Paleobiology, 30(4), 2004, pp. 522–542

Origination, , and mass depletions of marine diversity

Richard K. Bambach, Andrew H. Knoll, and Steve C. Wang

Abstract.—In post- time, five events—the end-, end- in the Late De- vonian, end-, end-, and end-—are commonly grouped as the ‘‘big five’’ global intervals of mass extinction. Plotted by magnitude, extinction intensities for all substages show a continuous distribution, with the five traditionally recognized mass located in the upper tail. Plotted by time, however, proportional extinctions clearly divide the Phan- erozoic Eon into six stratigraphically coherent intervals of alternating high and low extinction in- tensity. These stratigraphic neighborhoods provide a temporal context for evaluating the intensity of extinction during the ‘‘big five’’ events. Compared with other stages and substages in the same neighborhood, only the end-Ordovician, end-Permian, and end-Cretaceous extinction intensities appear as outliers. Moreover, when origination and extinction are considered together, only these three of the ‘‘big five’’ events appear to have been generated exclusively by elevated extinction. Low origination contributed more than high extinction to the marked loss of diversity in the late Fras- nian and at the end of the Triassic. Therefore, whereas the ‘‘big five’’ events are clearly times when diversity suffered mass depletion, only those at the end of the Ordovician, Permian, and Cretaceous periods unequivocally qualify as globally distinct mass extinctions. Each of the three has a unique pattern of extinction, and the diversity dynamics of these events differ, as well, from the other two major diversity depletions. As mass depletions of diversity have no common effect, common cau- sation seems unlikely.

Richard K. Bambach and Andrew H. Knoll. Botanical Museum, , 26 Oxford Street, Cambridge, Massachusetts 02138. E-mail: [email protected] Steve C. Wang. Department of Mathematics and Statistics, Swarthmore College, 500 College Avenue, Swarthmore, Pennsylvania 19081. E-mail: [email protected]

Accepted: 15 February 2004

Introduction: five’’ mass extinctions. Each had been noted Mass versus ‘‘Background’’ Extinction earlier by Newell (1967). Raup and Sepkoski plotted the extinction The idea that mass extinctions stand out as rate (number of families going extinct per mil- a class of events separate from the range of ) for each in time order and as- ‘‘normal’’ or ‘‘background’’ extinctions that sumed that apparent outliers on the arithme- characterize most of the geological record tic plot were true statistical outliers (and not originated with the work of Norman Newell aberrations produced by errors in the time- (1962, 1963, 1967) and crystallized through scale), thus identifying a distinct class of mass the quantitative analysis by Raup and Sepko- extinctions. They also calculated a 95% confi- ski (1982). Using Sepkoski’s compilation of dence interval around the remaining ‘‘back- stratigraphic ranges temporally resolved to ground’’ extinction stages and demonstrated the stage level for marine families of all - a secular decrease in extinction rates over mal taxa (Sepkoski 1982), Raup and Sepkoski time. Quinn (1983), however, showed that the identified five mass extinctions: the end-Or- extinction data were highly skewed and cor- dovician (Ashgillian); Late (includ- rectly pointed out that the assumption of a ing the Frasnian/ boundary); end- normal distribution for ‘‘background’’ extinc- Permian ( and Djhulfian togeth- tion data was not valid. When log-trans- er); end-Triassic (Late or ); formed, the distribution of extinction rates and end-Cretaceous (). These was approximately normal and did not have a have become known informally as ‘‘the big suite of outliers that could be categorized un- ambiguously as a class of mass extinctions * This paper is dedicated to the memory of Stephen Jay separate from the overall ‘‘background’’ dis- Gould (1941–2002). tribution. Bambach and Gilinsky (1986) dem-

᭧ 2004 The Paleontological Society. All rights reserved. 0094-8373/04/3004-0003/$1.00 ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 523 onstrated that this was also the case for several ly into intensities of background extinction. other extinction metrics, including propor- Although continuity of magnitude appears to tional metrics by interval that are not subject have been demonstrated by Quinn (1983) and to time-scale error. For all metrics the distri- Bambach and Gilinsky (1986), and was as- bution of extinction intensity grades smoothly sumed by Raup (1991) in his kill curve anal- from lowest to highest values with no discrete ysis for the Phanerozoic, several factors led us break between ‘‘background’’ and presumed to reconsider the status of these intervals. mass extinction intervals. Indeed, Raup (1991) These include (a) the rarity of the largest ex- developed his view of the Phanerozoic kill tinction intensities, (b) the possibility that they curve on the basis of this continuity of extinc- do not share continuity of cause or effect with tion magnitudes. Bambach and Gilinsky all other intervals, and (c) the fact that origi- (1986) did, however, support the finding that nation and extinction have rarely been consid- extinction intensities (and origination inten- ered together in examining patterns of diver- sities, as well) declined during the Phanero- sity change. zoic, a conclusion discussed more fully by Gil- In the following sections, we reevaluate the insky (1994). continuity or discontinuity of magnitude and Despite the evidence that intensities of ex- then briefly consider whether events that tinction form a continuum, the five events might be regarded as mass extinctions can be specified by Raup and Sepkoski (1982) contin- unified by effect or cause. We test whether any ue to be labeled ‘‘mass extinctions’’ (Finney et of the ‘‘big five’’ events are differentiable from al. 1999; McGhee 2001; Wignall and Twitchett the distribution of other extinction intensities, 1996; Pa´lfy et al. 2000; MacLeod and Keller explore the role of origination as well as ex- 1996). Current threats to have tinction in diversity changes associated with even been labeled ‘‘the sixth extinction’’ (Lea- these five intervals, and comment on the dif- key and Lewin 1995). It may be that magni- ferences, as well as similarities, among the in- tude alone is sufficient to justify the term tervals. The upshot will be that although the ‘‘mass extinction’’ because events with such five intervals in question—the end-Ordovi- pronounced loss of diversity are rare, with cian, Late Devonian, end-Permian, end-Trias- waiting times of about 100 million years (Raup sic, and end-Cretaceous—are the five intervals 1991). But is there any reason to think of these with the greatest diversity loss in the Phan- events as a separate class of events, rather than erozoic, they share little else in common. Only as the uncommon upper tail of a continuous three were driven predominantly by extinc- distribution? tion and even they display distinctly different Wang (2003) recently identified three con- patterns of diversity change, implying that cepts that must be considered individually these events are not related by continuity of when we ask whether putative mass extinc- effect or cause. tions grade continuously into the range of background extinction: continuity of cause, Tracking Genus Diversity continuity of effect, and continuity of magni- tude. Continuity of cause would be demon- Figure 1 illustrates the history of marine ge- strated if candidate mass extinctions could be nus diversity through Phanerozoic time. The shown to be driven by the same processes that data were compiled by using a computerized are responsible for background extinction, al- sorting routine written by Jack Sepkoski and beit operating at increased intensity or over modified by J. Bret Bennington to tabulate ge- larger areas. Continuity of effect would be es- nus diversity for 107 stages and substages us- tablished if background and mass extinctions ing Jack Sepkoski’s unpublished tabulation of exhibited common patterns of selectivity on the stratigraphic ranges of genera as of 1996. taxonomic, functional, ecological, or other Although the Paleontological Research Insti- grounds. And continuity of magnitude would tution has recently published the raw genus exist if the distribution of intensities of mass ranges from a later version (1998) of Sepko- extinctions graded smoothly and continuous- ski’s compilation (Sepkoski 2002), this publi- 524 RICHARD K. BAMBACH ET AL.

FIGURE 1. Diversity and diversity turnover of marine genera by interval through the Phanerozoic. The five major post-Cambrian diversity depletions are highlighted. The heavy line connects the data on number of genera crossing each interval boundary. The line directly connecting the numbers of boundary-crossing genera follows the path of minimum likely standing diversity, regarded as the minimum diversity because origination and extinction would have to work in exact lock-step to follow that diversity path. The peaked dotted line represents genus turnover within each interval. The rising part of each peak represents all genus originations (first occurrences) reported from the interval. The peak records the total number of genera reported from the time interval. The descending part of the peak represents the number of extinctions (last records) of genera in the interval. The magnitudes of the peaks compared with the minimum standing diversity at interval boundaries represent the degree of faunal turnover in the intervals. cation simply lists all the genera and does not within each interval, the apparent numerically tabulate the data on diversity. increase in diversity is proportionately greater Genus diversity follows the general pattern than that illustrated by Sepkoski for families. established in the ‘‘consensus paper’’ of Sep- There are some concerns that the apparent- koski et al. (1981) and best known from Sep- ly large Cenozoic increase in diversity may be koski’s (1981: Fig. 5) widely reproduced fam- partly artifactual. However, recent analyses ily diversity curve. In the we see the (Bush and Bambach in press on alpha diver- ‘‘’’ (the increase in diver- sity; Jablonski et al. 2003 on Pull of the Recent; sity in the Early Cambrian), a Middle and Late and Bush et al. 2001, in press on techniques of Cambrian ‘‘plateau’’ of diversity, and the Or- sample-standardization) demonstrate that an dovician , followed by the long in- increase in Cenozoic diversity is strongly in- terval of fluctuating, but non-trending, diver- dicated, although the exact amount is still un- sity that began in the Caradocian and lasted clear (Jackson and Johnson 2001). The ‘‘con- for the rest of the . Diversity changes dur- sensus paper’’ (Sepkoski et al. 1981) was put ing this ‘‘Paleozoic Plateau’’ include three of together because several of the data sets avoid- the ‘‘big five’’ diversity depletions, the end- ed or mitigated some of the biases, such as im- Ordovician, the Late Devonian, and the end- perfections of the geologic record, that were of Permian events. The post-Paleozoic is charac- concern then and still are (Peters and Foote terized by nearly continuous diversity in- 2001). Although every potential problem crease, interrupted by the other two ‘‘big five’’ should be analyzed and improvement in the diversity depletions, the end-Triassic and the data is necessary, it still appears, as was con- sharp, era-bounding end-Cretaceous events. cluded then, that the diversity signal is stron- Note that because we tabulated subgenera of ger than the noise. mollusks, resolved the data to the substage Figure 1 accounts for all the data in the Sep- level, and emphasized the diversity at interval koski genus compilation (see caption for full boundaries rather than the total diversity explanation). Many diversity curves use total ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 525 diversity as the recorded data (this is true for masked by an increase in origination in the published illustrations of Sepkoski’s family next. Total diversity might appear unchanged curve, for example). If one mentally ‘‘connects between the two intervals because origination the dots’’ of total diversity peaks in Figure 1, in a rapid recovery from an it is clear that the general shape of a curve con- could make total diversity in the succeeding necting total diversities would be very similar interval equal to that in the previous one, con- to the boundary-crossing diversity empha- cealing the low diversity at the start of the in- sized here. Mid-Devonian diversity would ap- terval. For example, although extinction ex- pear higher than Late Ordovician diversity, ceeded origination in each of the last two in- diversity would fluctuate more, tervals of the and diversity appears to and the upturn in diversity in the mid-Cre- have been lost between the Ludlovian and Pri- taceous would be sharper than shown by the dolian when looking at total diversity, the low standing diversity plot. The general pattern, point of diversity at the end of the Silurian however, would be the same. (end-Pridolian) is masked in the total diver- We use the boundary-crossing standing di- sity curve because, in the Gedinnian, the first versity as the preferred representation of di- interval of the Devonian, origination was high, versity and diversity change through time. We causing total diversity to exceed that of the know that boundary-crossing diversity is not Pridolian. Boundary-crossing diversity not anomalous compared with total diversity be- only approximates standing diversity, but it cause the trend of boundary-crossing diversi- also gives a clearer representation of the con- ty follows the general path of total diversity. sequences of within-interval evolutionary dy- Two factors make us prefer it to total diver- namics than that provided by summed total sity. First, it is the only measure we have of diversity data for whole intervals. actual standing diversity. Total diversity in an interval was not the actual standing diversity The ‘‘Big Five’’ as Diversity Depletions at any time because it is unlikely that all orig- Inspection of Figure 1 reveals that, although inations occurred in an interval before any ex- diversity decreased slightly on several other tinction. However, the recorded diversity at occasions, there are only five post-Cambrian the boundaries of each interval, calculated by intervals when diversity decreased markedly: subtracting all extinctions in the interval from (1) at the end of the Ordovician, (2) during the the total diversity in the interval, is a direct Middle and Late Devonian, (3) during the Late measure of standing diversity at interval Permian, (4) at the end of the Triassic, and (5) boundaries. The other compelling reason is at the end of the Cretaceous. The end-Triassic that change in diversity is shown best by com- decrease does not look as large as the other paring diversity at the start of different inter- four, but standing diversity throughout the vals. Triassic was lower than at any other time after Diversity is a function of both origination the mid-Ordovician, so the proportional de- and extinction. The peaks of turnover within crease in the latest Triassic is quite compara- each interval in Figure 1 reveal how much var- ble to the other four major diversity deple- iation of diversity can occur in any interval, tions. Two Cambrian intervals are also noted but comparing standing diversities at interval on Figure 1 (the late Botomian [LB] and early boundaries tells us whether origination and late Middle Cambrian [ELM]). These were extinction are in balance (little or no change of times of relatively small numerical change in diversity from one boundary to the next) or diversity but high proportional diversity loss. whether either origination or extinction dom- Because the evolutionary dynamics of the inated during an interval (origination domi- Cambrian and Early Ordovician are unusual nating if boundary-crossing diversity increas- we will consider them separately; the bulk of es, extinction being more important if bound- this paper emphasizes the post- por- ary-crossing diversity decreases). In plots of tion of the Phanerozoic. total diversity, a predominance of extinction Because it is hard to judge the proportional over origination in one interval could be magnitude of diversity change from a plot of 526 RICHARD K. BAMBACH ET AL.

FIGURE 2. Proportion of gain or loss of genus diversity from the Caradoc to the Plio-. The five major diversity depletions (decrease greater than 20%) are numbered. Symmetrical lines are drawn at Ϫ13.5% and ϩ13.5% (based on the sixth largest diversity decrease) to indicate the range that might be regarded as ‘‘background’’ fluc- tuation in diversity. Intervals with greater than 13.5% diversity increase are common only after major diversity depletions. absolute values, a plot of proportion of gain or number (the change in the number of genera loss of diversity, rather than a plot of the num- from the start to the end of the interval) by the bers of genera as such, is desirable. A display number of genera at the start of the interval. of numbers of taxa, as in Figure 1, is useful for For example, if 500 genera pass from interval illustrating the pattern of change in diversity, one to interval two and 600 genera pass from but the numbers represent only those taxa dis- interval two to interval three, then there were covered in the record and are not a com- 100 more originations than extinctions during plete record of all the taxa that existed. Pro- interval two, with a gain in diversity of 100 portional diversity change is what we seek to genera, a proportional increase of ϩ0.200. understand here—how episodes of diversity Likewise, a decrease from 600 to 500 genera loss affected the whole biota. The question, in during an interval (a loss of 100 genera as a effect, concerns the importance of an event in result of 100 more extinctions than origina- the context of its time, not just how many taxa tions) would be a proportional decrease of were involved. Ϫ0.167. As noted above, an advantage of de- Figure 2 shows the proportional gain or loss termining standing diversity at interval in the number of genera during each stage or boundaries is that one can follow the balance substage interval, starting with the Early Car- of origination and extinction as it influences adocian in the Middle Ordovician after the diversity change, something not possible large proportional increases in diversity as- when only tabulating total diversity for each sociated with the Cambrian Explosion and the interval. were over. The change Figure 2 shows that the five intervals al- in diversity is calculated as a proportional ready well known as the classic ‘‘big five’’ change by subtracting the number of genera at mass extinctions (with the Guadalupian as the start of each interval (the standing diver- well as the end-Permian Djhulfian included in sity at the boundary between the interval and the major later Permian diversity decrease its preceding interval) from the number of [Stanley and Yang 1994]) are the only post- genera at the end of the interval (the standing Llandeilian intervals with more than a 20% diversity at the boundary between the interval proportional loss of genus diversity. In fact, and its succeeding interval) and dividing that there is a gap of 8% between the largest loss ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 527 of diversity not included in the ‘‘big five’’ and first for the whole Phanerozoic and second for the smallest loss within the ‘‘big five,’’ but no the time after the after the ‘‘Cambrian Pla- gaps of as much as 2% occur between any teau’’ of low diversity and high turnover. (2) smaller values when arranged in rank order. We compared magnitudes of extinction for These five intervals were certainly times of each interval against the distribution of mag- mass depletion of diversity, but can we justify nitudes of extinction in the particular segment regarding any of them as times of mass ex- of the timescale, based on average high or low tinction different in cause, effect, or magni- extinction rates, to which the interval belongs. tude from ‘‘background’’ extinction? Only if an interval satisfies both criteria, that is, if the interval is not part of a continuous Large-Magnitude Proportional Increases smooth distribution of magnitudes, and if the in Diversity interval also appears as an ‘‘outlier’’ in mag- As a side issue, but one related to propor- nitude compared with the other intervals in tional diversity change and its timing, it is in- its particular segment of the timescale, do we teresting to note that the only times when pro- regard it as a ‘‘true’’ global mass extinction, portional increase of diversity exceeds 13.5% different in magnitude from the bulk of as- are during the Cambrian Explosion, the Or- sociated stratigraphic intervals. dovician Radiation (just ending in the early How Continuous Are the Values of Extinction Caradocian at the start of Fig. 2), in the im- Intensity? As noted above, several analyses mediate aftermath of each of the five ‘‘mass have concluded that the distribution of extinc- depletions’’ of diversity, and briefly (single in- tion intensities is apparently continuous tervals only) in the (Turoni- (Quinn 1983, Bambach and Gilinsky 1986, an) and (early ) (Fig. 2). Al- Raup 1991, Wang 2003). Figure 3A shows this though origination rates are not unusually effect for proportion of genus extinction ar- high in these intervals (no outliers for origi- ranged in rank order for the 107 stages and nation are found in an analysis of origination substages of the Phanerozoic as tabulated in proportions at these times), the combination our version of Sepkoski’s genus database. of higher origination and lower extinction Cambrian and Early Ordovician extinction during the ‘‘recovery’’ phase after diversity proportions, however, were consistently high depletion does mark these intervals as times (Table 1, Fig. 4). Sixteen of 19 Cambrian and of unusually great proportional increase in di- Early Ordovician intervals have extinction in- versity. These are not necessarily times of tensities that fall within the top quartile of all broad transgression or otherwise better rep- Phanerozoic intervals (Fig. 3A). Origination resentation of the marine record, so higher was unusually high, as well, during this in- origination rates in the wake of major diver- terval. Thus, whereas taxonomic turnover at sity depletions may reflect recovery from un- the genus level was great, overall diversity did usually low diversity and not just the effect of not fluctuate wildly (Fig. 1 and discussion be- improved record availability, a possibility low). These turnover rates are not like those of raised by Peters and Foote (2001). much of the later Phanerozoic. For example, the decrease in proportion of extinction ob- Testing for Continuity of Magnitude served in the Early Ordovician (Fig. 4A) was of Extinction not produced by the radiation of taxa with We tested for continuity or discontinuity of lower extinction rates diluting continuing magnitude of extinction (i.e., whether or not high extinction rates in the , which the distribution of intensities of apparent dominated Cambrian diversity. Instead, ex- mass extinctions grade smoothly and contin- tinction proportions for trilobites, which had uously into intensities of background extinc- consistently exceeded those of the non-trilo- tion) in two ways. (1) We tested whether there bite from the origin of the in the is a smooth continuous distribution of mag- early Atdabanian though the early Arenigian nitudes of extinction intensity with no strong (Foote 1988), dropped to the same level as variation in the upper tail of the distribution, non- proportions of extinction during 528 RICHARD K. BAMBACH ET AL.

FIGURE 3. Proportions of genus extinction arranged in rank order by magnitude. A, All 107 intervals of the Phan- erozoic. Magnitudes from the Cambrian and Early Ordovician are highlighted. B, Middle Ordovician to Plio-Pleis- tocene values only. Higher magnitude intervals are labeled. the Late Arenigian and remained at compa- brian and Early Ordovician, even when pro- rable levels thereafter (Fig. 4C). Clearly some- portions of extinction increased for extended thing changed for trilobite evolutionary dy- intervals, such as from the Middle Silurian to namics in the later part of the Early Ordovi- the mid-Carboniferous—this held for trilo- cian. Although the change was not as dramatic bites and non-trilobites alike. for the non-trilobite fauna, extinction propor- We do not yet understand why turnover tions for that fraction of the fauna, which had rates should have been so high during the been over 30% in two-thirds of the intervals of Cambrian and Early Ordovician. Perhaps ear- the Cambrian and Early Ordovician, dropped ly were more vulnerable to extinction to levels below 30% and remained low until for functional reasons—many Cambrian ani- the Middle Silurian, except for the end-Or- mals belonged to stem rather than crown dovician late Ashgillian extinction event. Pro- groups of bilaterian phyla and classes (Budd portions of extinction never returned consis- and Jensen 2000). Perhaps the low diversity of tently to the high levels common in the Cam- Cambrian and Early Ordovician animals con- ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 529 — 0.569 0.347 0.468 0.474 Omitted extinction* 0.556 0.686 proportions of 0.644 0.273 0.389 0.222 0.452 0.253 ion. extinction Maximum proportion of 0.460 0.174 0.287 0.128 0.341 0.123 Mean extinction* proportion of r interval. The means for proportion of extinction are calculated by eneral magnitude of extinct 0.270 0.114 0.191 0.054 0.281 0.043 extinction Minimum proportion of 0.695 0.406 0.441 0.315 0.563 0.328 Maximum origination proportion of 0.539 0.245 0.286 0.157 0.413 0.185 tion of origination* mitted proportions of extinction are listed in the column at the far right. They are those for the late Ashgillian (Ordovician), Mean propor-

FIGURE 4. Genus extinction by interval in stratigraphic

0.268 0.133 0.155 0.044 0.211 0.085 (time) order. A, Proportion of genus extinction. The depletions. The o Minimum

origination Cambrian and Early Ordovician concentration of very proportion of high proportions is highlighted. That concentration is further emphasized because only six of the 88 post-Ar- enigian intervals rise above the dashed horizontal line at 40% genus extinction. B, Natural logarithms of the 6

19 11 18 14 39 proportion of genus extinction. Intervals of generally

intervals high or low proportion of extinction are emphasized by contained Number of the fluctuation of the majority of points within blocks of time intervals above and below the horizontal line drawn at the lowest proportion in the Cambrian and Late Ordovician. Those large-scale long-term fluctua- tions are, of course, also visible in the plot of proportions (Fig. 4A). The dashed line is as in Figure 4A (the natural log of 40% genus extinction). Intervals identified in Fig- ure 5 as forming a group of outliers (the late Ashgillian in the Ordovician, the Guadalupian and Djhulfian at the end of the Permian, and the Maastrichtian at the end of the Cretaceous) are highlighted. C, Proportion of genus extinction of trilobites and non-trilobites during the Cambrian and Ordovician (except the end-Ordovician).

Major interval Note the shift of trilobites to magnitudes similar to non- trilobites during the last two intervals of the Early Or- the stage or substage intervals associated with the ‘‘big five’’ diversity 1. Data on proportions of origination and extinction for major intervals of the Phanerozoic based on g dovician and the lower proportions of all after that. * The means for proportion of origination are calculated by using the proportions of origination from all the stage and substage intervals in each majo ABLE T Cambrian & Early Ordovician Middle Ordovician–Early Silurian Mid Silurian–Early Carboniferous Late Carboniferous and Permian Triassic through Pleistocene omitting late Frasnian (Devonian), Guadalupian and Djhulfian (Permian), late Norian plus Rhaetian (Triassic), and Maastrichtian (Cretaceous). 530 RICHARD K. BAMBACH ET AL. tributed to low stability (Bambach would increase the coefficient of skewness to et al. 2002); many modes of life now heavily such an extent (p Ͻ 0.0001, calculated by sim- occupied were either vacant or contained few ulation). The sparseness of the remaining high taxa (Bambach 1983, 1985). Or perhaps phys- values raises the question of whether those ical environments experienced unusual per- magnitudes are actually outliers that can be turbation during this interval, as might be in- regarded as a separate group from the bulk of ferred from the carbon isotope record (Brasier lower values. and Sukhov 1998; Saltzman et al. 2000). Do All Intervals That Appear Discontinuous Whether we know the cause or not, the ob- with the Bulk of Post-Arenig Intervals Form a served patterns of turnover show that Cam- Group of Outliers When Compared with Their ‘‘Lo- brian and Early Ordovician extinction rates cal’’ Segment of Geologic Time? We can test di- form a distinct stratigraphic grouping that dif- rectly for the continuity of magnitude be- fers from the remainder of the Phanerozoic tween background and potential mass extinc- Eon. Statistically, it is extremely unlikely that tions in a temporal context. Because the focus the proportion of extinction in as many as 16 of this paper is on the ‘‘big five’’ mass deple- of the 19 Cambrian and Early Ordovician in- tions, which are all post-Arenig in age and be- tervals would fall within the top quartile of all cause the Cambrian and Early Ordovician are Phanerozoic values if there were nothing un- not comparable in evolutionary dynamics (for usual about that segment of time (p ϭ whatever reason, as noted above), we restrict- 0.000000002, calculated by using the hyper- ed the following analysis to the post-Arenig geometric distribution). Thus, we removed portion of the Phanerozoic. these data and replotted the distribution of ex- We tested for continuity of magnitude be- tinction intensities. tween background and mass extinctions over The resulting rank order distribution of the 88 post-Arenig intervals. To control for the mid-Ordovician to Recent extinction intensi- fluctuation in regimes appar- ties (Fig. 3B) retains the original smoothly ent in the grouping of intervals in Table 1 (for continuous appearance except for six intervals which the boundaries were chosen where the at the upper end: four of the ‘‘big five’’ (the change in extinction proportions seen in Fig. end-Ordovician, end-Permian, end-Triassic, 4 were greatest) we used time-adjusted data and end-Cretaceous) and the two intervals rather than the raw extinction intensities. To that bracket the terminal Permian interval. do this, we first fit a smooth lowess curve to The high Guadalupian intensity just before the raw extinction intensities (Fig. 5A). Low- the end-Permian Djhulfian likely combines ess (‘‘Locally Weighted Scatterplot Smoother’’ true extinction (Stanley and Yang 1994; Jin et [Cleveland 1979]) is a nonlinear regression al. 2000) with Signor-Lipps range truncations method that smoothes out the noise in a time (Signor and Lipps 1982; Jablonski 1986; Raup or scatterplot in order to emphasize the 1987) from the exceptionally severe end-Perm- signal. To use lowess, one must first choose the ian event. The initial Triassic interval (the In- value of a ‘‘bandwidth’’ parameter controlling duan) was a time of low diversity following the degree of smoothing. We used a band- the end-Permian devastation, and the cause of width of 11%, meaning that the smoothed val- its high extinction intensity has yet to be de- ue for each interval is calculated as a weighted termined. average of 11% of the surrounding intervals, The distribution of extinction intensities for with the intervals closest in time weighted the post-Arenig (Fig. 3B) still can be regarded more heavily. We chose this value because the as a continuous distribution, but one that is average length of a geologic time period in the more skewed than that for the entire Phaner- 470 million years after the Arenig is 52 million ozoic—the coefficient of skewness for the total years, and 11% of 470 million is 52 million. Phanerozoic was 0.89 whereas that for the Thus the smoothed value for each interval post-Arenig is 1.37. However, it is extremely takes into account the extinction intensities of unlikely that removing 19 randomly selected the surrounding intervals for a time equiva- intervals (consecutive or non-consecutive) lent to a . ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 531

On the other hand, a bimodal extinction in- tensity curve would suggest that background and mass extinctions are discontinuous in magnitude. The critical bandwidth test esti- mates the shape of the extinction intensity curve and tests whether there is significant ev- idence to reject the null hypothesis that the curve is unimodal. We found statistically sig- nificant evidence (p ϭ 0.028) for the existence of a second mode in the right tail of the dis- tribution of extinction intensities (Fig. 5B). The four intervals that make up this second mode are, from highest to lowest, the Djhulfian, Maastrichtian, Upper Ashgillian, and Guad- alupian, confirming that only the end-Ordo- vician, end-Permian, and end-Cretaceous have extinction magnitudes that would not be expected in their local context and are not part of a continuum of extinction magnitudes. Pattern of Temporal Change in Proportion of Ge- nus Extinction. Figure 4 plots the proportion of extinction in each interval arranged in tem- poral order. Although the numerous high val- FIGURE 5. Statistical analysis of post-Arenig extinction magnitudes. A, Nonlinear lowess regression with 11% ues of extinction intensity in the early and mid (52-million-) bandwidth, revealing long-term fluc- Paleozoic and the consistently lower intensi- tuation in extinction intensities. B, Histogram of resid- ties in the Jurassic through Cenozoic produce uals from nonlinear lowess regression with intervals having intensities comprising a statistically significant the decline in extinction through the Phaner- second mode (p ϭ 0.028) identified. The and the ozoic recognized by Raup and Sepkoski (1982) upper Norian are the last two intervals at high end tail and discussed by Gilinsky (1994), that decline of the main mode (time-adjusted values of 0.168 and 0.204), but they still lie well below the range of the sec- is not monotonic. Instead, there are strati- ond mode (0.307–0.416). The late Frasnian time-adjust- graphically coherent intervals with generally ed value of 0.062 is only the twelfth highest in the main higher and lower proportions of extinction mode and is one of ten values in the second bin above the mode. that are highlighted in Figure 4. Indeed, when the Cambrian–Early Ordovician data are re- moved from consideration, it is not obvious We then calculated the residuals, the differ- that extinction intensities trend through time ence between each interval’s extinction inten- for the remainder of the Phanerozoic; rather sity and its lowess smoothed value. Using we see low intensities during the mid Ordo- these residuals, we applied the critical band- vician–Early Silurian (except for the late Ash- width test (Silverman 1981), previously used gillian), Late Carboniferous–mid Permian, by Wang (2003) to test for continuity of mag- and Jurassic to present (except for the end- nitude over the entire Phanerozoic. The idea Cretaceous) separated by discrete intervals of of this test, in this context, is as follows: Sup- high extinction intensities during the Middle pose there is a curve (i.e., a probability density Silurian–Early Carboniferous and later Perm- function) that models an underlying process ian–Triassic. In total, then, the Phanerozoic from which extinction intensities are gener- can be divided into six segments based on ated. If this extinction intensity curve were fluctuation in average extinction proportion unimodal, we would infer that mass extinc- per interval (Table 1, Fig. 4). Excluding the tions are the right tail of a continuum of ex- post-Arenig intervals whose extinction rates tinction intensities—that background and fall in a second mode in the lowess/critical mass extinctions are continuous in magnitude. bandwidth analysis described above, the six 532 RICHARD K. BAMBACH ET AL. segments are apparent by inspection (Fig. 4) they are still clearly higher than any of those and are responsible for the pattern seen in the proportions. However, the late Frasnian (in lowess regression in Figure 5A. Although the Late Devonian) and the late Norian/ origination does not have as sharp or distinct Rhaetian (at the end of the Triassic) had ex- a set of changes from high to low proportions, tinction proportions that do not appear as out- the values of proportion of origination gener- liers for the larger time segment to which each ally parallel the pattern for extinction (as will belongs, although the end-Triassic point is be seen in Fig. 6). higher than the others in the Triassic. These six stratigraphically coherent seg- Three, Not Five, Global Mass Extinctions. We ments provide another ‘‘neighborhood’’ con- conclude there is a class of statistically distinct text in which variation in origination and ex- global mass extinctions, but that it contains tinction may be more meaningfully judged, only three members: the end-Ordovician, end- rather than comparing individual intervals Permian, and end-Cretaceous. These results against the full range of values that accumu- parallel the conservative bootstrap statistical lated during the Phanerozoic. Although a lin- analysis of Hubbard and Gilinsky (1992), who ear regression on extinction proportions also found only these same three unambigu- through the Phanerozoic does have a negative ous high extinction magnitudes in their anal- slope, the decline in extinction rate over time ysis. is caused by three sets of fluctuation between The other two traditional mass extinction consistently higher and lower rates, with the intervals do not fulfill the criteria for unusual negative slope of a linear regression largely extinction effect. The late Frasnian satisfies determined by the anomalously high propor- none of the criteria: it falls within the smooth tions of the Cambrian and Early Ordovician continuum of post-Arenigian extinction mag- and the predominantly low rates since the Tri- nitudes, it is not one of the magnitudes in the assic. We make this observation to suggest that second mode of post-Arenigian magnitudes if the pattern of extinction over time is to be using Silverman’s critical bandwidth test, and characterized it would be best to model it as a it is not an apparent outlier among the mid- three-phase , not a monotonic function Silurian through Early Carboniferous extinc- (nor a two-phase system as suggested by Van tion magnitudes. The end-Triassic is some- Valen [1984]). what more ambiguous because it is one of the Using the stratigraphic groupings of inter- intervals in the ‘‘off track’’ high-end tail of the vals with similar extinction intensities (Table rank order distribution of post-Arenigian 1, Fig. 4), we see how the outlier intensities magnitudes. However, although it falls at the from the critical bandwidth test look within high end of the main mode in Figure 5B, the individual segments of time. We show this in end-Triassic event does not fall in the separate both the arithmetic plot (Fig. 4A) and con- mode confirmed by the Critical Bandwidth verting the proportions to natural logarithms Test, nor is it distinctly different from other (Fig. 4B). The end-Ordovician (late Ashgillian) Triassic extinction intensities. We do not claim and end-Cretaceous (Maastrichtian) points that the end-Frasnian and end-Triassic were are obvious outliers, falling in intervals of innocent of pulsed extinctions, but we do infer generally low proportions of extinction. If the that, by itself, extinction is insufficient to ex- later Permian points (Guadalupian and Djhul- plain the strong diversity depletion at these fian) are regarded as belonging with the rest times. of the Permian (which could be justified be- cause (a) their fauna is taxonomically a contin- The Interaction of Origination uation of the earlier Permian fauna and (b) as and Extinction will be noted below, the origination rates for Paleontologists have focused on mass ex- these two intervals remain in the range of the tinctions as important evolutionary events for earlier Permian) they, too, would be extreme the past quarter of a century or more, but with outliers, but if they are grouped with the ele- few exceptions (e.g., Cutbill and Funnell 1967; vated proportions characteristic of the Triassic Knoll 1989) they have paid less attention to ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 533

FIGURE 6. Proportions of both genus origination and extinction through the Phanerozoic. Intervals of diversity loss (extinction exceeding origination) are circled. The ‘‘big five’’ mass depletions are numbered. origination, the other term in the diversity diversity was depleted when extinction was equation. In general, origination has been a fo- greater than origination, and, conversely, di- cus of interest mostly for the early Paleozoic versity increased when origination exceeded (Knoll and Carroll 1999; Budd and extinction. Diversity loss during intervals Jensen 2000; Connolly and Miller 2001) and when origination rate was typical for the the recovery intervals following mass extinc- stratigraphic neighborhood can be ascribed to tions (Hart 1996). elevated extinction alone. On the other hand, The five intervals of diversity loss seen in diversity loss when extinction was not mark- Figures 1 and 2 have traditionally been re- edly higher than the average for its strati- garded as mass extinctions because extinction graphic neighborhood must reflect sup- must have exceeded origination for diversity pressed origination—attrition by inadequate to drop so markedly during those intervals. replacement. The intervals during which di- However, this focus on extinction ignores two versity decreased are circled on Figure 6 and conditions. One is that there is considerable the ‘‘big five’’ diversity depletions are num- genus extinction during any interval of time bered. Using the average proportion of origi- (over 90% of the intervals of the Phanerozoic nation and extinction for the larger intervals in have 8% or greater genus extinction), yet when which each of the ‘‘big five’’ diversity deple- diversity is maintained because extinction is tions falls (Table 1), we can calculate the pro- matched by origination we are not concerned portional influence (‘‘importance’’) of origi- about its magnitude. Second is that origina- nation compared with extinction on the loss of tion can fluctuate, yet origination is seldom diversity in each major diversity depletion tracked. If origination should fall below typi- (Table 2). cal values while extinction remained at its typ- During the end-Ordovician, end-Permian, ical level, diversity would decrease, yet no and end-Cretaceous diversity depletions, change in extinction intensity would have oc- rates of origination were slightly to markedly curred. How do the classic ‘‘big five’’ diversity greater than the average for their stratigraphic depletions reflect the interaction between neighborhoods, whereas extinction rates were origination and extinction? exceptionally high (Fig. 7). By this criterion, Interaction of Origination and Extinction in then, these three intervals can be regarded as Major Diversity Depletions. Figure 6 illus- true global mass extinctions because diversity trates both origination and extinction propor- depletion in each was driven entirely by ele- tions through the Phanerozoic. By definition, vated extinction. Indeed, had rates of origi- 534 RICHARD K. BAMBACH ET AL. 67 232 117 0.326 0.094 0.165 307 594 115 711 190 901 422 479 500 310 567 644 165 Ϫ 1211 0.341 0.380 1.375 0.589 0.411 0.211 0.468 0.413 Ϫ Ϫ Ϫ Ϫ Ϫ Triassic: Rhaetian late Norian/ 77 192 126 66 0.213 0.085 0.140 902 186 378 710 361 175 438 825 115 312 776 Ϫ 1088 1263 0.515 1.212 0.635 0.365 0.171 0.347 0.286 0.287 Ϫ Ϫ Ϫ Ϫ Ϫ Devonian: Low origination plus extinction late Frasnian 92 48 830 878 0.335 0.355 0.046 654 562 385 269 Ϫ Ϫ 2475 1484 1645 1440 1597 3129 3037 2744 1099 0.209 0.185 0.123 1.164 3.855 1.046 0.474 0.109 Ϫ Ϫ Ϫ Ϫ Ϫ Cretaceous: Maastrichtian able 1 31 101 402 0.579 0.627 0.266 119 641 220 861 591 270 371 760 521 239 110 751 481 110 Ϫ 0.157 0.256 0.686 0.128 0.172 1.849 5.373 1.266 Ϫ Ϫ Ϫ Ϫ Ϫ ctual proportion of extinction Permian: Djhulfian hanges that would have occurred if origination or extinction in each interval able 1. Exclusively elevated extinction able 1 and a 27 12 527 539 0.420 0.429 0.018 435 408 294 668 141 962 729 947 717 Ϫ Ϫ 1256 1691 1664 1397 0.257 0.569 0.245 0.174 0.112 1.066 3.272 1.018 Ϫ Ϫ Ϫ Ϫ Ϫ Ordovician: depletions and the c late Ashgillian *2) *2) ϩ ϩ enera rigination (*1/*1 xtinction (*2/*1 ntinuing on ntinuing on Cause of ring interval diversity loss ntinuing on oing extinct 2. Actual diversity changes during the ‘‘big five’’ diversity Proportion of genus origination No. of new genera Total genus diversity in interval Proportion of genus extinction No. of genera ente Mean proportion of originations forModel large no. interval of newDifference genera from actual no. ofModel new total g diversity Mean proportion of extinctions forModel large no. interval of extinctions Model no. of genera co Difference from actual continuing (*2) Model diversity change in interval Model proportional diversity change No. of genera g No. of genera co Diversity change in interval Proportion of diversity change Model no. of extinctions (useModel real no. PExt) of genera co Difference from actual continuing (*1) Model diversity change in interval Model proportional diversity change ABLE Proportional influence of e T Actual data Model using mean proportion of origination for appropriate large interval in T Model using actual total diversity and mean proportion of extinction for appropriate large interval in T Originations: ratio real/mean Extinctions: ratio real/mean Proportional influence of o had been the mean for the larger segment of time to which each is assigned in T ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 535

FIGURE 7. Relationship between origination and extinction for the three mass diversity depletions that are true mass extinctions. Arrow marked O indicates the difference between the mean origination for the larger interval to which each is assigned (Table 1), shown by a dashed horizontal line, and the actual origination in the mass depletion interval. Arrow marked E indicates the difference between the mean extinction for the larger interval to which each is assigned (Table 1), shown by a horizontal solid line, and the actual extinction magnitude in the mass depletion interval. Diversity loss indicated by the vertical thin box between the origination and extinction values. A, Late Ashgillian, at the end of the Ordovician. B, Djhulfian, at the end of the Permian (with marked diversity loss in the preceding Guadalupian stage, as well). C, Maastrichtian, at the end of the Cretaceous. nation during these intervals been no more the role of origination failure is brought to the than average, diversity losses would actually fore for both the Frasnian and the end-Trias- have been somewhat greater than they were sic. Neither was an extinction event of the (Table 2). The noticeably higher-than-average magnitude of the end-Ordovician, end-Perm- proportion of origination in the Djhulfian ian, and end–Cretaceous events, yet each qual- (10% higher than the mean for the Late Car- ifies as one of the ‘‘big five’’ post-Cambrian di- boniferous and Permian) may reflect recovery versity depletions because of moderately ele- from the diversity loss in the Guadalupian, vated extinction in concert with marked orig- but the other two intervals have proportions ination failure. of origination only one to two-and-a-half per- Other intervals that have relatively high cent higher than the average for their strati- magnitude of extinction are occasionally la- graphic neighborhoods. beled ‘‘mass extinctions,’’ but they do not In contrast, the two remaining ‘‘big five’’ show dramatic losses of diversity. For exam- mass depletions—the late Frasnian and the ple, the Kaca´k/otomari event near the end of end-Triassic—reflect a more complicated im- the in the Middle Devonian has been balance between origination and extinction associated with impact ejecta in Morocco (Ell- (Fig. 8). During both intervals, origination was wood et al. 2003), but the cited extinction of markedly lower than average for their strati- ‘‘as many as 40% of all marine genera’’ graphic neighborhoods. Although each inter- is actually 37% extinction for the entire 11-mil- val registered somewhat elevated extinction, lion-year-long Eifelian stage, not just the Ka- about two-thirds of the diversity loss in the ca´k/otomari event (Sepkoski’s data, cited by late Frasnian and almost 60% in the end-Tri- Ellwood et al. is only resolved to the full stage assic can be ascribed to origination failure, not level for the Eifelian), and is nearly balanced elevated extinction (Table 2). McGhee (1988) by 33% origination, resulting in a net Eifelian originally emphasized that low origination diversity loss of only 4%. Extinction was equal was a major factor in the Frasnian diversity to the Eifelian level in the preceding depletion, but it is only with this paper that and was actually greater in the Ludlovian of 536 RICHARD K. BAMBACH ET AL.

FIGURE 8. Relationship between origination and extinction for the two mass diversity depletions that are not ex- clusively extinction driven. Arrows as in Figure 7. Diversity loss indicated by the vertical thin box between the origination and extinction values. A, Late Frasnian, in the Late Devonian. Note that several preceding intervals also have lower origination than extinction, indicating continuous diversity loss, although a drop in origination plus a small peak of extinction concentrates more diversity loss in the late Frasnian. B, Late Norian/Rhaetian, at the end of the Triassic. In this case, proportion of origination decreased through most of the Triassic as diversity rebounded from the end-Permian mass depletion, but exceeded extinction except at the end of the Triassic, when origination was at its low point and there was a small peak of extinction. the Silurian, but in both instances origination rest of the Phanerozoic, yet taxonomic turn- also nearly balanced extinction. Events that over is greater (as can be seen by the relative record moderate extinction over short time in- size of the turnover peaks compared with the tervals in some regions, like the Kaca´k/oto- boundary-crossing [minimum] diversity plot mari episode, deserve close attention, but they in Figs. 1 and 9A). Sepkoski’s (1996) strati- are simply not comparable to the end-Permian graphic subdivisions of Cambrian time may or end-Cretaceous devastations, nor were they be unrealistically small (e.g., Landing 1994), associated with diversity depletions on a glob- raising questions about the accuracy of his de- al scale similar to those of the late Frasnian or tailed correlations and calling his diversity end-Triassic. numbers for these fine-scale intervals into Mass Depletions during the Cambrian. The question; however, combining these intervals Cambrian and Early Ordovician are unusual into larger time divisions more comparable in in having very low diversity and very high duration to those characteristic of younger pe- rates of faunal turnover. Figures 3A, 4, and 9B riods would result in even more pronounced illustrate the preponderance of high propor- turnover rates because of the short ranges of tional origination and extinction in this inter- many Cambrian taxa. As an example, propor- val: 87% of the intervals in the Phanerozoic tion of origination in the Middle Cambrian as with genus origination greater than 50% and a whole was 0.691 and proportion of extinc- 68% of all intervals with genus extinction tion was 0.676, whereas origination averaged greater than 40% occur during the Cambrian 0.461 and extinction averaged 0.467 for each of and Early Ordovician. As noted above, it is the four intervals of the Middle Cambrian tab- statistically highly unlikely that the prepon- ulated here. Thus, regardless of any over-op- derance of high extinction magnitude was timism in the designation of stratigraphic bins produced by chance alone. What makes this used by Sepkoski, the Cambrian and Early Or- even more unusual is that the durations of dovician was an interval of unusual turnover. many subdivisions during this interval are Important extinctions have, of course, been much shorter than the average through the recognized in the Cambrian. Signor (1992) ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 537

FIGURE 9. A, Genus diversity and diversity turnover through the Cambrian and Early Ordovician. Graph plotted as in Figure 1. Notice the high degree of taxonomic turnover. Arrows mark the two times of marked diversity de- crease. B, Proportions of origination and extinction through the Cambrian and Early Ordovician. Both origination and extinction were generally high during the Cambrian and Early Ordovician. The two intervals of marked di- versity depletion are distinguished by depression of origination, not peaks of extinction.

first pointed to the Botomian as a time of mass cyathids increased, but rather because propor- extinction (see also Zhuravlev and Wood tions of origination for archaeocyathids, prob- 1996). Archaeocyathan diversity collapsed, lematica, hyolithids, and inarticulate brachio- and small shelly fossil diversity declined as pods all fell to one-fifth to one-third the values well (although, as Porter [2003] has shown, they had maintained in the Atdabanian and loss of preservational opportunity clouds the early Botomian. Among diverse groups in the picture for the latter group). Nonetheless, Sep- Early Cambrian, only the trilobites main- koski’s data suggest that Botomian extinction tained origination rates high enough to coun- proportions for the total fauna were actually ter attrition from the ‘‘normal’’ extinction pro- lower than those of several other Cambrian in- portions in the late Botomian. tervals, and the marked late Botomian change The same is true for the early part of the late for the fauna as a whole reflects a drop in orig- Middle Cambrian. Although Palmer’s (1984, ination, not an increase in extinction (Fig. 9B). 1998) documentation of extinction at biomere The loss of diversity in the late Botomian was boundaries may contribute to the high extinc- not because extinction proportion for arcaheo- tion magnitudes in the Middle and Late Cam- 538 RICHARD K. BAMBACH ET AL. brian, the diversity loss of the early part of the selectivity differences in the patterns of ex- late Middle Cambrian interval stands out tinction for these two events that clearly dif- mostly for its low level of genus origination ferentiate between them, and neither resem- (Fig. 9B). Thus, the two Cambrian intervals of bles the Permian pattern. Thus, although the diversity depletion resemble the Late Devo- end-Permian and end-Cretaceous global mass nian and end-Triassic more closely than they extinctions share one result—both devastated do the three unambiguous global mass extinc- antecedent —the patterns of the tions. two extinctions were different and their post- In one way, this finding is more or less in- extinction recoveries distinct (Bambach et al. evitable. When mean rates of extinction stand 2002). As pointed out by Droser et al. (2000), at 46% per interval, driving diversity deple- Brenchley et al. (2001), and Sheehan (2001), tion by increasing extinction rate is a tall order. and confirmed quantitatively by Bambach et However, the more specific question of why al. (2002), the Ordovician global mass extinc- archaeocyathans, trilobites, and other Cam- tion did not have a comparable effect on eco- brian dominants should have experienced de- system structure. clining rates of origination during these inter- As an illustration of the difference in effect vals has no clear answer at this time (as is also of the Ordovician and Permian extinctions, a the case for the Frasnian and end-Triassic not- recent study of in South ed above). Perhaps changing Botomian (Rong and Shen 2002) noted that there were chemistry selected against the massive calci- no ordinal extinctions in the Ordovician event fication that is the hallmark of archaeocy- and that there is a ‘‘close taxonomic and eco- athans (e.g., Rowland and Shapiro 2002). And logical relationship of pre- and post-extinction perhaps ocean circulation changed during the associations’’ (p. 25). In contrast, late Middle Cambrian, influencing the shelf four orders and 20 superfamilies disappeared environments that supported marine diversi- in the end-Permian event, and very few Tri- ty. Compelling answers may come from cre- assic brachiopods link back to the Permian at ative interactions between and the genus level. For the three unambiguous system geochemistry. global mass extinctions, then, there are differ- ences in the physiological selectivity of the What about Continuity of Effect events, the ecological impacts of the events, and Cause? and the style of effect on particular taxa. Con- Although the ‘‘big five’’ global mass deple- tinuity of effect is simply absent. tions of diversity do not share continuity of The two other global mass depletions differ magnitude it might be that they share com- from the three global mass extinctions in nu- mon properties in terms of the biological ef- merous ways, including effect when the bal- fects of diversity loss. This, however, does not ance between origination and extinction is appear to be the case. considered, but they are still not well under- Knoll et al. (1996) identified a distinct selec- stood. The Frasnian event is complicated. tivity in end-Permian extinction in which Most workers accept that at least two pulses of heavily calcified animals with low metabolic extinction occurred, in association with two rates were devastated (88% genus extinction), Kellwasser black-shale horizons (see, for ex- whereas metazoans with high metabolic rates ample, Chen and Tucker 2003). Extinction and calcareous skeletons precipitated from pulses are also recorded in the Middle and physiologically buffered solutions (or with Late Devonian (House 1985; McGhee 1996), skeletons made from materials other than especially the so-called at

CaCO3) were far less affected (49% genus ex- the end of the Famennian (House 1985; Si- tinction), and more recent work is refining the makov 1993; Wang et al. 1993). Indeed, at the pattern (Bambach and Knoll unpublished stage and substage levels, marine diversity data). During the end-Ordovician and end- decreased almost continuously through Mid- Cretaceous events, no selectivity of this sort dle and Late Devonian time (Fig. 1). Moreover, occurred. Sheehan et al. (1996) documented the marine fauna underwent dramatic turn- ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 539 over in dominant (Bambach 1999). One might, therefore, question whether our Copper (2002: p. 49) observed that distri- conclusions reflect artifactual, rather than bi- bution declined progressively from the Give- ological, patterns in the fossil record. Could tian through the Frasnian, and stated that there be defects or biases in the record that there is ‘‘no catastrophic reef ‘kill horizon’ at give the appearance of major diversity deple- the F/F boundary known anywhere in the tions when none actually exist? world.’’ Copper (2002) associated the ob- Although we do not deny that some of the served decline with climatic and tectonic apparent diversity change in each of the ‘‘big change. Although the causes of reduced Fras- five’’ diversity depletions could be accentuat- nian origination are not yet clearly known, ed by record failure, in none of these instances loss of complex reef habitats could have facil- is it reasonable to expect that tabulated diver- itated reduced origination by eliminating a sity change was produced entirely by failure of normally diverse ecosystem. the record. For instance, Raup (1978) once The end-Triassic event is the least well un- estimated the amount of extinction at the end derstood of the major diversity depletions. As of the Permian was equivalent to an 85-mil- noted above, this event was driven as much by lion-year gap in the geologic record, some- origination failure as by extinction, in contrast thing obviously precluded by radiometric to the end-Ordovician, end-Permian, and end- ages of Permian and Triassic rocks near the Cretaceous events. Moreover, neither glacia- Permo-Triassic boundary (Bowring et al. tion nor major biotic reorganization, charac- 1998). Also, Raup’s (1982) efforts to model ex- teristics associated with the end-Ordovician tinction by elimination of large areas of the and Late Devonian diversity depletions, is Earth—originally conceived as a test of im- manifest in the (although both pact scenarios for extinction, but equally ap- large plateau basalt eruptions and bolide im- plicable to questions of record failure—pro- pact have been implicated [Bice et al. 1992; duced surprisingly small extinctions of genera Courtillot et al. 1996; Wignall 2001; Olsen et and families (mean extinction of only 13.8% of al. 2002]). Although complete and informative marine genera and 12% of terrestrial families) marine sections are still being sought (Hallam when half our planet’s surface was eradicated. et al. 2000), there are now proposals that ob- Record failure is simply not capable of pro- served terrestrial and marine extinctions may ducing apparent diversity fluctuations on the not be synchronous (Pa´lfy et al. 2000) and geo- scale observed in the large global diversity de- chemical analyses that also suggest a double- pletions. pulsed event of some sort (Hesselbo et al. In summary, we believe that the major con- 2002). In concluding a recent survey of end- clusions articulated in this paper describe real Triassic data, Hallam (2002: p. 133) stated, changes in the diversity of marine animals ‘‘Though the current evidence cannot deci- though Phanerozoic time. sively exclude it, the foregoing review does not favour a major T–J boundary catastrophe.’’ Conclusions The five major mass depletions of diversity Of 88 stage or substage intervals during the are so different in major features that it is clear 470 million years since the Early Ordovician they cannot share common cause. Nor did Arenig, only five suffered a loss of diversity they have common effect, beyond major loss greater than 13.5% of the number of marine of diversity. genera that entered the interval. These five in- tervals—the late Ashgillian at the end of the Could It All Be Artifactual? Ordovician, the late Frasnian in the Late De- Variability in the quality of the geologic re- vonian, the Djhulfian at the end of the Perm- cord has the potential to affect observed di- ian, the late Norian/Rhaetian at the end of the versity and it undoubtedly has affected some Triassic, and the Maastrichtian at the end of aspects of detailed interval-to-interval chang- the Cretaceous—have been grouped as the es in apparent diversity (Peters and Foote ‘‘big five’’ mass extinctions, but they are better 2001, 2002; Smith et al. 2001; Kier 1974 1977). regarded as mass depletions of diversity. 540 RICHARD K. BAMBACH ET AL.

Two of the five mass depletions, the late Bambach, R. K., A. H. Knoll, and J. J. Sepkoski Jr. 2002. Anatom- ical and ecological constraints on Phanerozoic animal diver- Frasnian and the end-Triassic, resulted pri- sity in the marine realm. Proceedings of the National Acad- marily from attrition related to reduced orig- emy of Sciences USA 99:6854–6859. ination, rather than devastation from unusu- Bice, D. M., C. R. Newton, S. McCauley, P. W. Reiners, and C. A. McRoberts. 1992. Shocked quartz at the Triassic-Jurassic ally elevated extinction. Both intervals oc- boundary in Italy. Science 255:443–446. curred during times of generally high extinc- Bowring, S. A., D. H. Erwin, Y. G. Jin, M. W. Martin, K. Davidek, tion, so lowered origination had severe and W. Wang. 1998. U/Pb zircon geochronology and tempo of the end-Permian mass extinction. Science 280:1039–1045. consequences for diversity. Extinction in these Brasier, M. D., and S. S. Sukhov. 1998. The falling amplitude of two intervals was elevated above average for carbon isotopic oscillations through the lower to middle Cam- their stratigraphic neighborhoods, but in each brian: northern data. Canadian Journal of Earth Sci- ences 35:353–373. case elevated extinction was responsible for Brenchley, P. J., J. D. Marshall, and C. J. Underwood. 2001. Do only a little more than one-third of the diver- all mass extinctions represent an ecological crisis?’’ Evidence sity loss, leaving the remainder to be ex- from the Late Ordovician. Geological Journal 36:329–340. Budd, G. E., and S. Jensen. 2000. A critical reappraisal of the plained by reduced origination. A similar re- fossil record of the bilaterian phyla. Biological Reviews 75: lationship between reduced origination and 253–295. diversity loss is seen in two Cambrian inter- Bush, A. M., and R. K. Bambach. In press. Did increase during the Phanerozoic? Lifting the veil of tapho- vals with marked loss of diversity (the late Bo- nomic, latitudinal, and environmental biases in the study of tomian and the early part of the late Middle paleocommunities. Journal of Geology. Cambrian). Bush, A. M., M. J. Markey, and C. R. Marshall. 2001. Estimating biodiversity in light of heterogeneous sampling intensities: On the other hand, diversity loss in the end- the relationship between taxon-occurrence subsampling Ordovician, end-Permian, and end-Creta- methods and alpha and . PaleoBios 21(Suppl. to ceous intervals resulted exclusively from ele- No. 2):37. Bush, A. M., M. J. Markey, and C. R. Marshall. In press. Alpha, vated extinction. The extinction magnitudes of beta, gamma: the effects of spatially organized biodiversity these three intervals are statistically different on sampling-standardization. . from the extinction magnitudes in their strati- Chen, D., and M. E. Tucker. 2003. The Frasnian-Famennian mass extinction: insights from high-resolution sequence stratigra- graphic neighborhoods; they can be regarded phy and cyclostratigraphy in South China. Palaeogeography, as ‘‘true’’ global mass extinctions. Palaeoclimatology, Palaeoecology 193:87–111. Cleveland, W. S. 1979. Robust locally weighted regression and Acknowledgments smoothing scatterplots. Journal of the American Statistical Association 74:829–836. We thank A. I. Miller and an anonymous re- Connolly, S. R., and A. I. Miller. 2001. Global Ordovician faunal viewer for many suggestions that helped to transitions in the marine benthos: proximate causes. Paleo- 27:779–795. improve the manuscript. A.H.K.’s research Copper, P. 2002. Reef development at the Frasnian/Famennian was supported, in part, by the NASA Astro- mass extinction boundary. Palaeogeography, Palaeoclimatol- biology Institute. S.C.W. is grateful for fund- ogy, Palaeoecology 181:27–65. Courtillot, V. J.-J. Jaeger, Z. Yang, G. Fe´raud, and C. Hofmann. ing from the Swarthmore College Research 1996. The influence of continental flood basalts on mass ex- Fund and the Christian R. and Mary F. Lind- tinctions: where do we stand? In G. Ryder, D. Fastovsky, and back Foundation. S. Gartner, eds. The Cretaceous- event and other ca- tastrophes in earth history. Geological Society of America Special Paper 307:513–515. Literature Cited Cutbill, J. L., and B. M. Funnell, 1967. Numerical analysis of the Bambach, R. K. 1983. Ecospace utilization and guilds in marine fossil record. Pp. 791–820 in W. B. Harland, W. B., C. H. Hol- communities through the Phanerozoic. Pp. 719–746 (Chapter land, M. R. House, N. F. Hughes, A. B. Reynolds, M. J. S. Rud- 15) in M. Tevesz and P. McCall, eds. Biotic interactions in re- wick, G. E. Satterthwaite, L. B. Tarlow, and E. C. Willey, eds. cent and fossil benthic communities. Plenum, New York. The fossil record. Geological Society, London. Bambach, R. K. 1985. Classes and adaptive variety: the Droser, M. L., D. J. Bottjer, P. M. Sheehan, and G. R. McGhee. of diversification in marine through the Phanerozoic. 2000. Decoupling of taxonomic and ecologic severity of Phan- Pp. 191–253 in J. W. Valentine, ed. Phanerozoic diversity pat- erozoic marine mass extinctions. Geology 28:675–678. terns: profiles in macroevolution. Princeton University Press, Ellwood, B. B., S. L. Benoist, A. El Hassani, C. Wheeler, and R. Princeton, N.J. E. Crick. 2003. Impact ejecta layer from the Mid-Devonian: Bambach, R. K. 1999. Energetics in the global marine fauna: a possible connection to global mass extinctions. Science 300: connection between terrestrial diversification and change in 1734–1737. the marine biosphere. Geobios 32:131–144. Finney, S. C., W. B. N. Berry, J. D. Cooper, R. L. Ripperdan, W. Bambach, R. K., and N. L. Gilinsky. 1986. Perspectives on the C. Sweet, S. R. Jacobson, A. Soufiane, A. Achab, and P.J. Noble. distribution of origination and extinction during the Phan- 1999. Late Ordovician mass extinction: a new perspective erozoic. Geological Society of America Abstracts with Pro- from stratigraphic sections in central Nevada. Geology 27: grams 18:534. 215–218. ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS 541

Foote, M. 1988. Survivorship analysis of Cambrian and Ordo- ———. 1963. Crises in the . Scientific American vician trilobites. Paleobiology 14:258–271. 208(2):77–92. Gilinsky, N. L. 1994. Volatility and the Phanerozoic decline of ———. 1967. Revolutions in the history of life. In C. C. Albritton background extinction intensity. Paleobiology 20:445–458. Jr., ed. Uniformity and simplicity. Geological Society of Amer- Hallam, A. 2002. How catastrophic was the end-Triassic mass ica Special Paper 89:63–91. extinction? Lethaia 35:147–157. Olsen, P. E., D. V. Kent, H. D. Sues, C. Koeberl, H. Huber, A. Hallam, A., and P. B. Wignall. 1999. Mass extinctions and sea- Montanari, E. C. Rainforth, S. J. Fowell, M. J. Szajna, and B. level changes. Earth-Science Reviews 48:217–250. W. Hartline. 2002. Ascent of linked to an iridium Hart, M. B., ed. 1996. Biotic recovery from mass extinction anomaly at the Triassic-Jurassic boundary. Science 296:1305– events. Geological Society of London Special Publication 102. 1307. Hesselbo, S. P., S. A. Robinson, F. Surlyk, and S. Piasecki. 2002. Pa´lfy, J., J. K. Mortensen, E. S. Carter, P. L. Smith, R. M. Fried- Terrestrial and marine extinction at the Triassic-Jurassic man, and H. W. Tipper. 2000. Timing the end-Triassic mass boundary synchronized with major carbon-cycle perturba- extinction: first on land, then in the sea? Geology 28:39–42. tion: a link to initiation of massive volcanism? Geology 30: Palmer, A. R. 1984. The biomere problem: evolution of an idea. 251–254. Journal of Paleontology 58:599–611. House, M. R. 1985. Correlation of mid Paleozoic ammonoid evo- ———. 1998. A proposed nomenclature for stages and series for lutionary events with global sedimentary perturbations. Na- the Cambrian of . Canadian Journal of Earth Scienc- ture 313:17–22. es 35:323–328. Hubbard, A. E., and N. L. Gilinsky. 1992. Mass extinctions as Peters, S. E., and M. Foote. 2001. Biodiversity in the Phanero- statistical phenomena: an examination of the evidence using zoic: a reinterpretation. Paleobiology 27:583–601. ␹2 tests and bootstrapping. Paleobiology 18:148–160. ———. 2002. Determinants of extinction in the fossil record. Na- Jablonski, D. J. 1986. Causes and consequences of mass extinc- ture 416:420–424. tions: a comparative approach. Pp. 183–229 in D. K. Elliott, ed. Porter, S. M. 2004. Closing the ‘‘phosphatization’’ window: test- Dynamics of extinction. Wiley, New York. ing for the influence of taphonomic megabias on the pattern Jablonski, D. J., K. Roy, J. W. Valentine, R. M. Price, and P. S. An- of small shelly fossil decline. Palaios 19:178–183. derson. 2003. The impact of the Pull of the Recent on the his- Quinn, J. F. 1983. Comment on: mass extinctions in the fossil re- tory of marine diversity. Science 300:1133–1135. cord. Science 219:1239–1240. Jackson, J. B. C., and K. G. Johnson. 2001. Measuring past bio- Raup, D. M. 1978. Cohort analysis of generic survivorship. Pa- diversity. Science 293:2401–2404. leobiology 4:1–15. Jin, Y.-g., Y. Wang, W. Wang, Q. H. Shang, C. Q. Cao, and D. H. ———. 1982. Biogeographic extinction: a feasibility test. In L. E. Erwin. 2000. Pattern of marine mass extinction near the Perm- Silver and P. H. Schultz, eds. Geological implications of im- ian/Triassic boundary in South China. Science 289:432–436. pacts of large asteroids and on the Earth. Geological Kier, P. M. 1974. Evolutionary trends and their functional sig- Society of America Special Paper 190:277–281. nificance in post-Paleozoic echinoids. Paleontological Society ———. 1987. Mass extinction: a commentary. Palaeontology 30: Memoir 5. Journal of Paleontology 48(Suppl. to No. 3). 1–13. ———. 1977. The poor fossil record of the regular echinoid. Pa- ———. 1991. A kill curve for Phanerozoic marine . Pa- leobiology 3:168–174. leobiology 17:37–48. Knoll, A. H. 1989. Evolution and extinction in the marine realm: Raup, D. M., and J. J. Sepkoski Jr. 1982. Mass extinctions in the some constraints imposed by . Philosophical marine fossil record. Science 215:1501–1503. Transactions of the Royal Society of London B 325:279–290. Rong, J.-y., and S.-z. Shen. 2002. Comparative analysis of the Knoll, A. H., R. K. Bambach, D. E. Canfield, and J. P. Grotzinger. end-Permian and end-Ordovician brachiopod mass extinc- 1996. Comparative earth history and Late Permian mass ex- tions and survivals in South China. Palaeogeography, Palaeo- tinction. Science 273:452–457. climatology, Palaeoecology 188:25–38. Knoll, A. H., and S. B. Carroll. 1999. Early animal evolution: Rowland, S. M., and R. S. Shapiro. 2002. Reef patterns and en- emerging views from comparative biology and geology. Sci- vironmental influences in the Cambrian and earliest Ordo- ence 284:2129–2137. vician. In W. Kiessling, E. Flu¨gel, and J. Golonka, eds. Phan- Landing, E. 1994. Lower Cambrian of southeastern Newfound- erozoic reef patterns. SEPM Special Publication. 72:95–128. land: epeirogeny and Lazarus faunas, lithofacies-biofacies Saltzman, M. R., R. L. Ripperdan, M. D. Brasier, K. C. Lohmann, links, and the myth of a global . Pp. 283– R. A. Robison, W. T. Chang, S. C. Peng, E. K. Ergaliev, and B. 309 in J. H. Lipps and P. W. Signor, eds. Origin and early evo- Runnegar. 2000. A global carbon isotope excursion (SPICE) lution of the Metazoa. Plenum, New York. during the Late Cambrian: relation to trilobite extinctions, or- Leakey, R. E., and R. Lewin. 1995. The sixth extinction: patterns ganic-matter burial and . Palaeogeography, Palaeo- of life and the future of humankind. Doubleday, New York, climatology, Palaeoecology 162:211–223. 271 p. Sepkoski, J. J., Jr. 1981. A factor analytic description of the Phan- MacLeod, N., and G. Keller, eds. 1996. Cretaceous-Tertiary mass erozoic marine fossil record. Paleobiology 7:36–53. extinctions: biotic and environmental changes. Norton, New ———. 1982. A compendium of fossil marine families. Milwau- York . kee Public Museum Contributions to Biology and Geology McGhee, George R., Jr. 1988. The No. 51. event: evidence for abrupt ecosystem collapse. Paleobiology ———. 2002. A compendium of fossil marine animal genera. 14:250–257. Bulletins of American Paleontology No. 363. ———. 1996. The Late Devonian mass extinction. Columbia Uni- Sepkoski, J. J., Jr., R. K. Bambach, D. M. Raup, and J. W.Valentine. versity Press, New York. 1981. Phanerozoic marine diversity: a strong signal from the ———. 2001. The ‘multiple impacts hypothesis’ for mass extinc- fossil record. Nature 293:435–437. tion: a comparison of the Late Devonian and the late . Sheehan, P. M. 2001. The Late Ordovician mass extinction. An- Palaeogeography, Palaeoclimatology, Palaeoecology 176:47– nual Reviews of Earth and Planetary Science 29:331–364. 58. Sheehan, P. M., P. J. Coorough, and D. E. Fastovsky. 1996. Biotic Newell, N. D. 1962. Paleontological gaps and geochronology. selectivity during the K/T and Late Ordovician extinction Journal of Paleontology 36:592–610. events. In G. Ryder, D. Fastovsky, and S. Gartner, eds. The 542 RICHARD K. BAMBACH ET AL.

Cretaceous-Tertiary event and other catastrophes in earth his- laeogeography, Palaeoclimatology, Palaeoecology 104:127– tory. Geological Society of America Special Paper 307:477– 137. 489. Smith, A. B., A. S. Gale, and N. E. A. Monks. 2001. Sea-level Signor, P. W. 1992. Taxonomic diversity and faunal turnover in change and rock-record bias in the Cretaceous: a problem for extinction and biodiversity studies. Paleobiology 27:241–253. the Early Cambrian: did the most severe mass extinction of Stanley, S. M., and X. Yang. 1994. A double mass extinction at the Phanerozoic occur in the Botomian stage? In S. Lidgard the end of the Paleozoic era. Science 266:1340–1344. and P. R. Crane, eds. Fifth North American Paleontological Van Valen, L. M. 1984. A resetting of Phanerozoic community Convention, Abstracts and program. Paleontological Society evolution. Nature 307:50–52. Special Publication 6:272. Wang, K., M. Attrep, and C. J. Orth. 1993. Global iridium anom- Signor, P. W., and J. H. Lipps. 1982. Sampling bias, gradual ex- aly, mass extinction, and redox change at the Devonian-Car- tinction patterns, and catastrophes in the fossil record. In L. boniferous boundary. Geology 21:1071–1074. E. Silver and P. H. Schultz, eds. Geological implications of im- Wang, S. C. 2003. On the continuity of background and mass pacts of large asteroids and comets on the Earth. Geological extinction. Paleobiology 29:455–467. Wignall, P. B. 2001. Large igneous provinces and mass extinc- Society of America Special Paper 190:291–296. tions. Earth-Science Reviews 53:1–33. Silverman, B. W. 1981. Using kernel density estimates to inves- Wignall, P. B., and R. J. Twitchett. 1996. Oceanic anoxia and the tigate multimodality. Journal of the Royal Statistical Society B end Permian mass extinction. Science 272:1155–1158. 43:97–99. Zhuravlev, A. Yu., and R. A. Wood. 1996. Anoxia as the cause Simakov, K. V. 1993. Biochronological aspects of the Devonian- of the mid-Early Cambrian (Botomian) extinction event. Ge- Carboniferous crisis in the regions of the former U.S.S.R. Pa- ology 24:311–314.