
Collar, J. I. 1996. Biological effects of stellar collapse neutrinos. Physical Review Letters 76: 999–1002.Google Scholar
Copper, P. 1977. Paleolatitudes in the Devonian of Brazil and the Frasnian-Famennian mass extinction. Palaeogeography Palaeoclimatology, Palaeoecology 21: 165–207.Google Scholar
Courtillot, V., Jaeger, J. J., Yang, Z., Feraud, G., and Hofmann, C. 1996. The influence of continental flood basalts on mass extinctions: where do we stand? Geological Society of America Special Paper 307: 513–525.Google Scholar
Craig, C. L. and Bernard, G. D. 1990. Insect attraction to ultraviolet-reflecting spider webs and web decorations. Ecology 71: 616–623.Google Scholar
Crutzen, P. J. and Bruhl, C. 1996. Mass extinctions and supernova explosions. Proceedings of the National Academy of Sciences USA. 93: 1582–1584.Google Scholar
Cullen, J. C. and Neale, P. J. 1994. Ultraviolet radiation ozone depletion and marine photosynthesis. Photosynthesis Research 39: 303–320.Google Scholar
D’Hondt, S., Herbert, D., King, J., and Gibson, C. 1996. Planktic foraminifera asteroids, and marine production: death and recovery at the Cretaceous-Tertiary boundary. Geological Society of America Special Paper 307: 303–317.Google Scholar
Dar, A., Laor, A., and Shaviv, N. J. 1996. Life extinctions due to neutron star mergers. The Astrophysical Journal 160(2).Google Scholar
Donkor, V. A., Amewowor, D. H. A. K., and Häder, D. 1993a. Effects of tropical solar radiation on the motility of filamentous cyanobacteria. FEMS Microbiology Ecology 12: 143–148.Google Scholar
Donkor, V. A., Amewowor, D. H. A. K., and Häder, D. 1993b. Effects of tropical solar radiation on the velocity and photophobic behavior of filamentous gliding cyanobacteria. Acta Protozoologica 32: 67–72.Google Scholar
Donkor, V. A. and Häder, D. 1995. Protective strategies of several cyanobacteria against solar radiation. Journal of Plant Physiology 145: 750–755.Google Scholar
Downing, J. E. G., Djamgoz, M. B. A., and Bowmaker, J. K. 1986. Photoreceptors of cyprinid fish: morphological and spectral characteristics. Journal of Comparative Physiology 159: 859–868.Google Scholar
Elliott, D. K. 1986. Dynamics of extinction. Wiley New York.Google Scholar
Ellis, J. and Schramm, D. N. 1995. Could a nearby supernova explosion have caused a mass extinction? Proceedings of the National Academy of Sciences USA. 92: 235–238.Google Scholar
Erwin, D. H. 1994. The Permo-Triassic extinction. Nature 367: 231–236.Google Scholar
Fagerstrom, J. A. 1987. The evolution of reef communities. Wiley New York.Google Scholar
Flint, S. D. and Caldwell, M. M. 1983. Influence of floral optical properties on the ultraviolet radiation environment of pollen. American Journal of Botany 70: 1416–1419.Google Scholar
Geldsetzer, H. H. J., Goodfellow, W. D., and McLaren, D. J. 1993. The Frasnian-Famennian extinction event in a stable cratonic shelf setting: Trout River Northwest Territories Canada. Palaeogeography Palaeoclimatology, Palaeoecology 104: 81–95.Google Scholar
Gleason, D. F. and Wellington, G. M. 1993. Ultraviolet radiation and coral bleaching. Nature 365: 836–838.Google Scholar
Goreau, T. J. and Hayes, R. L. 1994. Coral bleaching and ocean “hot spots.”. Ambio 23: 176–180.Google Scholar
Häder, D-P. 1993. Effects of enhanced solar ultraviolet radiation on aquatic ecosystems. In Tevini, M. ed. UV-B radiation and ozone depletion. Lewis Publishers Boca Raton Fla.Google Scholar
Häder, D-P. and Worrest, R. C. 1991. Effects of enhanced solar ultraviolet radiation on aquatic ecosystems. Photochemistry and Photobiology 53: 717–725.Google Scholar
Hallam, A. and Wignall, P. B. 1997. Mass extinctions and their aftermath. Oxford University Press Oxford.Google Scholar
Harm, W. 1980. Biological effects of ultraviolet radiation. IUPAB Biophysics Series I Cambridge University Press Cambridge.Google Scholar
Harosi, F. I. and Hashimoto, Y. 1983. Ultraviolet sensitivity in goldfish: an independent UV retinal mechanism. Vision Research 25: 11–20.Google Scholar
Helbling, E. W., Villafane, V., and Holm-Hansen, O. 1994. Effects of ultraviolet radiation on antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing. In Weiler, C. S., Penhale, P. A. eds. Ultraviolet radiation in Antarctica: measurements and biological effects. Antarctic Research Series 62: 207–227.Google Scholar
Hoffman, A. 1986. Neutral model of phanerozoic diversification: implications for macro-evolution. Neues Jahrbuch für Geologie und Paläontolgie Abhandlungen 172: 219–244.Google Scholar
Hunt, G. E. 1978. Possible climatic and biological impact of nearby supernovae. Nature 271: 430–431.Google Scholar
Hunter, J. R., Taylor, J. H., and Moser, H. G. 1979. Effect of ultraviolet irradition on eggs and larvae of the northern anchovy Engraulis mordax, and the pacific mackerel Scomber japonicus, during the embryonic stage. Photochemistry and Photobiology 29: 325–338.Google Scholar
Jacobs, G. H. 1992. Ultraviolet vision in vertebrates. American Zoologist 32: 544–554.Google Scholar
Johnston, D. A. 1980. Volcanic contribution of chlorine to the stratosphere: more significant to ozone that previously estimated? Science 209: 491–493.Google Scholar
Kaiho, K. 1992. A low extinction rate of intermediate-water benthic foraminifera at the Cretaceous/Tertiary boundary. Marine Micropaleontology 18: 229-159.Google Scholar
Karanas, J. J., Worrest, R. C., and Van Dyke, H. 1981. Impact of UV-B radiation on the fecundidty of the copepod Acartia clausii. Marine Biology 65: 125–133.Google Scholar
Karentz, D., Cleaver, J. E., and Mitchell, D. L. 1991. Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultraviolet-B radiation. Journal of Phycology 27: 326–341.Google Scholar
Kasting, J. F. 1993. Earth's early atmosphere. Science 259: 920–926.Google Scholar
Keller, G., Barrera, E., Schmitz, B., and Mattson, E. 1993. Gradual mass extinction species survivorship and long-term environmental changes across the Cretaceous-tertiary boundary in high latitudes. Geological Society of America Bulletin 105: 979–997.Google Scholar
Knoll, A. H., Bambach, R. K., Canfield, D. E., and Grotzinger, J. P. 1996. Comparative earth history and Late Permian mass extinction. Science 273: 452–457.Google Scholar
Leroux, H., Warme, J. E., and Doukham, J. C. 1995. Shocked quartz in the Alamo Breccia South Nevada: evidence for a Devonian impact event. Geology 23: 1003–1006.Google Scholar
Lojtnant, B. and Pedersen, H. A. 1996. UV patterns of five species of Dactylorhea. Flora og Fauna 102: 205–208.Google Scholar
MacLeod, N. and Keller, G. 1996. Cretaceous-Tertiary mass extinctions. Norton London.Google Scholar
Madronich, S., Bjorn, L. O., Ilyas, M., and Caldwell, M. M. 1991. Changes in biologically effective ultraviolet radiation reaching the earth's surface. Pp. 1–13. in van der Leun, J. C., Tevini, M. eds. Environmental effects of ozone depletion. [1991 update.].Google Scholar
Makino, C. L., Dodd, R. L., Rohlich, P., and Baylor, D. A. 1985. Salamander UV-sensitive cones utilize more than one visual pigment. Biophysical Journal 68: A19.Google Scholar
Marshall, H. T. 1928. Ultra-violet and extinction. American Naturalist 62: 165–187.Google Scholar
McGhee, G. R. 1988. The Late Devonian extinction event: evidence for abrupt ecosystem collapse. Paleobiology 14: 250–257.Google Scholar
McGhee, G. R. 1996. The Late Devonian mass extinction. Columbia University Press, New York.Google Scholar
McLaren, D. J. and Goodfellow, W. D. 1990. Geological and biological consequences of giant impacts. Annual Reviews of Earth and Planetary Sciences 18: 123–171.Google Scholar
McMinn, A., Heljns, H., and Hodgson, D. 1994. Minimal effects of UVB radiation on Antarctic diatoms over the past 20 years. Nature 370: 547–549.Google Scholar
Menzel, R. and Backhaus, W. 1991. Colour vision in insects. Pp. 262–288. in Gouras, P. ed. Vision and visual dysfunction: the perception of colour. Macmillan London.Google Scholar
Meyer-Rochow, V. B. 1991. Differences in ultraviolet wing patterns in the New Zealand lucaenid butterflies Lucaena salustius, Lucaena rauparaha, and Lucaena feredayi as a likely isolating mechanism. Journal of the Royal Society of New Zealand 21: 169–178.Google Scholar
Mirecki, R. M. and Teramura, A. H. 1984. Effects of ultraviolet-B irradiance on soybean Part V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. Plant Physiology 74: 475–480.Google Scholar
Murali, N. S. and Teramura, A. H. 1987. Insensitivity of soybean photosynthesis to ultraviolet-B radiation under phosphorus deficiency. Journal of Plant Nutrition 10: 501–515.Google Scholar
Musil, C. F. 1996. Accumulated effect of elevated ultraviolet-B radiation over multiple generations of the arid-environment annual Dimorphotheca sinuata DC (Asteraceae). Plant, Cell and Environment 19: 1017–1027.Google Scholar
Ovaska, K., Davis, T. M., and Flamarique, I. N. 1997. Hatching success and larval survival of the frogs Hyla regilla and Rana aurora under ambient and artificially enhanced solar ultraviolet radiation. Canadian Journal of Zoology 75: 1081–1088.Google Scholar
Panagopoulus, I., Bornman, J. F., and Bjorn, L. O. 1991. Response of sugar beet plants to ultraviolet-B (280-320 nm) radiation and Cercospora leaf spot disease. Physiologia Plantarum 84: 14–145.Google Scholar
Pedder, A. E. H. 1982. The rugose coral record across the Frasnian-Famennian boundary. Geological Society of America Special Paper 190: 485–490.Google Scholar
Pollack, J. B., Toon, O. B., Ackerman, T. P., and McKay, C. P. 1983. Environmental effects of an impact-generated dust cloud: implications for the Cretaceous-Tertiary extinctions. Science 219: 287–289.Google Scholar
Prinn, R. G. and Fegley, B. 1987. Bolide impacts, acid rain, and biospheric traumas at the Cretaceous-Tertiary boundary. Earth and Planetary Science Letters 83: 1–15.Google Scholar
Rampino, M. R. and Haggerty, B. M. 1996. Impact crises and mass extinctions: a working hypothesis. Geological Society of America Special Paper 307: 11–29.Google Scholar
Rampino, M. R., Self, S., and Stothers, R. B. 1988. Volcanic winters. Annual Reviews of Earth and Planetary Sciences 16: 73–99.Google Scholar
Raup, D. M. 1979. Size of the Permo-Triassic bottleneck and its evolutionary implications. Science 206: 217–218.Google Scholar
Raup, D. M. 1992. Large body impact and extinction in the Phanerozoic. Paleobiology 18: 80–88.Google Scholar
Reid, G. C., Isaksen, I. S. A., Holzer, T. E., and Crutzen, P. J. 1976. Influence of ancient solar-proton events on the evolution of life. Nature 259: 177–179.CrossRefGoogle Scholar
Reid, G. C., McAfee, J. R., and Crutzen, P. J. 1978. Effects of intense stratospheric ionisation events. Nature 275: 489–492.Google Scholar
Renne, P. R. and Basu, A. R. 1991. Rapid eruption of the Siberian Traps flood basalts at the Permo-Triassic boundary. Science 253: 176–179.Google Scholar
Renne, P. R., Zhang, Z., Richardson, M. A., Black, M. T., and Basu, A. R. 1995. Synchrony and causal relations between Permo-Triassic boundary crises and Siberian flood volcanism. Science 269: 1413–1416.Google Scholar
Retallack, G. J. 1995. Permian-Triassic life crisis on land. Science 267: 77–80.Google Scholar
Ruderman, M. A. 1974. Possible consequences of nearby supernova explosions for atmospheric ozone and terrestrial life. Science 184: 1079–1081.Google Scholar
Russell, D. and Tucker, W. 1971. Supernovae and the extinction of the dinosaurs. Nature 229: 553–554.Google Scholar
Sepkoski, J. J. 1996. Patterns of Phanerozoic extinction: a perspective from global data bases. Pp. 35–52. in Walliser, O. H.Global events and event stratigraphy. Springer, Berlin.Google Scholar
Shick, J. M., Lesser, M. P., and Jokiel, P. L. 1996. Effects of ultraviolet radiation on corals and other coral reef organisms. Global Change Biology 2: 527–545.Google Scholar
Shoemaker, E. M., Wolfe, R. F., and Shoemaker, C. S. 1990. Asteroid and comet flux in the neighbourhood of Earth. In Sharpton, V., Ward, P. eds. Global catastrophes in earth history Geological Society of America Special Paper. 247: 155–170.Google Scholar
Siebeck, O., Vail, T. L., Williamson, C. E., Vetter, R., Hessen, D., Zagarese, H., Little, E., Balseiro, E., Modenutti, B., Seva, J., and Shumate, A. eds. 1994. Impact of UV-B radiation on zooplankton and fish in pelagic freshwater ecosystems. Ergebnisse der Limnologie 43: 101–114.Google Scholar
Sinha, R. P., Singh, N., Kumar, A., Kumar, H. D., Häder, M., and Häder, D. P. 1996. Effects of UV irradiation on certain physiological and biochemical processes in cyanobacteria. Journal of Photochemistry and Photobiology 32: 107–113.Google Scholar
Smith, R. C. and Baker, K. S. 1979. Penetration of UV-B and biologically effective dose-rates in natural waters. Photochemistry and Photobiology 29: 311–323.Google Scholar
Smith, R. C., Baker, K. S., Holm-Hansen, O., and Olsen, R. 1980. Photoinhibition of photosynthesis in natural waters. Photochemistry and Photobiology 31: 585–592.Google Scholar
Smith, R. C., Prezelin, B. B., Baker, K. S., Bidigare, R. R., Boucher, N. P., Coley, T., Karentz, D., MacIntyre, S., Matlick, H. A., Menzies, D., Ondrusek, M., Wan, Z., and Waters, K. J. 1992. Ozone depletion: ultraviolet radiation and phytoplankton biology in Antarctic waters. Science 255: 952–959.Google Scholar
Stanley, S. M. 1988. Paleozoic mass extinctions: shared patterns suggest global cooling as a common cause. American Journal of Science 288: 334–352.Google Scholar
Stephenson, J. A. E. and Scourfield, M. W. J. 1991. Importance of energetic solar protons in ozone depletion. Nature 352: 137–139.Google Scholar
Stothers, R. B., Rampino, M. R., Self, S., and Wolfe, J. A. 1993. Volcanic winter? Climatic effects of the largest volcanic eruptions. In Latter, J. H. ed. Volcanic hazards Springer, Berlin.Google Scholar
Taylor, H. R., West, S. K., Rosenthal, F. S., Munoz, B., Newland, H. S., Abbey, H., and Emmett, E. A. 1988. Effect of ultraviolet radiation on cataract formation. New England Journal of Medicine 319: 1429–1433.Google Scholar
Teramura, A. H., Sullivan, J. H., and Lydon, J. 1990. Effects of UV-B radiation on soybean yield and seed quality: a 6-year field study. Physiologia Plantarum 80: 5–11.Google Scholar
Teramura, A. H., Ziska, L. H., and Sztein, A. E. 1991. Changes in growth and photosynthetic capacity of rice with increased UV-B radiation. Physiologia Plantarum 83: 373–383.Google Scholar
Terry, K. D. and Tucker, W. H. 1968. Biologic effects of supernovae. Science 159: 421–423.Google Scholar
Tevini, M. 1993. UV-B radiation and ozone depletion: effects on humans animals, plants, microorganisms, and materials. Lewis Publishers, Boca Raton, Fla.Google Scholar
Tevini, M. and Teramura, A. H. 1989. UV-B effects on terrestrial plants. Photochemistry and Photobiology 50: 479–487.Google Scholar
Thorsett, S. E. 1995. Terrestrial implications of cosmological gamma-ray burst models. The Astrophysical Journal 444: L53.Google Scholar
Toon, O. B., Zahnle, K., Morrison, D., Turco, R. P., and Covey, C. 1997. Environmental perturbations caused by the impacts of asteroids and comets. Reviews of Geophysics 35: 41–78.Google Scholar
Tschudy, R. H. and Tschudy, B. D. 1986. Extinction and survival of plant life following the Cretaceous/Tertiary boundary event Western Interior North America. Geology 14: 667–670.Google Scholar
Turco, R. P., Toon, O. B., Park, C., Whitten, R. C., and Pollack, J. B. 1981. Tunguska meteor fall of 1908: effects on stratospheric ozone. Science 214: 19–24.Google Scholar
van der Leun, J. C. and de Gruijl, F. R. 1993. Influences of ozone depletion on human and animal health. In Tevini, M. ed. UV-B radiation and ozone depletion: effects on humans, animals, plants, microorganisms, and materials. Lewis Publishers Boca Raton, Fla.Google Scholar
Vincent, W. F. and Quesada, A. 1994. Ultraviolet radiation effects on cyanobacteria: implications for Antarctic microbial ecosystems. In Weiler, C. S., Penhale, P. A. eds. Ultraviolet radiation in Antarctica: measurements and biological effects. Antarctic Research Series 62: 111–124.Google Scholar
Vincent, W. F. and Roy, S. 1993. Solar ultraviolet-B radiation and aquatic primary production: damage, protection and recovery. Environmental Reviews 1: 1–12.Google Scholar
Vogelmann, A. M., Ackerman, T. P., and Turco, R. P. 1992. Enhancements of biologically effective ultraviolet radiation following volcanic eruptions. Nature 359: 47–49.Google Scholar
Warner, C. W. and Caldwell, M. M. 1983. Influence of photon flux density in the 400-700 nm waveband on inhibition of photosynthesis by UV-B (280-320 nm) irradiation in soybean leaves: separation of indirect and immediate effects. Photochemistry and Photobiology 38: 341–346.Google Scholar
Whitten, R. C., Cuzzi, J., Borucki, W. J., and Wolfe, J. A. 1976. Effect of nearby supernova explosions on atmospheric ozone. Nature 263: 398–400.Google Scholar
Wignall, P. B. and Twitchett, R. J. 1996. Oceanic anoxia and the end-Permian mass extinction. Science 272: 1155–1158.Google Scholar
Williamson, C. E., Zagarase, H. E., Schulze, P. C., Hargreaves, B. R., and Seva, J. 1994. The impact of short-term exposure to UV-B radiation on zooplankton communities in north temperate lakes. Journal of Plankton Research 16: 205–218.Google Scholar
Yayanos, A. A. 1983. Thermal neutrons could be a cause of biological extinctions 65 Myr ago. Nature 303: 797–798.Google Scholar