Origination, extinction, and mass depletions of marine diversity · 2004-11-01 · mass extinction intervals. Indeed, Raup (1991) developed his view of the Phanerozoic kill curve

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

Origination, extinction, and mass depletions of marine diversity

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

Abstract.—In post-Cambrian time, five events—the end-Ordovician, end-Frasnian in the Late De-vonian, end-Permian, end-Triassic, and end-Cretaceous—are commonly grouped as the ‘‘big five’’global intervals of mass extinction. Plotted by magnitude, extinction intensities for all Phanerozoicsubstages show a continuous distribution, with the five traditionally recognized mass extinctionslocated 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 intensityof extinction during the ‘‘big five’’ events. Compared with other stages and substages in the sameneighborhood, only the end-Ordovician, end-Permian, and end-Cretaceous extinction intensitiesappear as outliers. Moreover, when origination and extinction are considered together, only thesethree of the ‘‘big five’’ events appear to have been generated exclusively by elevated extinction. Loworigination 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 whendiversity suffered mass depletion, only those at the end of the Ordovician, Permian, and Cretaceousperiods unequivocally qualify as globally distinct mass extinctions. Each of the three has a uniquepattern of extinction, and the diversity dynamics of these events differ, as well, from the other twomajor 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, Harvard University, 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:Mass versus ‘‘Background’’ Extinction

The idea that mass extinctions stand out asa class of events separate from the range of‘‘normal’’ or ‘‘background’’ extinctions thatcharacterize most of the geological recordoriginated with the work of Norman Newell(1962, 1963, 1967) and crystallized throughthe quantitative analysis by Raup and Sepko-ski (1982). Using Sepkoski’s compilation ofstratigraphic ranges temporally resolved tothe stage level for marine families of all ani-mal taxa (Sepkoski 1982), Raup and Sepkoskiidentified five mass extinctions: the end-Or-dovician (Ashgillian); Late Devonian (includ-ing the Frasnian/Famennian boundary); end-Permian (Guadalupian and Djhulfian togeth-er); end-Triassic (Late Norian or Rhaetian);and end-Cretaceous (Maastrichtian). Thesehave become known informally as ‘‘the big

* This paper is dedicated to the memory of Stephen JayGould (1941–2002).

five’’ mass extinctions. Each had been notedearlier by Newell (1967).

Raup and Sepkoski plotted the extinctionrate (number of families going extinct per mil-lion years) for each stage in time order and as-sumed that apparent outliers on the arithme-tic plot were true statistical outliers (and notaberrations produced by errors in the time-scale), thus identifying a distinct class of massextinctions. They also calculated a 95% confi-dence interval around the remaining ‘‘back-ground’’ extinction stages and demonstrateda secular decrease in extinction rates overtime. Quinn (1983), however, showed that theextinction data were highly skewed and cor-rectly pointed out that the assumption of anormal distribution for ‘‘background’’ extinc-tion data was not valid. When log-trans-formed, the distribution of extinction rateswas approximately normal and did not have asuite of outliers that could be categorized un-ambiguously as a class of mass extinctionsseparate from the overall ‘‘background’’ dis-tribution. Bambach and Gilinsky (1986) dem-

523ORIGINATION, EXTINCTION, AND DIVERSITY DEPELETIONS

onstrated that this was also the case for severalother extinction metrics, including propor-tional metrics by interval that are not subjectto time-scale error. For all metrics the distri-bution of extinction intensity grades smoothlyfrom lowest to highest values with no discretebreak between ‘‘background’’ and presumedmass extinction intervals. Indeed, Raup (1991)developed his view of the Phanerozoic killcurve on the basis of this continuity of extinc-tion magnitudes. Bambach and Gilinsky(1986) did, however, support the finding thatextinction intensities (and origination inten-sities, as well) declined during the Phanero-zoic, a conclusion discussed more fully by Gil-insky (1994).

Despite the evidence that intensities of ex-tinction form a continuum, the five eventsspecified by Raup and Sepkoski (1982) contin-ue to be labeled ‘‘mass extinctions’’ (Finney etal. 1999; McGhee 2001; Wignall and Twitchett1996; Palfy et al. 2000; MacLeod and Keller1996). Current threats to biodiversity haveeven been labeled ‘‘the sixth extinction’’ (Lea-key and Lewin 1995). It may be that magni-tude alone is sufficient to justify the term‘‘mass extinction’’ because events with suchpronounced loss of diversity are rare, withwaiting times of about 100 million years (Raup1991). But is there any reason to think of theseevents as a separate class of events, rather thanas the uncommon upper tail of a continuousdistribution?

Wang (2003) recently identified three con-cepts that must be considered individuallywhen we ask whether putative mass extinc-tions grade continuously into the range ofbackground extinction: continuity of cause,continuity of effect, and continuity of magni-tude. Continuity of cause would be demon-strated if candidate mass extinctions could beshown to be driven by the same processes thatare responsible for background extinction, al-beit operating at increased intensity or overlarger areas. Continuity of effect would be es-tablished if background and mass extinctionsexhibited common patterns of selectivity ontaxonomic, functional, ecological, or othergrounds. And continuity of magnitude wouldexist if the distribution of intensities of massextinctions graded smoothly and continuous-

ly into intensities of background extinction.Although continuity of magnitude appears tohave been demonstrated by Quinn (1983) andBambach and Gilinsky (1986), and was as-sumed by Raup (1991) in his kill curve anal-ysis for the Phanerozoic, several factors led usto reconsider the status of these intervals.These include (a) the rarity of the largest ex-tinction intensities, (b) the possibility that theydo not share continuity of cause or effect withall other intervals, and (c) the fact that origi-nation and extinction have rarely been consid-ered together in examining patterns of diver-sity change.

In the following sections, we reevaluate thecontinuity or discontinuity of magnitude andthen briefly consider whether events thatmight be regarded as mass extinctions can beunified by effect or cause. We test whether anyof the ‘‘big five’’ events are differentiable fromthe distribution of other extinction intensities,explore the role of origination as well as ex-tinction in diversity changes associated withthese five intervals, and comment on the dif-ferences, as well as similarities, among the in-tervals. The upshot will be that although thefive intervals in question—the end-Ordovi-cian, Late Devonian, end-Permian, end-Trias-sic, and end-Cretaceous—are the five intervalswith the greatest diversity loss in the Phan-erozoic, they share little else in common. Onlythree were driven predominantly by extinc-tion and even they display distinctly differentpatterns of diversity change, implying thatthese events are not related by continuity ofeffect or cause.

Tracking Genus Diversity

Figure 1 illustrates the history of marine ge-nus diversity through Phanerozoic time. Thedata were compiled by using a computerizedsorting routine written by Jack Sepkoski andmodified by J. Bret Bennington to tabulate ge-nus diversity for 107 stages and substages us-ing Jack Sepkoski’s unpublished tabulation ofthe stratigraphic ranges of genera as of 1996.Although the Paleontological Research Insti-tution has recently published the raw genusranges from a later version (1998) of Sepko-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 majorpost-Cambrian diversity depletions are highlighted. The heavy line connects the data on number of genera crossingeach interval boundary. The line directly connecting the numbers of boundary-crossing genera follows the path ofminimum likely standing diversity, regarded as the minimum diversity because origination and extinction wouldhave to work in exact lock-step to follow that diversity path. The peaked dotted line represents genus turnoverwithin each interval. The rising part of each peak represents all genus originations (first occurrences) reported fromthe interval. The peak records the total number of genera reported from the time interval. The descending part ofthe peak represents the number of extinctions (last records) of genera in the interval. The magnitudes of the peakscompared with the minimum standing diversity at interval boundaries represent the degree of faunal turnover inthe intervals.

cation simply lists all the genera and does notnumerically tabulate the data on diversity.

Genus diversity follows the general patternestablished in the ‘‘consensus paper’’ of Sep-koski et al. (1981) and best known from Sep-koski’s (1981: Fig. 5) widely reproduced fam-ily diversity curve. In the Paleozoic we see the‘‘Cambrian Explosion’’ (the increase in diver-sity in the Early Cambrian), a Middle and LateCambrian ‘‘plateau’’ of diversity, and the Or-dovician Radiation, followed by the long in-terval of fluctuating, but non-trending, diver-sity that began in the Caradocian and lastedfor the rest of the era. Diversity changes dur-ing this ‘‘Paleozoic Plateau’’ include three ofthe ‘‘big five’’ diversity depletions, the end-Ordovician, the Late Devonian, and the end-Permian events. The post-Paleozoic is charac-terized by nearly continuous diversity in-crease, interrupted by the other two ‘‘big five’’diversity depletions, the end-Triassic and thesharp, era-bounding end-Cretaceous events.Note that because we tabulated subgenera ofmollusks, resolved the data to the substagelevel, and emphasized the diversity at intervalboundaries rather than the total diversity

within each interval, the apparent Cenozoicincrease in diversity is proportionately greaterthan that illustrated by Sepkoski for families.

There are some concerns that the apparent-ly large Cenozoic increase in diversity may bepartly artifactual. However, recent analyses(Bush and Bambach in press on alpha diver-sity; Jablonski et al. 2003 on Pull of the Recent;and Bush et al. 2001, in press on techniques ofsample-standardization) demonstrate that anincrease in Cenozoic diversity is strongly in-dicated, although the exact amount is still un-clear (Jackson and Johnson 2001). The ‘‘con-sensus paper’’ (Sepkoski et al. 1981) was puttogether because several of the data sets avoid-ed or mitigated some of the biases, such as im-perfections of the geologic record, that were ofconcern then and still are (Peters and Foote2001). Although every potential problemshould be analyzed and improvement in thedata is necessary, it still appears, as was con-cluded then, that the diversity signal is stron-ger than the noise.

Figure 1 accounts for all the data in the Sep-koski genus compilation (see caption for fullexplanation). Many diversity curves use total


diversity as the recorded data (this is true forpublished illustrations of Sepkoski’s familycurve, for example). If one mentally ‘‘connectsthe dots’’ of total diversity peaks in Figure 1,it is clear that the general shape of a curve con-necting total diversities would be very similarto the boundary-crossing diversity empha-sized here. Mid-Devonian diversity would ap-pear higher than Late Ordovician diversity,Carboniferous diversity would fluctuate more,and the upturn in diversity in the mid-Cre-taceous would be sharper than shown by thestanding diversity plot. The general pattern,however, would be the same.

We use the boundary-crossing standing di-versity as the preferred representation of di-versity and diversity change through time. Weknow that boundary-crossing diversity is notanomalous compared with total diversity be-cause the trend of boundary-crossing diversi-ty follows the general path of total diversity.Two factors make us prefer it to total diver-sity. First, it is the only measure we have ofactual standing diversity. Total diversity in aninterval was not the actual standing diversityat any time because it is unlikely that all orig-inations occurred in an interval before any ex-tinction. However, the recorded diversity atthe boundaries of each interval, calculated bysubtracting all extinctions in the interval fromthe total diversity in the interval, is a directmeasure of standing diversity at intervalboundaries. The other compelling reason isthat change in diversity is shown best by com-paring diversity at the start of different inter-vals.

Diversity is a function of both originationand extinction. The peaks of turnover withineach interval in Figure 1 reveal how much var-iation of diversity can occur in any interval,but comparing standing diversities at intervalboundaries tells us whether origination andextinction are in balance (little or no change ofdiversity from one boundary to the next) orwhether either origination or extinction dom-inated during an interval (origination domi-nating if boundary-crossing diversity increas-es, extinction being more important if bound-ary-crossing diversity decreases). In plots oftotal diversity, a predominance of extinctionover origination in one interval could be

masked by an increase in origination in thenext. Total diversity might appear unchangedbetween the two intervals because originationin a rapid recovery from an extinction eventcould make total diversity in the succeedinginterval equal to that in the previous one, con-cealing the low diversity at the start of the in-terval. For example, although extinction ex-ceeded origination in each of the last two in-tervals of the Silurian and diversity appears tohave been lost between the Ludlovian and Pri-dolian when looking at total diversity, the lowpoint of diversity at the end of the Silurian(end-Pridolian) is masked in the total diver-sity curve because, in the Gedinnian, the firstinterval of the Devonian, origination was high,causing total diversity to exceed that of thePridolian. Boundary-crossing diversity notonly approximates standing diversity, but italso gives a clearer representation of the con-sequences of within-interval evolutionary dy-namics than that provided by summed totaldiversity data for whole intervals.

The ‘‘Big Five’’ as Diversity Depletions

Inspection of Figure 1 reveals that, althoughdiversity decreased slightly on several otheroccasions, there are only five post-Cambrianintervals when diversity decreased markedly:(1) at the end of the Ordovician, (2) during theMiddle and Late Devonian, (3) during the LatePermian, (4) at the end of the Triassic, and (5)at the end of the Cretaceous. The end-Triassicdecrease does not look as large as the otherfour, but standing diversity throughout theTriassic was lower than at any other time afterthe mid-Ordovician, so the proportional de-crease in the latest Triassic is quite compara-ble to the other four major diversity deple-tions. Two Cambrian intervals are also notedon Figure 1 (the late Botomian [LB] and earlylate Middle Cambrian [ELM]). These weretimes of relatively small numerical change indiversity but high proportional diversity loss.Because the evolutionary dynamics of theCambrian and Early Ordovician are unusualwe will consider them separately; the bulk ofthis paper emphasizes the post-Arenig por-tion of the Phanerozoic.

Because it is hard to judge the proportionalmagnitude of diversity change from a plot of


FIGURE 2. Proportion of gain or loss of genus diversity from the Caradoc to the Plio-Pleistocene. The five majordiversity depletions (decrease greater than 20%) are numbered. Symmetrical lines are drawn at 213.5% and 113.5%(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 diversitydepletions.

absolute values, a plot of proportion of gain orloss of diversity, rather than a plot of the num-bers of genera as such, is desirable. A displayof numbers of taxa, as in Figure 1, is useful forillustrating the pattern of change in diversity,but the numbers represent only those taxa dis-covered in the fossil record and are not a com-plete record of all the taxa that existed. Pro-portional diversity change is what we seek tounderstand here—how episodes of diversityloss affected the whole biota. The question, ineffect, concerns the importance of an event inthe context of its time, not just how many taxawere involved.

Figure 2 shows the proportional gain or lossin the number of genera during each stage orsubstage interval, starting with the Early Car-adocian in the Middle Ordovician after thelarge proportional increases in diversity as-sociated with the Cambrian Explosion and theOrdovician Radiation were over. The changein diversity is calculated as a proportionalchange by subtracting the number of genera atthe start of each interval (the standing diver-sity at the boundary between the interval andits preceding interval) from the number ofgenera at the end of the interval (the standingdiversity at the boundary between the intervaland its succeeding interval) and dividing that

number (the change in the number of generafrom the start to the end of the interval) by thenumber of genera at the start of the interval.For example, if 500 genera pass from intervalone to interval two and 600 genera pass frominterval two to interval three, then there were100 more originations than extinctions duringinterval two, with a gain in diversity of 100genera, a proportional increase of 10.200.Likewise, a decrease from 600 to 500 generaduring an interval (a loss of 100 genera as aresult of 100 more extinctions than origina-tions) would be a proportional decrease of20.167. As noted above, an advantage of de-termining standing diversity at intervalboundaries is that one can follow the balanceof origination and extinction as it influencesdiversity change, something not possiblewhen only tabulating total diversity for eachinterval.

Figure 2 shows that the five intervals al-ready well known as the classic ‘‘big five’’mass extinctions (with the Guadalupian aswell as the end-Permian Djhulfian included inthe major later Permian diversity decrease[Stanley and Yang 1994]) are the only post-Llandeilian intervals with more than a 20%proportional loss of genus diversity. In fact,there is a gap of 8% between the largest loss


of diversity not included in the ‘‘big five’’ andthe smallest loss within the ‘‘big five,’’ but nogaps of as much as 2% occur between anysmaller values when arranged in rank order.These five intervals were certainly times ofmass depletion of diversity, but can we justifyregarding any of them as times of mass ex-tinction different in cause, effect, or magni-tude from ‘‘background’’ extinction?

Large-Magnitude Proportional Increasesin Diversity

As a side issue, but one related to propor-tional diversity change and its timing, it is in-teresting to note that the only times when pro-portional increase of diversity exceeds 13.5%are during the Cambrian Explosion, the Or-dovician Radiation (just ending in the earlyCaradocian at the start of Fig. 2), in the im-mediate aftermath of each of the five ‘‘massdepletions’’ of diversity, and briefly (single in-tervals only) in the Late Cretaceous (Turoni-an) and Neogene (early Miocene) (Fig. 2). Al-though origination rates are not unusuallyhigh in these intervals (no outliers for origi-nation are found in an analysis of originationproportions at these times), the combinationof higher origination and lower extinctionduring the ‘‘recovery’’ phase after diversitydepletion does mark these intervals as timesof unusually great proportional increase in di-versity. These are not necessarily times ofbroad transgression or otherwise better rep-resentation of the marine record, so higherorigination rates in the wake of major diver-sity depletions may reflect recovery from un-usually low diversity and not just the effect ofimproved record availability, a possibilityraised by Peters and Foote (2001).

Testing for Continuity of Magnitudeof Extinction

We tested for continuity or discontinuity ofmagnitude of extinction (i.e., whether or notthe distribution of intensities of apparentmass extinctions grade smoothly and contin-uously into intensities of background extinc-tion) in two ways. (1) We tested whether thereis a smooth continuous distribution of mag-nitudes of extinction intensity with no strongvariation in the upper tail of the distribution,

first for the whole Phanerozoic and second forthe time after the after the ‘‘Cambrian Pla-teau’’ of low diversity and high turnover. (2)We compared magnitudes of extinction foreach interval against the distribution of mag-nitudes of extinction in the particular segmentof the timescale, based on average high or lowextinction rates, to which the interval belongs.Only if an interval satisfies both criteria, thatis, if the interval is not part of a continuoussmooth distribution of magnitudes, and if theinterval also appears as an ‘‘outlier’’ in mag-nitude compared with the other intervals inits particular segment of the timescale, do weregard it as a ‘‘true’’ global mass extinction,different in magnitude from the bulk of as-sociated stratigraphic intervals.

How Continuous Are the Values of ExtinctionIntensity? As noted above, several analyseshave concluded that the distribution of extinc-tion intensities is apparently continuous(Quinn 1983, Bambach and Gilinsky 1986,Raup 1991, Wang 2003). Figure 3A shows thiseffect for proportion of genus extinction ar-ranged in rank order for the 107 stages andsubstages of the Phanerozoic as tabulated inour version of Sepkoski’s genus database.

Cambrian and Early Ordovician extinctionproportions, however, were consistently high(Table 1, Fig. 4). Sixteen of 19 Cambrian andEarly Ordovician intervals have extinction in-tensities that fall within the top quartile of allPhanerozoic intervals (Fig. 3A). Originationwas unusually high, as well, during this in-terval. Thus, whereas taxonomic turnover atthe genus level was great, overall diversity didnot fluctuate wildly (Fig. 1 and discussion be-low). These turnover rates are not like those ofmuch of the later Phanerozoic. For example,the decrease in proportion of extinction ob-served in the Early Ordovician (Fig. 4A) wasnot produced by the radiation of taxa withlower extinction rates diluting continuinghigh extinction rates in the trilobites, whichdominated Cambrian diversity. Instead, ex-tinction proportions for trilobites, which hadconsistently exceeded those of the non-trilo-bite fauna from the origin of the clade in theearly Atdabanian though the early Arenigian(Foote 1988), dropped to the same level asnon-trilobite proportions of extinction during


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-rable levels thereafter (Fig. 4C). Clearly some-thing changed for trilobite evolutionary dy-namics in the later part of the Early Ordovi-cian. Although the change was not as dramaticfor the non-trilobite fauna, extinction propor-tions for that fraction of the fauna, which hadbeen over 30% in two-thirds of the intervals ofthe Cambrian and Early Ordovician, droppedto levels below 30% and remained low untilthe Middle Silurian, except for the end-Or-dovician late Ashgillian extinction event. Pro-portions of extinction never returned consis-tently to the high levels common in the Cam-

brian and Early Ordovician, even when pro-portions of extinction increased for extendedintervals, such as from the Middle Silurian tothe mid-Carboniferous—this held for trilo-bites and non-trilobites alike.

We do not yet understand why turnoverrates should have been so high during theCambrian and Early Ordovician. Perhaps ear-ly animals were more vulnerable to extinctionfor functional reasons—many Cambrian ani-mals belonged to stem rather than crowngroups of bilaterian phyla and classes (Buddand Jensen 2000). Perhaps the low diversity ofCambrian and Early Ordovician animals con-


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FIGURE 4. Genus extinction by interval in stratigraphic(time) order. A, Proportion of genus extinction. TheCambrian and Early Ordovician concentration of veryhigh proportions is highlighted. That concentration isfurther emphasized because only six of the 88 post-Ar-enigian intervals rise above the dashed horizontal lineat 40% genus extinction. B, Natural logarithms of theproportion of genus extinction. Intervals of generallyhigh or low proportion of extinction are emphasized bythe fluctuation of the majority of points within blocks oftime intervals above and below the horizontal linedrawn at the lowest proportion in the Cambrian andLate 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 naturallog of 40% genus extinction). Intervals identified in Fig-ure 5 as forming a group of outliers (the late Ashgillianin the Ordovician, the Guadalupian and Djhulfian at theend of the Permian, and the Maastrichtian at the end ofthe Cretaceous) are highlighted. C, Proportion of genusextinction of trilobites and non-trilobites during theCambrian and Ordovician (except the end-Ordovician).Note the shift of trilobites to magnitudes similar to non-trilobites during the last two intervals of the Early Or-dovician and the lower proportions of all after that.


tributed to low ecosystem stability (Bambachet al. 2002); many modes of life now heavilyoccupied were either vacant or contained fewtaxa (Bambach 1983, 1985). Or perhaps phys-ical environments experienced unusual per-turbation during this interval, as might be in-ferred from the carbon isotope record (Brasierand Sukhov 1998; Saltzman et al. 2000).

Whether we know the cause or not, the ob-served patterns of turnover show that Cam-brian and Early Ordovician extinction ratesform a distinct stratigraphic grouping that dif-fers from the remainder of the PhanerozoicEon. Statistically, it is extremely unlikely thatthe proportion of extinction in as many as 16of the 19 Cambrian and Early Ordovician in-tervals would fall within the top quartile of allPhanerozoic values if there were nothing un-usual about that segment of time (p 50.000000002, calculated by using the hyper-geometric distribution). Thus, we removedthese data and replotted the distribution of ex-tinction intensities.

The resulting rank order distribution ofmid-Ordovician to Recent extinction intensi-ties (Fig. 3B) retains the original smoothlycontinuous appearance except for six intervalsat the upper end: four of the ‘‘big five’’ (theend-Ordovician, end-Permian, end-Triassic,and end-Cretaceous) and the two intervalsthat bracket the terminal Permian interval.The high Guadalupian intensity just beforethe end-Permian Djhulfian likely combinestrue extinction (Stanley and Yang 1994; Jin etal. 2000) with Signor-Lipps range truncations(Signor and Lipps 1982; Jablonski 1986; Raup1987) from the exceptionally severe end-Perm-ian event. The initial Triassic interval (the In-duan) was a time of low diversity followingthe end-Permian devastation, and the cause ofits high extinction intensity has yet to be de-termined.

The distribution of extinction intensities forthe post-Arenig (Fig. 3B) still can be regardedas a continuous distribution, but one that ismore skewed than that for the entire Phaner-ozoic—the coefficient of skewness for the totalPhanerozoic was 0.89 whereas that for thepost-Arenig is 1.37. However, it is extremelyunlikely that removing 19 randomly selectedintervals (consecutive or non-consecutive)

would increase the coefficient of skewness tosuch an extent (p , 0.0001, calculated by sim-ulation). The sparseness of the remaining highvalues raises the question of whether thosemagnitudes are actually outliers that can beregarded as a separate group from the bulk oflower values.

Do All Intervals That Appear Discontinuouswith the Bulk of Post-Arenig Intervals Form aGroup of Outliers When Compared with Their ‘‘Lo-cal’’ Segment of Geologic Time? We can test di-rectly for the continuity of magnitude be-tween background and potential mass extinc-tions in a temporal context. Because the focusof this paper is on the ‘‘big five’’ mass deple-tions, which are all post-Arenig in age and be-cause the Cambrian and Early Ordovician arenot comparable in evolutionary dynamics (forwhatever reason, as noted above), we restrict-ed the following analysis to the post-Arenigportion of the Phanerozoic.

We tested for continuity of magnitude be-tween background and mass extinctions overthe 88 post-Arenig intervals. To control for thefluctuation in local extinction regimes appar-ent in the grouping of intervals in Table 1 (forwhich the boundaries were chosen where thechange in extinction proportions seen in Fig.4 were greatest) we used time-adjusted datarather than the raw extinction intensities. Todo this, we first fit a smooth lowess curve tothe raw extinction intensities (Fig. 5A). Low-ess (‘‘Locally Weighted Scatterplot Smoother’’[Cleveland 1979]) is a nonlinear regressionmethod that smoothes out the noise in a timeseries or scatterplot in order to emphasize thesignal. To use lowess, one must first choose thevalue of a ‘‘bandwidth’’ parameter controllingthe degree of smoothing. We used a band-width of 11%, meaning that the smoothed val-ue for each interval is calculated as a weightedaverage of 11% of the surrounding intervals,with the intervals closest in time weightedmore heavily. We chose this value because theaverage length of a geologic time period in the470 million years after the Arenig is 52 millionyears, and 11% of 470 million is 52 million.Thus the smoothed value for each intervaltakes into account the extinction intensities ofthe surrounding intervals for a time equiva-lent to a geological period.


FIGURE 5. Statistical analysis of post-Arenig extinctionmagnitudes. A, Nonlinear lowess regression with 11%(52-million-year) bandwidth, revealing long-term fluc-tuation in extinction intensities. B, Histogram of resid-uals from nonlinear lowess regression with intervalshaving intensities comprising a statistically significantsecond mode (p 5 0.028) identified. The Induan and theupper Norian are the last two intervals at high end tailof the main mode (time-adjusted values of 0.168 and0.204), but they still lie well below the range of the sec-ond mode (0.307–0.416). The late Frasnian time-adjust-ed value of 0.062 is only the twelfth highest in the mainmode and is one of ten values in the second bin abovethe mode.

We then calculated the residuals, the differ-ence between each interval’s extinction inten-sity and its lowess smoothed value. Usingthese residuals, we applied the critical band-width test (Silverman 1981), previously usedby Wang (2003) to test for continuity of mag-nitude over the entire Phanerozoic. The ideaof this test, in this context, is as follows: Sup-pose there is a curve (i.e., a probability densityfunction) that models an underlying processfrom which extinction intensities are gener-ated. If this extinction intensity curve wereunimodal, we would infer that mass extinc-tions are the right tail of a continuum of ex-tinction intensities—that background andmass extinctions are continuous in magnitude.

On the other hand, a bimodal extinction in-tensity curve would suggest that backgroundand mass extinctions are discontinuous inmagnitude. The critical bandwidth test esti-mates the shape of the extinction intensitycurve and tests whether there is significant ev-idence to reject the null hypothesis that thecurve is unimodal. We found statistically sig-nificant evidence (p 5 0.028) for the existenceof a second mode in the right tail of the dis-tribution of extinction intensities (Fig. 5B). Thefour intervals that make up this second modeare, from highest to lowest, the Djhulfian,Maastrichtian, Upper Ashgillian, and Guad-alupian, confirming that only the end-Ordo-vician, end-Permian, and end-Cretaceoushave extinction magnitudes that would not beexpected in their local context and are not partof a continuum of extinction magnitudes.

Pattern of Temporal Change in Proportion of Ge-nus Extinction. Figure 4 plots the proportionof extinction in each interval arranged in tem-poral order. Although the numerous high val-ues of extinction intensity in the early and midPaleozoic and the consistently lower intensi-ties in the Jurassic through Cenozoic producethe decline in extinction through the Phaner-ozoic recognized by Raup and Sepkoski (1982)and discussed by Gilinsky (1994), that declineis not monotonic. Instead, there are strati-graphically coherent intervals with generallyhigher and lower proportions of extinctionthat are highlighted in Figure 4. Indeed, whenthe Cambrian–Early Ordovician data are re-moved from consideration, it is not obviousthat extinction intensities trend through timefor the remainder of the Phanerozoic; ratherwe see low intensities during the mid Ordo-vician–Early Silurian (except for the late Ash-gillian), Late Carboniferous–mid Permian,and Jurassic to present (except for the end-Cretaceous) separated by discrete intervals ofhigh extinction intensities during the MiddleSilurian–Early Carboniferous and later Perm-ian–Triassic. In total, then, the Phanerozoiccan be divided into six segments based onfluctuation in average extinction proportionper interval (Table 1, Fig. 4). Excluding thepost-Arenig intervals whose extinction ratesfall in a second mode in the lowess/criticalbandwidth analysis described above, the six


segments are apparent by inspection (Fig. 4)and are responsible for the pattern seen in thelowess regression in Figure 5A. Althoughorigination does not have as sharp or distincta set of changes from high to low proportions,the values of proportion of origination gener-ally parallel the pattern for extinction (as willbe seen in Fig. 6).

These six stratigraphically coherent seg-ments provide another ‘‘neighborhood’’ con-text in which variation in origination and ex-tinction may be more meaningfully judged,rather than comparing individual intervalsagainst the full range of values that accumu-lated during the Phanerozoic. Although a lin-ear regression on extinction proportionsthrough the Phanerozoic does have a negativeslope, the decline in extinction rate over timeis caused by three sets of fluctuation betweenconsistently higher and lower rates, with thenegative slope of a linear regression largelydetermined by the anomalously high propor-tions of the Cambrian and Early Ordovicianand the predominantly low rates since the Tri-assic. We make this observation to suggest thatif the pattern of extinction over time is to becharacterized it would be best to model it as athree-phase system, not a monotonic function(nor a two-phase system as suggested by VanValen [1984]).

Using the stratigraphic groupings of inter-vals with similar extinction intensities (Table1, Fig. 4), we see how the outlier intensitiesfrom the critical bandwidth test look withinindividual segments of time. We show this inboth the arithmetic plot (Fig. 4A) and con-verting the proportions to natural logarithms(Fig. 4B). The end-Ordovician (late Ashgillian)and end-Cretaceous (Maastrichtian) pointsare obvious outliers, falling in intervals ofgenerally low proportions of extinction. If thelater Permian points (Guadalupian and Djhul-fian) are regarded as belonging with the restof the Permian (which could be justified be-cause (a) their fauna is taxonomically a contin-uation of the earlier Permian fauna and (b) aswill be noted below, the origination rates forthese two intervals remain in the range of theearlier Permian) they, too, would be extremeoutliers, but if they are grouped with the ele-vated proportions characteristic of the Triassic

they are still clearly higher than any of thoseproportions. However, the late Frasnian (inthe Late Devonian) and the late Norian/Rhaetian (at the end of the Triassic) had ex-tinction proportions that do not appear as out-liers for the larger time segment to which eachbelongs, although the end-Triassic point ishigher than the others in the Triassic.

Three, Not Five, Global Mass Extinctions. Weconclude there is a class of statistically distinctglobal mass extinctions, but that it containsonly three members: the end-Ordovician, end-Permian, and end-Cretaceous. These resultsparallel the conservative bootstrap statisticalanalysis of Hubbard and Gilinsky (1992), whoalso found only these same three unambigu-ous high extinction magnitudes in their anal-ysis.

The other two traditional mass extinctionintervals do not fulfill the criteria for unusualextinction effect. The late Frasnian satisfiesnone of the criteria: it falls within the smoothcontinuum of post-Arenigian extinction mag-nitudes, it is not one of the magnitudes in thesecond mode of post-Arenigian magnitudesusing Silverman’s critical bandwidth test, andit is not an apparent outlier among the mid-Silurian through Early Carboniferous extinc-tion magnitudes. The end-Triassic is some-what more ambiguous because it is one of theintervals in the ‘‘off track’’ high-end tail of therank order distribution of post-Arenigianmagnitudes. However, although it falls at thehigh end of the main mode in Figure 5B, theend-Triassic event does not fall in the separatemode confirmed by the Critical BandwidthTest, nor is it distinctly different from otherTriassic extinction intensities. We do not claimthat the end-Frasnian and end-Triassic wereinnocent of pulsed extinctions, but we do inferthat, by itself, extinction is insufficient to ex-plain the strong diversity depletion at thesetimes.

The Interaction of Originationand Extinction

Paleontologists have focused on mass ex-tinctions as important evolutionary events forthe past quarter of a century or more, but withfew exceptions (e.g., Cutbill and Funnell 1967;Knoll 1989) they have paid less attention to


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 diversityequation. In general, origination has been a fo-cus of interest mostly for the early Paleozoicradiations (Knoll and Carroll 1999; Budd andJensen 2000; Connolly and Miller 2001) andthe recovery intervals following mass extinc-tions (Hart 1996).

The five intervals of diversity loss seen inFigures 1 and 2 have traditionally been re-garded as mass extinctions because extinctionmust have exceeded origination for diversityto drop so markedly during those intervals.However, this focus on extinction ignores twoconditions. One is that there is considerablegenus extinction during any interval of time(over 90% of the intervals of the Phanerozoichave 8% or greater genus extinction), yet whendiversity is maintained because extinction ismatched by origination we are not concernedabout its magnitude. Second is that origina-tion can fluctuate, yet origination is seldomtracked. If origination should fall below typi-cal values while extinction remained at its typ-ical level, diversity would decrease, yet nochange in extinction intensity would have oc-curred. How do the classic ‘‘big five’’ diversitydepletions reflect the interaction betweenorigination and extinction?

Interaction of Origination and Extinction inMajor Diversity Depletions. Figure 6 illus-trates both origination and extinction propor-tions through the Phanerozoic. By definition,

diversity was depleted when extinction wasgreater than origination, and, conversely, di-versity increased when origination exceededextinction. Diversity loss during intervalswhen origination rate was typical for thestratigraphic neighborhood can be ascribed toelevated extinction alone. On the other hand,diversity loss when extinction was not mark-edly higher than the average for its strati-graphic neighborhood must reflect sup-pressed origination—attrition by inadequatereplacement. The intervals during which di-versity decreased are circled on Figure 6 andthe ‘‘big five’’ diversity depletions are num-bered. Using the average proportion of origi-nation and extinction for the larger intervals inwhich each of the ‘‘big five’’ diversity deple-tions falls (Table 1), we can calculate the pro-portional influence (‘‘importance’’) of origi-nation compared with extinction on the loss ofdiversity in each major diversity depletion(Table 2).

During the end-Ordovician, end-Permian,and end-Cretaceous diversity depletions,rates of origination were slightly to markedlygreater than the average for their stratigraphicneighborhoods, whereas extinction rates wereexceptionally high (Fig. 7). By this criterion,then, these three intervals can be regarded astrue global mass extinctions because diversitydepletion in each was driven entirely by ele-vated extinction. Indeed, had rates of origi-


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FIGURE 7. Relationship between origination and extinction for the three mass diversity depletions that are truemass extinctions. Arrow marked O indicates the difference between the mean origination for the larger interval towhich each is assigned (Table 1), shown by a dashed horizontal line, and the actual origination in the mass depletioninterval. Arrow marked E indicates the difference between the mean extinction for the larger interval to which eachis assigned (Table 1), shown by a horizontal solid line, and the actual extinction magnitude in the mass depletioninterval. Diversity loss indicated by the vertical thin box between the origination and extinction values. A, LateAshgillian, at the end of the Ordovician. B, Djhulfian, at the end of the Permian (with marked diversity loss in thepreceding Guadalupian stage, as well). C, Maastrichtian, at the end of the Cretaceous.

nation during these intervals been no morethan average, diversity losses would actuallyhave been somewhat greater than they were(Table 2). The noticeably higher-than-averageproportion of origination in the Djhulfian(10% higher than the mean for the Late Car-boniferous and Permian) may reflect recoveryfrom the diversity loss in the Guadalupian,but the other two intervals have proportionsof origination only one to two-and-a-half per-cent higher than the average for their strati-graphic neighborhoods.

In contrast, the two remaining ‘‘big five’’mass depletions—the late Frasnian and theend-Triassic—reflect a more complicated im-balance between origination and extinction(Fig. 8). During both intervals, origination wasmarkedly lower than average for their strati-graphic neighborhoods. Although each inter-val registered somewhat elevated extinction,about two-thirds of the diversity loss in thelate Frasnian and almost 60% in the end-Tri-assic can be ascribed to origination failure, notelevated extinction (Table 2). McGhee (1988)originally emphasized that low originationwas a major factor in the Frasnian diversitydepletion, but it is only with this paper that

the role of origination failure is brought to thefore for both the Frasnian and the end-Trias-sic. Neither was an extinction event of themagnitude of the end-Ordovician, end-Perm-ian, and end–Cretaceous events, yet each qual-ifies as one of the ‘‘big five’’ post-Cambrian di-versity depletions because of moderately ele-vated extinction in concert with marked orig-ination failure.

Other intervals that have relatively highmagnitude of extinction are occasionally la-beled ‘‘mass extinctions,’’ but they do notshow dramatic losses of diversity. For exam-ple, the Kacak/otomari event near the end ofthe Eifelian in the Middle Devonian has beenassociated with impact ejecta in Morocco (Ell-wood et al. 2003), but the cited extinction of‘‘as many as 40% of all marine animal genera’’is actually 37% extinction for the entire 11-mil-lion-year-long Eifelian stage, not just the Ka-cak/otomari event (Sepkoski’s data, cited byEllwood et al. is only resolved to the full stagelevel for the Eifelian), and is nearly balancedby 33% origination, resulting in a net Eifeliandiversity loss of only 4%. Extinction was equalto the Eifelian level in the preceding Emsianand was actually greater in the Ludlovian of


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 theorigination and extinction values. A, Late Frasnian, in the Late Devonian. Note that several preceding intervals alsohave lower origination than extinction, indicating continuous diversity loss, although a drop in origination plus asmall peak of extinction concentrates more diversity loss in the late Frasnian. B, Late Norian/Rhaetian, at the endof the Triassic. In this case, proportion of origination decreased through most of the Triassic as diversity reboundedfrom the end-Permian mass depletion, but exceeded extinction except at the end of the Triassic, when originationwas at its low point and there was a small peak of extinction.

the Silurian, but in both instances originationalso nearly balanced extinction. Events thatrecord moderate extinction over short time in-tervals in some regions, like the Kacak/oto-mari episode, deserve close attention, but theyare simply not comparable to the end-Permianor end-Cretaceous devastations, nor were theyassociated with diversity depletions on a glob-al scale similar to those of the late Frasnian orend-Triassic.

Mass Depletions during the Cambrian. TheCambrian and Early Ordovician are unusualin having very low diversity and very highrates of faunal turnover. Figures 3A, 4, and 9Billustrate the preponderance of high propor-tional origination and extinction in this inter-val: 87% of the intervals in the Phanerozoicwith genus origination greater than 50% and68% of all intervals with genus extinctiongreater than 40% occur during the Cambrianand Early Ordovician. As noted above, it isstatistically highly unlikely that the prepon-derance of high extinction magnitude wasproduced by chance alone. What makes thiseven more unusual is that the durations ofmany subdivisions during this interval aremuch shorter than the average through the

rest of the Phanerozoic, yet taxonomic turn-over is greater (as can be seen by the relativesize of the turnover peaks compared with theboundary-crossing [minimum] diversity plotin Figs. 1 and 9A). Sepkoski’s (1996) strati-graphic subdivisions of Cambrian time maybe unrealistically small (e.g., Landing 1994),raising questions about the accuracy of his de-tailed correlations and calling his diversitynumbers for these fine-scale intervals intoquestion; however, combining these intervalsinto larger time divisions more comparable induration to those characteristic of younger pe-riods would result in even more pronouncedturnover rates because of the short ranges ofmany Cambrian taxa. As an example, propor-tion of origination in the Middle Cambrian asa whole was 0.691 and proportion of extinc-tion was 0.676, whereas origination averaged0.461 and extinction averaged 0.467 for each ofthe four intervals of the Middle Cambrian tab-ulated here. Thus, regardless of any over-op-timism in the designation of stratigraphic binsused by Sepkoski, the Cambrian and Early Or-dovician was an interval of unusual turnover.

Important extinctions have, of course, beenrecognized in the Cambrian. Signor (1992)


FIGURE 9. A, Genus diversity and diversity turnover through the Cambrian and Early Ordovician. Graph plottedas 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 originationand 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 massextinction (see also Zhuravlev and Wood1996). Archaeocyathan diversity collapsed,and small shelly fossil diversity declined aswell (although, as Porter [2003] has shown,loss of preservational opportunity clouds thepicture for the latter group). Nonetheless, Sep-koski’s data suggest that Botomian extinctionproportions for the total fauna were actuallylower than those of several other Cambrian in-tervals, and the marked late Botomian changefor the fauna as a whole reflects a drop in orig-ination, not an increase in extinction (Fig. 9B).The loss of diversity in the late Botomian wasnot because extinction proportion for arcaheo-

cyathids increased, but rather because propor-tions of origination for archaeocyathids, prob-lematica, hyolithids, and inarticulate brachio-pods all fell to one-fifth to one-third the valuesthey had maintained in the Atdabanian andearly Botomian. Among diverse groups in theEarly Cambrian, only the trilobites main-tained origination rates high enough to coun-ter attrition from the ‘‘normal’’ extinction pro-portions in the late Botomian.

The same is true for the early part of the lateMiddle Cambrian. Although Palmer’s (1984,1998) documentation of extinction at biomereboundaries may contribute to the high extinc-tion magnitudes in the Middle and Late Cam-


brian, the diversity loss of the early part of thelate Middle Cambrian interval stands outmostly for its low level of genus origination(Fig. 9B). Thus, the two Cambrian intervals ofdiversity depletion resemble the Late Devo-nian and end-Triassic more closely than theydo the three unambiguous global mass extinc-tions.

In one way, this finding is more or less in-evitable. When mean rates of extinction standat 46% per interval, driving diversity deple-tion by increasing extinction rate is a tall order.However, the more specific question of whyarchaeocyathans, trilobites, and other Cam-brian dominants should have experienced de-clining rates of origination during these inter-vals has no clear answer at this time (as is alsothe case for the Frasnian and end-Triassic not-ed above). Perhaps changing Botomian oceanchemistry selected against the massive calci-fication that is the hallmark of archaeocy-athans (e.g., Rowland and Shapiro 2002). Andperhaps ocean circulation changed during thelate Middle Cambrian, influencing the shelfenvironments that supported marine diversi-ty. Compelling answers may come from cre-ative interactions between paleontology andEarth system geochemistry.

What about Continuity of Effectand Cause?

Although the ‘‘big five’’ global mass deple-tions of diversity do not share continuity ofmagnitude it might be that they share com-mon properties in terms of the biological ef-fects of diversity loss. This, however, does notappear to be the case.

Knoll et al. (1996) identified a distinct selec-tivity in end-Permian extinction in whichheavily calcified animals with low metabolicrates were devastated (88% genus extinction),whereas metazoans with high metabolic ratesand calcareous skeletons precipitated fromphysiologically buffered solutions (or withskeletons made from materials other thanCaCO3) were far less affected (49% genus ex-tinction), and more recent work is refining thepattern (Bambach and Knoll unpublisheddata). During the end-Ordovician and end-Cretaceous events, no selectivity of this sortoccurred. Sheehan et al. (1996) documented

selectivity differences in the patterns of ex-tinction for these two events that clearly dif-ferentiate between them, and neither resem-bles the Permian pattern. Thus, although theend-Permian and end-Cretaceous global massextinctions share one result—both devastatedantecedent ecosystems—the patterns of thetwo extinctions were different and their post-extinction recoveries distinct (Bambach et al.2002). As pointed out by Droser et al. (2000),Brenchley et al. (2001), and Sheehan (2001),and confirmed quantitatively by Bambach etal. (2002), the Ordovician global mass extinc-tion did not have a comparable effect on eco-system structure.

As an illustration of the difference in effectof the Ordovician and Permian extinctions, arecent study of brachiopods in South China(Rong and Shen 2002) noted that there wereno ordinal extinctions in the Ordovician eventand that there is a ‘‘close taxonomic and eco-logical relationship of pre- and post-extinctionbrachiopod associations’’ (p. 25). In contrast,four orders and 20 superfamilies disappearedin the end-Permian event, and very few Tri-assic brachiopods link back to the Permian atthe genus level. For the three unambiguousglobal mass extinctions, then, there are differ-ences in the physiological selectivity of theevents, the ecological impacts of the events,and the style of effect on particular taxa. Con-tinuity of effect is simply absent.

The two other global mass depletions differfrom the three global mass extinctions in nu-merous ways, including effect when the bal-ance between origination and extinction isconsidered, but they are still not well under-stood. The Frasnian event is complicated.Most workers accept that at least two pulses ofextinction occurred, in association with twoKellwasser black-shale horizons (see, for ex-ample, Chen and Tucker 2003). Extinctionpulses are also recorded in the Middle andLate Devonian (House 1985; McGhee 1996),especially the so-called Hangenberg event atthe end of the Famennian (House 1985; Si-makov 1993; Wang et al. 1993). Indeed, at thestage and substage levels, marine diversitydecreased almost continuously through Mid-dle and Late Devonian time (Fig. 1). Moreover,the marine fauna underwent dramatic turn-


over in dominant organisms (Bambach 1999).Copper (2002: p. 49) observed that reef distri-bution declined progressively from the Give-tian through the Frasnian, and stated thatthere is ‘‘no catastrophic reef ‘kill horizon’ atthe F/F boundary known anywhere in theworld.’’ Copper (2002) associated the ob-served decline with climatic and tectonicchange. Although the causes of reduced Fras-nian origination are not yet clearly known,loss of complex reef habitats could have facil-itated reduced origination by eliminating anormally diverse ecosystem.

The end-Triassic event is the least well un-derstood of the major diversity depletions. Asnoted above, this event was driven as much byorigination failure as by extinction, in contrastto the end-Ordovician, end-Permian, and end-Cretaceous events. Moreover, neither glacia-tion nor major biotic reorganization, charac-teristics associated with the end-Ordovicianand Late Devonian diversity depletions, ismanifest in the Late Triassic (although bothlarge plateau basalt eruptions and bolide im-pact have been implicated [Bice et al. 1992;Courtillot et al. 1996; Wignall 2001; Olsen etal. 2002]). Although complete and informativemarine sections are still being sought (Hallamet al. 2000), there are now proposals that ob-served terrestrial and marine extinctions maynot be synchronous (Palfy et al. 2000) and geo-chemical analyses that also suggest a double-pulsed event of some sort (Hesselbo et al.2002). In concluding a recent survey of end-Triassic data, Hallam (2002: p. 133) stated,‘‘Though the current evidence cannot deci-sively exclude it, the foregoing review doesnot favour a major T–J boundary catastrophe.’’

The five major mass depletions of diversityare so different in major features that it is clearthey cannot share common cause. Nor didthey have common effect, beyond major lossof diversity.

Could It All Be Artifactual?

Variability in the quality of the geologic re-cord has the potential to affect observed di-versity and it undoubtedly has affected someaspects of detailed interval-to-interval chang-es in apparent diversity (Peters and Foote2001, 2002; Smith et al. 2001; Kier 1974 1977).

One might, therefore, question whether ourconclusions reflect artifactual, rather than bi-ological, patterns in the fossil record. Couldthere be defects or biases in the record thatgive the appearance of major diversity deple-tions when none actually exist?

Although we do not deny that some of theapparent diversity change in each of the ‘‘bigfive’’ diversity depletions could be accentuat-ed by record failure, in none of these instancesis it reasonable to expect that tabulated diver-sity change was produced entirely by failure ofthe rock record. For instance, Raup (1978) onceestimated the amount of extinction at the endof the Permian was equivalent to an 85-mil-lion-year gap in the geologic record, some-thing obviously precluded by radiometricages of Permian and Triassic rocks near thePermo-Triassic boundary (Bowring et al.1998). Also, Raup’s (1982) efforts to model ex-tinction by elimination of large areas of theEarth—originally conceived as a test of im-pact scenarios for extinction, but equally ap-plicable to questions of record failure—pro-duced surprisingly small extinctions of generaand families (mean extinction of only 13.8% ofmarine genera and 12% of terrestrial families)when half our planet’s surface was eradicated.Record failure is simply not capable of pro-ducing apparent diversity fluctuations on thescale observed in the large global diversity de-pletions.

In summary, we believe that the major con-clusions articulated in this paper describe realchanges in the diversity of marine animalsthough Phanerozoic time.

Conclusions

Of 88 stage or substage intervals during the470 million years since the Early OrdovicianArenig, only five suffered a loss of diversitygreater than 13.5% of the number of marinegenera that entered the interval. These five in-tervals—the late Ashgillian at the end of theOrdovician, the late Frasnian in the Late De-vonian, the Djhulfian at the end of the Perm-ian, the late Norian/Rhaetian at the end of theTriassic, and the Maastrichtian at the end ofthe Cretaceous—have been grouped as the‘‘big five’’ mass extinctions, but they are betterregarded as mass depletions of diversity.


Two of the five mass depletions, the lateFrasnian and the end-Triassic, resulted pri-marily from attrition related to reduced orig-ination, rather than devastation from unusu-ally elevated extinction. Both intervals oc-curred during times of generally high extinc-tion, so lowered origination had severeconsequences for diversity. Extinction in thesetwo intervals was elevated above average fortheir stratigraphic neighborhoods, but in eachcase elevated extinction was responsible foronly a little more than one-third of the diver-sity loss, leaving the remainder to be ex-plained by reduced origination. A similar re-lationship between reduced origination anddiversity loss is seen in two Cambrian inter-vals with marked loss of diversity (the late Bo-tomian and the early part of the late MiddleCambrian).

On the other hand, diversity loss in the end-Ordovician, end-Permian, and end-Creta-ceous intervals resulted exclusively from ele-vated extinction. The extinction magnitudes ofthese three intervals are statistically differentfrom the extinction magnitudes in their strati-graphic neighborhoods; they can be regardedas ‘‘true’’ global mass extinctions.

Acknowledgments

We thank A. I. Miller and an anonymous re-viewer for many suggestions that helped toimprove the manuscript. A.H.K.’s researchwas supported, in part, by the NASA Astro-biology Institute. S.C.W. is grateful for fund-ing from the Swarthmore College ResearchFund and the Christian R. and Mary F. Lind-back Foundation.

Literature CitedBambach, R. K. 1983. Ecospace utilization and guilds in marine

communities through the Phanerozoic. Pp. 719–746 (Chapter15) in M. Tevesz and P. McCall, eds. Biotic interactions in re-cent and fossil benthic communities. Plenum, New York.

Bambach, R. K. 1985. Classes and adaptive variety: the ecologyof diversification in marine faunas through the Phanerozoic.Pp. 191–253 in J. W. Valentine, ed. Phanerozoic diversity pat-terns: profiles in macroevolution. Princeton University Press,Princeton, N.J.

Bambach, R. K. 1999. Energetics in the global marine fauna: aconnection between terrestrial diversification and change inthe marine biosphere. Geobios 32:131–144.

Bambach, R. K., and N. L. Gilinsky. 1986. Perspectives on thedistribution of origination and extinction during the Phan-erozoic. Geological Society of America Abstracts with Pro-grams 18:534.

Bambach, R. K., A. H. Knoll, and J. J. Sepkoski Jr. 2002. Anatom-ical and ecological constraints on Phanerozoic animal diver-sity in the marine realm. Proceedings of the National Acad-emy of Sciences USA 99:6854–6859.

Bice, D. M., C. R. Newton, S. McCauley, P. W. Reiners, and C. A.McRoberts. 1992. Shocked quartz at the Triassic-Jurassicboundary in Italy. Science 255:443–446.

Bowring, S. A., D. H. Erwin, Y. G. Jin, M. W. Martin, K. Davidek,and W. Wang. 1998. U/Pb zircon geochronology and tempoof the end-Permian mass extinction. Science 280:1039–1045.

Brasier, M. D., and S. S. Sukhov. 1998. The falling amplitude ofcarbon isotopic oscillations through the lower to middle Cam-brian: northern Siberia data. Canadian Journal of Earth Sci-ences 35:353–373.

Brenchley, P. J., J. D. Marshall, and C. J. Underwood. 2001. Doall mass extinctions represent an ecological crisis?’’ Evidencefrom the Late Ordovician. Geological Journal 36:329–340.

Budd, G. E., and S. Jensen. 2000. A critical reappraisal of thefossil record of the bilaterian phyla. Biological Reviews 75:253–295.

Bush, A. M., and R. K. Bambach. In press. Did alpha diversityincrease during the Phanerozoic? Lifting the veil of tapho-nomic, latitudinal, and environmental biases in the study ofpaleocommunities. Journal of Geology.

Bush, A. M., M. J. Markey, and C. R. Marshall. 2001. Estimatingbiodiversity in light of heterogeneous sampling intensities:the relationship between taxon-occurrence subsamplingmethods and alpha and beta diversity. PaleoBios 21(Suppl. toNo. 2):37.

Bush, A. M., M. J. Markey, and C. R. Marshall. In press. Alpha,beta, gamma: the effects of spatially organized biodiversityon sampling-standardization. Paleobiology.

Chen, D., and M. E. Tucker. 2003. The Frasnian-Famennian massextinction: insights from high-resolution sequence stratigra-phy and cyclostratigraphy in South China. Palaeogeography,Palaeoclimatology, Palaeoecology 193:87–111.

Cleveland, W. S. 1979. Robust locally weighted regression andsmoothing scatterplots. Journal of the American StatisticalAssociation 74:829–836.

Connolly, S. R., and A. I. Miller. 2001. Global Ordovician faunaltransitions in the marine benthos: proximate causes. Paleo-biology 27:779–795.

Copper, P. 2002. Reef development at the Frasnian/Famennianmass extinction boundary. Palaeogeography, Palaeoclimatol-ogy, Palaeoecology 181:27–65.

Courtillot, V. J.-J. Jaeger, Z. Yang, G. Feraud, and C. Hofmann.1996. The influence of continental flood basalts on mass ex-tinctions: where do we stand? In G. Ryder, D. Fastovsky, andS. Gartner, eds. The Cretaceous-Tertiary event and other ca-tastrophes in earth history. Geological Society of AmericaSpecial Paper 307:513–515.

Cutbill, J. L., and B. M. Funnell, 1967. Numerical analysis of thefossil record. Pp. 791–820 in W. B. Harland, W. B., C. H. Hol-land, M. R. House, N. F. Hughes, A. B. Reynolds, M. J. S. Rud-wick, G. E. Satterthwaite, L. B. Tarlow, and E. C. Willey, eds.The fossil record. Geological Society, London.

Droser, M. L., D. J. Bottjer, P. M. Sheehan, and G. R. McGhee.2000. Decoupling of taxonomic and ecologic severity of Phan-erozoic marine mass extinctions. Geology 28:675–678.

Ellwood, B. B., S. L. Benoist, A. El Hassani, C. Wheeler, and R.E. Crick. 2003. Impact ejecta layer from the Mid-Devonian:possible connection to global mass extinctions. Science 300:1734–1737.

Finney, S. C., W. B. N. Berry, J. D. Cooper, R. L. Ripperdan, W.C. Sweet, S. R. Jacobson, A. Soufiane, A. Achab, and P. J. Noble.1999. Late Ordovician mass extinction: a new perspectivefrom stratigraphic sections in central Nevada. Geology 27:215–218.


Foote, M. 1988. Survivorship analysis of Cambrian and Ordo-vician trilobites. Paleobiology 14:258–271.

Gilinsky, N. L. 1994. Volatility and the Phanerozoic decline ofbackground extinction intensity. Paleobiology 20:445–458.

Hallam, A. 2002. How catastrophic was the end-Triassic massextinction? Lethaia 35:147–157.

Hallam, A., and P. B. Wignall. 1999. Mass extinctions and sea-level changes. Earth-Science Reviews 48:217–250.

Hart, M. B., ed. 1996. Biotic recovery from mass extinctionevents. Geological Society of London Special Publication 102.

Hesselbo, S. P., S. A. Robinson, F. Surlyk, and S. Piasecki. 2002.Terrestrial and marine extinction at the Triassic-Jurassicboundary synchronized with major carbon-cycle perturba-tion: a link to initiation of massive volcanism? Geology 30:251–254.

House, M. R. 1985. Correlation of mid Paleozoic ammonoid evo-lutionary events with global sedimentary perturbations. Na-ture 313:17–22.

Hubbard, A. E., and N. L. Gilinsky. 1992. Mass extinctions asstatistical phenomena: an examination of the evidence usingx2 tests and bootstrapping. Paleobiology 18:148–160.

Jablonski, D. J. 1986. Causes and consequences of mass extinc-tions: a comparative approach. Pp. 183–229 in D. K. Elliott, ed.Dynamics of extinction. Wiley, New York.

Jablonski, D. J., K. Roy, J. W. Valentine, R. M. Price, and P. S. An-derson. 2003. The impact of the Pull of the Recent on the his-tory of marine diversity. Science 300:1133–1135.

Jackson, J. B. C., and K. G. Johnson. 2001. Measuring past bio-diversity. Science 293:2401–2404.

Jin, Y.-g., Y. Wang, W. Wang, Q. H. Shang, C. Q. Cao, and D. H.Erwin. 2000. Pattern of marine mass extinction near the Perm-ian/Triassic boundary in South China. Science 289:432–436.

Kier, P. M. 1974. Evolutionary trends and their functional sig-nificance in post-Paleozoic echinoids. Paleontological SocietyMemoir 5. Journal of Paleontology 48(Suppl. to No. 3).

———. 1977. The poor fossil record of the regular echinoid. Pa-leobiology 3:168–174.

Knoll, A. H. 1989. Evolution and extinction in the marine realm:some constraints imposed by phytoplankton. PhilosophicalTransactions of the Royal Society of London B 325:279–290.

Knoll, A. H., R. K. Bambach, D. E. Canfield, and J. P. Grotzinger.1996. Comparative earth history and Late Permian mass ex-tinction. Science 273:452–457.

Knoll, A. H., and S. B. Carroll. 1999. Early animal evolution:emerging views from comparative biology and geology. Sci-ence 284:2129–2137.

Landing, E. 1994. Lower Cambrian of southeastern Newfound-land: epeirogeny and Lazarus faunas, lithofacies-biofacieslinks, and the myth of a global chronostratigraphy. Pp. 283–309 in J. H. Lipps and P. W. Signor, eds. Origin and early evo-lution of the Metazoa. Plenum, New York.

Leakey, R. E., and R. Lewin. 1995. The sixth extinction: patternsof life and the future of humankind. Doubleday, New York,271 p.

MacLeod, N., and G. Keller, eds. 1996. Cretaceous-Tertiary massextinctions: biotic and environmental changes. Norton, NewYork.

McGhee, George R., Jr. 1988. The Late Devonian extinctionevent: evidence for abrupt ecosystem collapse. Paleobiology14:250–257.

———. 1996. The Late Devonian mass extinction. Columbia Uni-versity Press, New York.

———. 2001. The ‘multiple impacts hypothesis’ for mass extinc-tion: a comparison of the Late Devonian and the late Eocene.Palaeogeography, Palaeoclimatology, Palaeoecology 176:47–58.

Newell, N. D. 1962. Paleontological gaps and geochronology.Journal of Paleontology 36:592–610.

———. 1963. Crises in the history of life. Scientific American208(2):77–92.

———. 1967. Revolutions in the history of life. In C. C. AlbrittonJr., ed. Uniformity and simplicity. Geological Society of Amer-ica Special Paper 89:63–91.

Olsen, P. E., D. V. Kent, H. D. Sues, C. Koeberl, H. Huber, A.Montanari, E. C. Rainforth, S. J. Fowell, M. J. Szajna, and B.W. Hartline. 2002. Ascent of dinosaurs linked to an iridiumanomaly at the Triassic-Jurassic boundary. Science 296:1305–1307.

Palfy, J., J. K. Mortensen, E. S. Carter, P. L. Smith, R. M. Fried-man, and H. W. Tipper. 2000. Timing the end-Triassic massextinction: first on land, then in the sea? Geology 28:39–42.

Palmer, A. R. 1984. The biomere problem: evolution of an idea.Journal of Paleontology 58:599–611.

———. 1998. A proposed nomenclature for stages and series forthe Cambrian of Laurentia. Canadian Journal of Earth Scienc-es 35:323–328.

Peters, S. E., and M. Foote. 2001. Biodiversity in the Phanero-zoic: a reinterpretation. Paleobiology 27:583–601.

———. 2002. Determinants of extinction in the fossil record. Na-ture 416:420–424.

Porter, S. M. 2004. Closing the ‘‘phosphatization’’ window: test-ing for the influence of taphonomic megabias on the patternof small shelly fossil decline. Palaios 19:178–183.

Quinn, J. F. 1983. Comment on: mass extinctions in the fossil re-cord. Science 219:1239–1240.

Raup, D. M. 1978. Cohort analysis of generic survivorship. Pa-leobiology 4:1–15.

———. 1982. Biogeographic extinction: a feasibility test. In L. E.Silver and P. H. Schultz, eds. Geological implications of im-pacts of large asteroids and comets on the Earth. GeologicalSociety of America Special Paper 190:277–281.

———. 1987. Mass extinction: a commentary. Palaeontology 30:1–13.

———. 1991. A kill curve for Phanerozoic marine species. Pa-leobiology 17:37–48.

Raup, D. M., and J. J. Sepkoski Jr. 1982. Mass extinctions in themarine fossil record. Science 215:1501–1503.

Rong, J.-y., and S.-z. Shen. 2002. Comparative analysis of theend-Permian and end-Ordovician brachiopod mass extinc-tions and survivals in South China. Palaeogeography, Palaeo-climatology, Palaeoecology 188:25–38.

Rowland, S. M., and R. S. Shapiro. 2002. Reef patterns and en-vironmental influences in the Cambrian and earliest Ordo-vician. In W. Kiessling, E. Flugel, and J. Golonka, eds. Phan-erozoic reef patterns. SEPM Special Publication. 72:95–128.

Saltzman, M. R., R. L. Ripperdan, M. D. Brasier, K. C. Lohmann,R. A. Robison, W. T. Chang, S. C. Peng, E. K. Ergaliev, and B.Runnegar. 2000. A global carbon isotope excursion (SPICE)during the Late Cambrian: relation to trilobite extinctions, or-ganic-matter burial and sea level. Palaeogeography, Palaeo-climatology, Palaeoecology 162:211–223.

Sepkoski, J. J., Jr. 1981. A factor analytic description of the Phan-erozoic marine fossil record. Paleobiology 7:36–53.

———. 1982. A compendium of fossil marine families. Milwau-kee Public Museum Contributions to Biology and GeologyNo. 51.

———. 2002. A compendium of fossil marine animal genera.Bulletins of American Paleontology No. 363.

Sepkoski, J. J., Jr., R. K. Bambach, D. M. Raup, and J. W. Valentine.1981. Phanerozoic marine diversity: a strong signal from thefossil record. Nature 293:435–437.

Sheehan, P. M. 2001. The Late Ordovician mass extinction. An-nual Reviews of Earth and Planetary Science 29:331–364.

Sheehan, P. M., P. J. Coorough, and D. E. Fastovsky. 1996. Bioticselectivity during the K/T and Late Ordovician extinctionevents. In G. Ryder, D. Fastovsky, and S. Gartner, eds. The


Cretaceous-Tertiary event and other catastrophes in earth his-tory. Geological Society of America Special Paper 307:477–489.

Signor, P. W. 1992. Taxonomic diversity and faunal turnover inthe Early Cambrian: did the most severe mass extinction ofthe Phanerozoic occur in the Botomian stage? In S. Lidgardand P. R. Crane, eds. Fifth North American PaleontologicalConvention, Abstracts and program. Paleontological SocietySpecial Publication 6:272.

Signor, P. W., and J. H. Lipps. 1982. Sampling bias, gradual ex-tinction patterns, and catastrophes in the fossil record. In L.E. Silver and P. H. Schultz, eds. Geological implications of im-pacts of large asteroids and comets on the Earth. GeologicalSociety of America Special Paper 190:291–296.

Silverman, B. W. 1981. Using kernel density estimates to inves-tigate multimodality. Journal of the Royal Statistical Society B43:97–99.

Simakov, K. V. 1993. Biochronological aspects of the Devonian-Carboniferous crisis in the regions of the former U.S.S.R. Pa-

laeogeography, Palaeoclimatology, Palaeoecology 104:127–137.

Smith, A. B., A. S. Gale, and N. E. A. Monks. 2001. Sea-levelchange and rock-record bias in the Cretaceous: a problem forextinction and biodiversity studies. Paleobiology 27:241–253.

Stanley, S. M., and X. Yang. 1994. A double mass extinction atthe end of the Paleozoic era. Science 266:1340–1344.

Van Valen, L. M. 1984. A resetting of Phanerozoic communityevolution. Nature 307:50–52.

Wang, K., M. Attrep, and C. J. Orth. 1993. Global iridium anom-aly, mass extinction, and redox change at the Devonian-Car-boniferous boundary. Geology 21:1071–1074.

Wang, S. C. 2003. On the continuity of background and massextinction. Paleobiology 29:455–467.

Wignall, P. B. 2001. Large igneous provinces and mass extinc-tions. Earth-Science Reviews 53:1–33.

Wignall, P. B., and R. J. Twitchett. 1996. Oceanic anoxia and theend Permian mass extinction. Science 272:1155–1158.

Zhuravlev, A. Yu., and R. A. Wood. 1996. Anoxia as the causeof the mid-Early Cambrian (Botomian) extinction event. Ge-ology 24:311–314.

Origination, extinction, and mass depletions of marine diversity · 2004-11-01 · mass extinction intervals. Indeed, Raup (1991) developed his view of the Phanerozoic kill curve

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