Estimates of the magnitudes of major marine mass PNAS PLUS extinctions in earth history Steven M. Stanleya,1 aDepartment of Geology and Geophysics, University of Hawaii, Honolulu, HI 96822 Contributed by Steven M. Stanley, August 8, 2016 (sent for review June 7, 2016; reviewed by David J. Bottjer and George McGhee Jr.) Procedures introduced here make it possible, first, to show that Another model of Foote (5) based on expected forward survivor- background (piecemeal) extinction is recorded throughout geo- ship also produced a large Signor–Lipps effect, as well as intervals logic stages and substages (not all extinction has occurred with no actual extinction whatever, but it was oversimplified in suddenly at the ends of such intervals); second, to separate out using average overall extinction rates for marine taxa. Melott and background extinction from mass extinction for a major crisis in Bambach plotted percentage of extinction for marine taxa at the earth history; and third, to correct for clustering of extinctions genus level for stages and substages against the lengths of these when using the rarefaction method to estimate the percentage of intervals (6). They found no correlation, and concluded that species lost in a mass extinction. Also presented here is a method background extinction has been minimal. There were two problems for estimating the magnitude of the Signor–Lipps effect, which is here. One was that intervals exhibiting mass extinctions were not the incorrect assignment of extinctions that occurred during a cri- excluded. The second was that the regression was not forced sis to an interval preceding the crisis because of the incomplete- through zero. When these two measures are taken, there is, in fact, ness of the fossil record. Estimates for the magnitudes of mass a strong correlation between interval length and percentage of extinctions presented here are in most cases lower than those extinction, indicating that there has been a significant amount of previously published. They indicate that only ∼81% of marine spe- background extinction during the Phanerozoic (Fig. 1A;seeSI Text cies died out in the great terminal Permian crisis, whereas levels of for excluded mass extinctions). This is not to deny that some back- 90–96% have frequently been quoted in the literature. Calcula- ground extinctions may have occurred in small pulses, but not nec- tions of the latter numbers were incorrectly based on combined essarily simultaneously. Despite the high level of R for the regression data for the Middle and Late Permian mass extinctions. About 90 for this plot (boldfaced to distinguish it from R, the symbol used here EARTH, ATMOSPHERIC, orders and more than 220 families of marine animals survived the forrateofchangeofdiversity),thevarianceinFig.1A is quite high AND PLANETARY SCIENCES terminal Permian crisis, and they embodied an enormous amount (see Table 1 for definitions of symbols). A major factor here is the of morphological, physiological, and ecological diversity. Life did well-known decline for rates of extinction in the marine realm from not nearly disappear at the end of the Permian, as has often the early Paleozoic to the late Cenozoic: a roughly threefold decline been claimed. for non-mass-extinction intervals (Fig. 1B). In effect, these rates were collapsed onto a single axis in the production of Fig. 1A. mass extinction | paleontology | biodiversity In fact, taxa such as Cambrian trilobites (7) and Triassic conodonts (8) that experienced very high extinction rates and global mass extinction can be defined qualitatively as an had excellent fossil records that have been studied in detail have Aevent in which an unusually large percentage of higher taxa been clearly shown to have experienced much background ex- in several biological groups died out globally within a brief in- tinction during formally recognized intervals (ones representing terval of geologic time. There is no satisfactory way to provide a substages and stages). Furthermore, throughout the stratigraphic universally applicable quantitative definition of a mass extinc- record many zones within substages and stages are formally de- tion. Major marine mass extinctions have been associated with fined by the disappearance of a single species or genus, not by relatively abrupt excursions of the stable carbon isotope ratio in clusters of extinctions. seawater, as reflected in fossil skeletal material. Contempora- neous oxygen isotope excursions that have paralleled the carbon Significance isotope excursions, as well as other forms of evidence, connect the biotic crises to global climate change and support other ev- This paper shows that background extinction definitely pre- idence that the crises were relatively sudden events (1). Most ceded mass extinctions; introduces a mathematical method for major pulses of extinction occurred at or near the ends of for- estimating the amount of this background extinction and, by mally recognized geologic intervals. In fact, the resulting biotic subtracting it from total extinction, correcting estimates of transitions have led to the establishment of the boundaries be- losses in mass extinctions; presents a method for estimating tween most geologic systems and many geologic stages. Any the amount of erroneous backward smearing of extinctions extinctions scattered within such an interval or within an inter- from mass extinction intervals; and introduces a method for val not containing a mass extinction are known collectively as calculating species losses in a mass extinction that takes into background extinction. account clustering of losses. It concludes that the great termi- Comparing models to empirical numbers, Foote (2) considered nal Permian crisis eliminated only about 81% of marine species, two extreme scenarios for extinctions in the marine realm: one in not the frequently quoted 90–96%. Life did not almost disap- which all extinctions occurred in pulses, primarily at the ends of pear at the end of the Permian, as has often been asserted. geologic ages (the intervals representing stages) and one in which they were spread throughout ages (see also ref. 3). He found the Author contributions: S.M.S. designed research, performed research, analyzed data, and pulsed model to be more strongly supported, which would imply wrote the paper. that substantial backward smearing of extinctions occurred because Reviewers: D.J.B., University of Southern California; and G.M., Rutgers University. of the incompleteness of the fossil record [the Signor–Lipps effect The author declares no conflict of interest. (4)]. As I will show here, there is evidence that this result reflects Freely available online through the PNAS open access option. an intermediate situation: the occurrence of a large percentage of 1To whom correspondence should be addressed. Email: [email protected]. extinctions as pulses at the ends of recognized stratigraphic inter- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. vals following a considerable amount of background extinction. 1073/pnas.1613094113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1613094113 PNAS | Published online October 3, 2016 | E6325–E6334 Downloaded by guest on October 4, 2021 A B Fig. 1. Strong correlation between lengths of stratigraphic intervals and the percentages of total marine genera that became extinct within them (A)and Phanerozoic decline of extinction rates for marine genera (B). Included intervals range from the late Llanvirnian (Middle Ordovician, following the early Paleozoic interval of very high extinction rates) through the Messinian (late Miocene). Intervals characterized by mass extinctions are excluded (SI Text). There is another very important point. Not all extinctions have denoted by N). The third error of the traditional e/D calculation resulted from global or regional changes in the physical envi- is that it fails to take into account the Signor–Lipps effect. The ronment. Adverse biotic interactions have certainly caused many impact of this omission is also illustrated in Fig. 2. piecemeal extinctions. For example, the impact of a group of The approach introduced here employs a technique for esti- highly efficient, newly evolved predators on prey that are readily mating the number of background extinctions for a particular accessible to them will often have caused extinctions that were MEI and, from this, the standing diversity at the start of the mass not clustered but spread over millions of years. This is a matter extinction. These numbers make it possible to estimate the of extinction by attrition, which is quite different in temporal magnitude of the mass extinction appropriately. The same pattern from the lethal impact of a sudden physical catastrophe. technique makes it possible to evaluate the magnitude of the The numerical size of a mass extinction has commonly been Signor–Lipps effect at the stage or substage level. It is highly calculated as the ratio between the total number of extinctions of significant that the methodology is independent of the duration genera or families (e) for the mass extinction interval (MEI) and of the MEI. In other words, any future alteration of the esti- the total number of such taxa that existed during the interval (D) mated duration of an MEI will have no effect on the calculation (9–11). This convention suffers from three errors. First, it ignores of the impact of a crisis. The methodology yields estimates of that fact that during an MEI many taxa will have died out not as percentages of genera lost in marine mass extinctions that in part of the mass extinction but as background extinction that most cases are lower than conventional estimates. took place throughout the interval, as it does during intervals not Rarefaction curves have been used to estimate the number of characterized by mass extinctions (Fig. 1). Fig. 2 illustrates how, species lost in the terminal Permian mass extinction (9, 12). The by including background extinction, the use of e erroneously results exaggerated the impact of the event, however, because to exaggerates the number of taxa lost in a mass extinction.