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Evolutionary rates of mid-Permian tetrapods from South Africa and the role of temporal resolution in turnover reconstruction

  • Michael O. Day (a1), Roger B. J. Benson (a2), Christian F. Kammerer (a3) and Bruce S. Rubidge (a1)

Abstract

The Main Karoo Basin of South Africa contains a near-continuous sequence of continental deposition spanning ~80 Myr from the mid-Permian to the Early Jurassic. The terrestrial vertebrates of this sequence provide a high-resolution stratigraphic record of regional origination and extinction, especially for the mid–late Permian. Until now, data have only been surveyed at coarse stratigraphic resolution using methods that are biased by nonuniform sampling rates, limiting our understanding of the dynamics of diversification through this important time period. Here, we apply robust methods (gap-filler and modified gap-filler rates) for the inference of patterns of species richness, origination rates, and extinction rates to a subset of 1321 reliably-identified fossil occurrences resolved to approximately 50 m stratigraphic intervals. This data set provides an approximate time resolution of 0.3–0.6 Myr and shows that extinction rates increased considerably in the upper 100 m of the mid-Permian Abrahamskraal Formation, corresponding to the latest part of the Tapinocephalus Assemblage Zone (AZ). Origination rates were only weakly elevated in the same interval and were not sufficient to compensate for these extinctions. Subsampled species richness estimates for the lower part of the overlying Teekloof Formation (corresponding to the Pristerognathus and Tropidostoma AZs) are low, showing that species richness remained low for at least 1.5–3 million years after the main extinction pulse. A high unevenness of the taxon abundance–frequency distribution, which is classically associated with trophically unstable postextinction faunas, in fact developed shortly before the acme of elevated extinction rates due to the appearance and proliferation of the dicynodont Diictodon. Our findings provide strong support for a Capitanian (“end-Guadalupian”) extinction event among terrestrial vertebrates and suggest that further high-resolution quantitative studies may help resolve the lack of consensus among paleobiologists regarding this event.

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Present address: Department of Earth Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom.

*

Present address: North Carolina Museum of Natural Sciences, Raleigh, North Carolina 27601-1029, U.S.A.

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Alroy, J. 1996. Constant extinction, constrained diversification, and uncoordinated stasis in North American mammals. Palaeogeography, Palaeoclimatology, Palaeoecology 127:285311.
Alroy, J. 2008. Dynamics of origination and extinction in the marine fossil record. Proceedings of the National Academy of Sciences USA 105:1153611542.
Alroy, J. 2009. Speciation and extinction in the fossil record of North American mammals. Pp. 301323. in R. Butlin, J. Bridle, and D. Schluter, eds. Speciation and patterns of diversity. Cambridge University Press, Cambridge.
Alroy, J. 2010a. Fair sampling of taxonomic richness and unbiased estimation of origination and extinction rates. In J. Alroy, and G. Hunt, eds. Quantitative methods in paleobiology (Paleontological Society Papers 16 5580.
Alroy, J. 2010b. Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification. Palaeontology 53:12111235.
Alroy, J. 2010c. The shifting balance of diversity among major marine animal groups. Science 329:11911194.
Alroy, J. 2014. Accurate and precise estimates of origination and extinction rates. Paleobiology 40:374397.
Alroy, J. 2015. A more precise speciation and extinction rate estimator. Paleobiology 41:633639.
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J., Sommers, M. G., Wagner, P. J., and Webber, A.. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences USA 98:62616266.
Alroy, J., Aberhan, M., Bottjer, D. J., Foote, M., Fürsich, F. T., Harries, P. J., Hendy, A. J. W., Holland, S. M., Ivany, L. C., Kiessling, W., Kosnik, M. A., Marshall, C. R., McGowan, A. J., Miller, A. I., Olszewski, T. D., Patzkowsky, M. E., Peters, S. E., Villier, L., Wagner, P. J., Bonuso, N., Borkow, P. S., Brenneis, B., Clapham, M. E., Fall, L. M., Ferguson, C. A., Hanson, V. L., Krug, A. Z., Layou, K. M., Leckey, E. H., Nürnberg, S., Powers, C. M., Sessa, J. A., Simpson, C., Tomašových, A., and Visaggi, C. C.. 2008. Phanerozoic trends in the global diversity of marine invertebrates. Science 321:97100.
Arefiev, M. P., Golubev, V. K., Karasev, E. V., Zhokina-Naumcheva, M. A., Balabanov, Y. P., Minikh, A. V., Minikh, M. G., Molostovskaya, I. I., and Yaroshenko, O.P.. 2015. Type and reference sections of the Permian–Triassic continental sequences of the Eastern European Platform: main isotope, magnetic, and biotic events. P. 103 in Field Guide for XVIII International Congress on the Carboniferous and Permian. Sukhona and Severnaya Dvina Rivers field trip. Kazan, Russia.
Bambach, R. K., Knoll, A. H., and Wang, S. C.. 2004. Origination, extinction, and mass depletions of marine diversity. Paleobiology 30:522542.
Benson, R. B. J., and Upchurch, P.. 2013. Diversity trends in the establishment of terrestrial vertebrate ecosystems: interactions between spatial and temporal sampling biases. Geology 41:4346.
Benson, R. B. J., Butler, R. J., Alroy, J., Mannion, P. D., Carrano, M. T., and Lloyd, G. T.. 2016. Near-stasis in the long-term diversification of Mesozoic tetrapods. PLOS Biology 14:e1002359.
Benton, M. J. 1985. Mass extinction among non-marine tetrapods. Nature 316:811814.
Benton, M. J., Tverdokhlebov, V. P., and Surkov, M. V.. 2004. Ecosystem remodelling among vertebrates at the Permian–Triassic boundary in Russia. Nature 432:97100.
Benton, M. J., Ruta, M., Dunhill, A. M., and Sakamoto, M.. 2013. The first half of tetrapod evolution, sampling proxies, and fossil record quality. Palaeogeography, Palaeoclimatology, Palaeoecology 372:1841.
Bond, D. P. G., and Grasby, S. E.. 2017. Editorial: Mass extinction causality. Palaeogeography, Palaeoclimatology, Palaeoecology 478:12.
Bond, D. P. G., and Wignall, P. B.. 2014. Large igneous provinces and mass extinctions: an update. Geological Society of America Special Papers 505:29–56.
Bond, D. P. G., Hilton, J., Wignall, P. B., Ali, J. R., Stevens, L. G., Sun, Y., and Lai, X.. 2010. The Middle Permian (Capitanian) mass extinction on land and in the oceans. Earth-Science Reviews 102:100116.
Bond, D. P. G., Wignall, P. B., Joachimski, M. M., Sun, Y., Savov, I., Grasby, S. E., Beauchamp, B., and Blomeier, D. P. G.. 2015. An abrupt extinction in the Middle Permian (Capitanian) of the Boreal Realm (Spitsbergen) and its link to anoxia and acidification. GSA Bulletin 127:14111421.
Botha, J., and Smith, R. M. H.. 2006. Rapid vertebrate recuperation in the Karoo Basin of South Africa following the End-Permian extinction. Journal of African Earth Sciences 45:502514.
Brocklehurst, N., Ruta, M., Müller, J., and Fröbisch, J.. 2015. Elevated extinction rates as a trigger for diversification rate shifts: early amniotes as a case study. Scientific Reports 5:ar17104.
Catuneanu, O., Hancox, P. J., and Rubidge, B. S.. 1998. Reciprocal flexural behaviour and contrasting stratigraphies: a new basin development model for the Karoo retroarc foreland system, South Africa. Basin Research 10:417439.
Clapham, M. E., Shen, S., and Bottjer, D. J.. 2009. The double mass extinction revisited: reassessing the severity, selectivity, and causes of the end-Guadalupian biotic crisis (Late Permian). Paleobiology 35:3250.
Close, R. A., Benson, R. B. J., Upchurch, P., and Butler, R. J.. 2017. Controlling for the species–area effect supports constrained long-term Mesozoic terrestrial vertebrate diversification. Nature. Communications 8:15381.
Close, R. A., Evers, S. W., Alroy, J., and Butler, R. J.. 2018. How should we estimate diversity in the fossil record? Testing richness estimators using sampling-standardised discovery curves. Methods in Ecology and Evolution. doi: 10.1111/2041-210X.12.
Cole, D. I., and Wipplinger, P. E.. 2001. Sedimentology and molybdenum potential of the Beaufort Group in the main Karoo basin, South Africa. Memoirs of the Council for Geoscience 80:1225.
Day, M. O. 2013. Middle Permian continental biodiversity changes as reflected in the Beaufort Group of South Africa: a bio- and lithostratigraphic review of the eodicynodon, tapinocephalus and pristerognathus Assemblage Zones. Unpublished Ph.D. thesis. University of the Witwatersrand, Johannesburg.
Day, M. O., and Rubidge, B. S.. 2014. A brief lithostratigraphic review of the Abrahamskraal and Koonap formations of the Beaufort Group, South Africa: towards a basin–wide stratigraphic scheme for the Middle Permian Karoo. Journal of African Earth Sciences 100:227242.
Day, M. O., Güven, S., Abdala, F., Jirah, S., Rubidge, B., and Almond, J.. 2015a. Youngest dinocephalian fossils extend the Tapinocephalus Zone, Karoo Basin, South Africa. South African Journal of Science 111(3–4), 15.
Day, M. O., Ramezani, J., Bowring, S. A., Sadler, P. M., Erwin, D. H., Abdala, F., and Rubidge, B. S.. 2015b. When and how did the terrestrial mid-Permian mass extinction occur? Evidence from the tetrapod record of the Karoo Basin, South Africa. Proceedings of the Royal Society of London B 282(1811) 20150834.
Foote, M. 1999. Morphological diversity in the evolutionary radiation of Paleozoic and post-Paleozoic crinoids. Paleobiology 25(Suppl. 2) 115.
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74102.
Foote, M. 2003. Origination and extinction through the Phanerozoic: a new approach. Journal of Geology 111:125148.
Foote, M., and Sepkoski, J. J.. 1999. Absolute measures of the completeness of the fossil record. Nature 398:415417.
Fröbisch, J. 2013. Vertebrate diversity across the end-Permian mass extinction—separating biological and geological signals. Palaeogeography Palaeolimatology Palaeoecology 372:5061.
Fröbisch, J. 2014. Synapsid diversity and the rock record in the Permian–Triassic Beaufort Group (Karoo Supergroup), South Africa. Pp. 305319. in C. Kammerer, K. Angielczyk, and J. Fröbisch, eds. Early evolutionary history of the Synapsida. Springer, Dordrecht, Netherlands.
Glazier, D. S. 1987. Toward a predictive theory of speciation: the ecology of isolate selection. Journal of Theoretical Biology 126:323333.
Golubev, V. K. 2000. The faunal assemblages of Permian terrestrial vertebrates from Eastern Europe. Paleontological Journal 34(Suppl. 2), S211S224.
Hannisdal, B., and Peters, S. E.. 2011. Phanerozoic Earth system evolution and marine biodiversity. Science 334:11211124.
Harnik, P. G., Simpson, C., and Payne, J. L.. 2012. Long-term differences in extinction risk among the seven forms of rarity. Proceedings of the Royal Society of London B 279:49694976.
Huang, H., Cawood, P. A., Hou, M.-C., Yang, J.-H., Ni, S.-J., Du, Y.-S., Yan, Z.-K., and Wang, J.. 2016. Silicic ash beds bracket Emeishan Large Igneous province to <1m.y. at ~260Ma. Lithos 264:1727.
Irmis, R. B., and Whiteside, J. H.. 2011. Delayed recovery of non-marine tetrapods after the end-Permian mass extinction tracks global carbon cycle. Proceedings of the Royal Society of London B. doi: 10.1098/rspb.2011.1895.
Jablonski, D. 2002. Survival without recovery after mass extinctions. Proceedings of the National Academy of Sciences USA 99:81398144.
Jablonski, D. 2008. Extinction and the spatial dynamics of biodiversity. Proceedings of the National Academy of Sciences USA 105(Suppl. 1), 1152811535.
Jin, Y., Shen, S., Henderson, C. M., Wang, X., Wang, W., Wang, Y., Cao, C., and Shang, Q.. 2006. The Global Stratotype Section and Point (GSSP) for the boundary between the Capitanian and Wuchiapingian stage (Permian). Episodes 29:253.
Johnson, C. 1998. Species extinction and the relationship between distribution and abundance. Nature 394:272.
Kiessling, W., and Simpson, C.. 2011. On the potential for ocean acidification to be a general cause of ancient reef crises. Global Change Biology 17:5667.
Lanci, L., Tohver, E., Wilson, A., and Flint, S.. 2013. Upper Permian magnetic stratigraphy of the lower Beaufort Group, Karoo Basin. Earth and Planetary Science Letters 375:123134.
Leonova, T. B. 2009. Ammonoid evolution in marine ecosystems prior to the Permian–Triassic crisis. Paleontological Journal 43:858.
Longrich, N. R., Scriberas, J., and Wills, M. A.. 2016. Severe extinction and rapid recovery of mammals across the Cretaceous–Palaeogene boundary, and the effects of rarity on patterns of extinction and recovery. Journal of Evolutionary Biology 29:14951512.
Lucas, S. G. 1998. Global Triassic tetrapod biostratigraphy and biochronology. Palaeogeography, Palaeoclimatology, Palaeoecology 143:347384.
Lucas, S. G. 2009. Timing and magnitude of tetrapod extinctions across the Permo–Triassic boundary. Journal of Asian Earth Sciences 36:491502.
Mayhew, P. J., Bell, M. A., Benton, T. G., and McGowan, A. J.. 2012. Biodiversity tracks temperature over time. Proceedings of the National Academy of Sciences USA 109:1514115145.
Maxwell, W. D. 1992. Permian and Early Triassic extinction of non-marine tetrapods. Palaeontology 35:571583.
McGhee, G. R. Jr., Clapham, M. E., Sheehan, P. M., Bottjer, D. J., and Droser, M. L.. 2013. A new ecological-severity ranking of major Phanerozoic biodiversity crises. Palaeogeography, Palaeoclimatology, Palaeoecology 370:260270.
McKinney, M. L. 1997a. Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28:495516.
McKinney, M. L. 1997b. How do rare species avoid extinction? A paleontological view. Pp. 110129. in W. E. Kunin, and K. J. Gaston, eds. The biology of rarity. Chapman & Hall, London.
Modesto, S. P., Damiani, R. J., Neveling, J., and Yates, A. M.. 2003. A new Triassic owenettid parareptile and the mother of mass extinctions. Journal of Vertebrate Paleontology 23:715719.
Nicolas, M. V. 2007. Tetrapod biodiversity through the Permo-Triassic Beaufort Group (Karoo Supergroup) of South Africa. Unpublished Ph.D. thesis. University of the Witwatersrand, Johannesburg, South Africa. http://146.141.12.21/handle/10539/5391.
Norell, M. A. 1992. Taxic origin and temporal diversity: the effect of phylogeny. Pp. 89118. in M. J. Novacek, and Q. D. Wheeler, eds. Extinction and phylogeny. Columbia University Press, New York.
Paiva, F. 2016. Fluvial facies architecture and provenance history of the Abrahamskraal–Teekloof Formation transition (Lower Beaufort Group) in the main Karoo Basin. Unpublished M.Sc. dissertation, University of Cape Town, Cape Town, South Africa. https://open.uct.ac.za/handle/11427/20615?show=full.
Payne, J. L., and Clapham, M. E.. 2012. End-Permian mass extinction in the oceans: an ancient analog for the twenty-first century? Annual Review of Earth and Planetary Sciences 40:89111.
Quental, T. B., and Marshall, C. R.. 2013. How the Red Queen drives terrestrial mammals to extinction. Science 341:290292.
Raup, D. M. 1972. Taxonomic diversity during the Phanerozoic. Science 177:10651071.
Raup, D. M. 1976. Species diversity in the Phanerozoic: a tabulation. Paleobiology 2:279288.
Raup, D. M. 1988. Diversity crises in the geological past. Pp. 5157. in E. O. Wilson, and F. M. Peter, eds. Biodiversity. National Academies Press, Washington, D.C.
Raup, D. M., and Sepkoski, J. J.. 1982. Mass extinctions in the marine fossil record. Science 215:15011503.
Reisz, R. R., and Modesto, S. P.. 2007. Heleosaurus scholtzi from the Permian of South Africa: a varanopid synapsid, not a diapsid reptile. Journal of Vertebrate Paleontology 27:734739.
Retallack, G. J., Metzger, C. A., Greaver, T., Jahren, A. H., Smith, R. M. H., and Sheldon, N. D.. 2006. Middle–Late Permian mass extinction on land. Geological Society of America Bulletin 118:13981411.
Rubidge, B. 1995a. Biostratigraphy of the Eodicynodon Assemblage Zone. Pp. 37. in B. S. Rubidge, ed. Biostratigraphy of the Beaufort Group (Karoo Supergroup). Council for Geoscience, Pretoria.
Rubidge, B. S. ed. 1995b. Biostratigraphy of the Beaufort Group (Karoo Supergroup). Council for Geoscience, Pretoria.
Rubidge, B. S., and Hopson, J. A.. 1996. A primitive anomodont therapsid from the base of the Beaufort Group (Upper Permian) of South Africa. Zoological Journal of the Linnean Society 117:115139.
Rubidge, B. S., Modesto, S. P., and Sidor, C. P.. 1999. Eunotosaurus africanus from the Ecca–Beaufort contact in Northern Cape Province, South Africa—implications for Karoo Basin development. South African Journal of Science 95:553555.
Rubidge, B. S., Erwin, D. H., Ramezani, J., Bowring, S. A., and de Klerk, W. J.. 2013. High-precision temporal calibration of Late Permian vertebrate biostratigraphy: U-Pb zircon constraints from the Karoo Supergroup, South Africa. Geology 41:363366.
Ruta, M., and Benton, M. J.. 2008. Calibrated diversity, tree topology and the mother of mass extinctions: the lesson of temnospondyls. Palaeontology 51:12611288.
Ruta, M., Cisneros, J. C., Liebrecht, T., Tsuji, L. A., and Müller, J.. 2011. Amniotes through major biological crises: faunal turnover among Parareptiles and the end-Permian mass extinction. Palaeontology 54:11171137.
Ruta, M., Angielczyk, K. D., Fröbisch, J., and Benton, M. J.. 2013. Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids. Proceedings of the Royal Society of London B 280(1768.
Sadler, P. M., Kemple, W. G., and Kooser, M. A.. 2008. CONOP9 programs for solving the stratigraphic correlation and seriation problems as constrained optimization. Pp. 461462. in P. J. Harries, ed. High-resolution approaches in stratigraphic paleontology. Springer, Dordrecht, Netherlands.
Sepkoski, J. J. 1982. Mass extinctions in the Phanerozoic oceans: a review. Pp. 283290. in L. T. Silver, and P. H. Schultz, eds. Geological implications of impacts of large asteroids and comets on the Earth (Geological Society of America Special Papers 190.
Sepkoski, J. J. 1994. Limits to randomness in paleobiologic models: the case of Phanerozoic species diversity. Acta Palaeontologica Polonica 38:175198.
Sepkoski, J. J. 1996. Patterns of Phanerozoic extinction: a perspective from global data bases. Pp. 3551. in O. H. Walliser, ed. Global events and event stratigraphy in the Phanerozoic: results of the international interdisciplinary cooperation in the IGCP–Project 216 “Global Biological Events in Earth History.” Springer, Berlin.
Sepkoski, J. J. 2002. A compendium of fossil marine animal genera. Bulletins of American Paleontology 363:1560.
Shen, S.-Z., and Shi, G. R.. 1996. Diversity and extinction patterns of Permian Brachiopoda of South China. Historical. Biology 12:93110.
Shen, S.-Z., and Shi, G. R.. 2002. Paleobiogeographical extinction patterns of Permian brachiopods in the Asian–western Pacific region. Paleobiology 28:449463.
Shen, S.-Z., and Shi, G. R.. 2009. Latest Guadalupian brachiopods from the Guadalupian/Lopingian boundary GSSP section at Penglaitan in Laibin, Guangxi, South China and implications for the timing of the pre-Lopingian crisis. Palaeoworld 18:152161.
Silvestro, D., Salamin, N., and Schnitzler, J.. 2014. PyRate: a new program to estimate speciation and extinction rates from incomplete fossil data. Methods in Ecology and Evolution 5:11261131.
Smith, A. B. 1994. Systematics and the fossil record. Wiley-Blackwell, Oxford.
Smith, A. B. 2001. Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies. Philosophical Transactions of the Royal Society of London B 356:351367.
Smith, A. B., and McGowan, A. J.. 2011. The ties linking rock and fossil records and why they are important for palaeobiodiversity studies. Geological Society of London Special Publication 358:17.
Smith, R. M. H., and Botha, J.. 2005. The recovery of terrestrial vertebrate diversity in the South African Karoo Basin after the end-Permian extinction. Comptes Rendus Palevol 4:623636.
Smith, R. M. H., and Botha-Brink, J.. 2014. Anatomy of a mass extinction: sedimentological and taphonomic evidence for drought-induced die-offs at the Permo-Triassic boundary in the main Karoo Basin, South Africa. Palaeogeography, Palaeoclimatology, Palaeoecology 396:99118.
Smith, R. M. H., Rubidge, B. S., and Van der Walt, M. V. M.. 2012. Therapsid biodiversity patterns and palaeoenvirnoments of the Karoo Basin, South Africa. Pp. 3164. in A. Chinsamy-Turan, ed. Forerunners of mammals. Indiana University Press, Bloomington.
Stanley, S. M. 1986. Population size, extinction, and speciation: the fission effect in Neogene Bivalvia. Paleobiology 12:89110.
Stanley, S. M. 2016. Estimates of the magnitudes of major marine mass extinctions in earth history. Proceedings of the National Academy of Sciences USA 113:E6325E6334.
Stanley, S. M., and Yang, X.. 1994. A double mass extinction at the end of the Paleozoic era. Science 266:13401344.
Twitchett, R. J., Krystyn, L., Baud, A., Wheeley, J. R., and Richoz, S.. 2004. Rapid marine recovery after the end-Permian mass-extinction event in the absence of marine anoxia. Geology 32:805808.
Vrba, E. S., and DeGusta, D.. 2004. Do species populations really start small? New perspectives from the Late Neogene fossil record of African mammals. Philosophical Transactions of the Royal Society of London B 359:285293.
Wagner, P. J., Kosnik, M. A., and Lidgard, S.. 2006. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:12891292.
Wang, X. D., and Sugiyama, T.. 2000. Diversity and extinction patterns of Permian coral faunas of China. Lethaia 33:285294.
Weidlich, O. 2002. Permian reefs re-examined: extrinsic control mechanisms of gradual and abrupt changes during 40 my of reef evolution. Geobios 35:287294.
Wilson, G. P. 2014. Mammalian extinction, survival, and recovery dynamics across the Cretaceous–Paleogene boundary in northeastern Montana, USA. Pp. 365392. in G. P. Wilson, W. A. Clemens, J. R. Horner, and J. H. Hartman, eds. Through the end of the Cretaceous in the type locality of the Hell Creek Formation in Montana and adjacent areas. Geological Society of America, Boulder, Colo.
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Evolutionary rates of mid-Permian tetrapods from South Africa and the role of temporal resolution in turnover reconstruction

  • Michael O. Day (a1), Roger B. J. Benson (a2), Christian F. Kammerer (a3) and Bruce S. Rubidge (a1)

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