Bryozoan Generic Extinctions and Orginations During the ... · BRYOZOAN GENERIC EXTINCTIONS AND ORIGINATIONS DURING THE LAST ONE HUNDRED MILLION YEARS Frank K. McKinney and Paul D

Palaeontologia Electronica http://palaeo-electronica.org

BRYOZOAN GENERIC EXTINCTIONS AND ORIGINATIONS DURING THE LAST ONE HUNDRED MILLION YEARS

Frank K. McKinney and Paul D. TaylorFrank K. McKinney. Department of Geology, Appalachian State University, Boone, North Carolina 28608, USA. Honorary Research Fellow, Department of Palaeontology, The Natural History Museum, Cromwell Road, London, UKPaul D. Taylor. Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

ABSTRACT

Stage-level analysis of extinctions and originations of bryozoan genera of theorders Cyclostomata and Cheilostomata for the Upper Cretaceous and Cenozoicyields some predictable and some unexpected results. Extinction rates in cyclostomesand cheilostomes track one another except for some lower Upper Cretaceous stagesin which apparently random extinctions among the small numbers of cheilostome gen-era generated ‘noise’. Both orders experienced high rates of extinction during or at theend of the Maastrichtian (our data cannot resolve position of extinctions within a stage)but, surprisingly, Danian extinction rates were essentially equal to Maastrichtian rates.High extinction rates for the Danian are attributed to loss of the ‘chalk’ sea of northernEurope, which was a centre of bryozoan diversity from early in the Late Cretaceousuntil its disappearance at the end of the Danian. Origination rates of cyclostomes andcheilostomes were similar and relatively high during the Late Cretaceous, but followingthe K-T extinction event, cyclostome origination rates dropped and remained at lowlevels through the Cenozoic, while cheilostome origination rates rebounded by theEocene and then declined through the Pleistocene. The different Cenozoic diversitytrajectories of cyclostomes and cheilostomes appear to derive primarily from differ-ences in origination rather than extinction rates.

KEY WORDS: extinctions, originations, Cretaceous-Tertiary, K-T, benthic invertebrates

Copyright: Palaeontological Association, 22 June 2001Submission: 9 February 2001 Acceptance: 23 May 2001

INTRODUCTION

Much attention has been focused onthe K-T extinction since the now famoushypothesis of bolide impact was first

mooted in 1980. Substantial informationhas been amassed and used to addressissues relating to the causal mechanism(s)of the extinction (e.g., Alvarez et al. 1980,Bohor et al. 1984, Venkatesan and Dahl

McKinney, Frank K. and Paul D. Taylor, 2001. Bryozoan Generic Extinctions and Originations During the Last One Hundred Million Years. Palaeontologia Electronica, vol. 4, issue 1, art. 3: 26pp., 2.4MB. http://palaeo-electronica.org/2001_1/bryozoan/issue1_01.htm

FRANK K. MCKINNEY & PAUL D. TAYLOR: BRYOZOAN EXTINCTIONS AND ORIGINATIONS

1989, Hildebrand and Boynton 1990, Izettet al. 1991), as well as to patterns ofextinction and recovery experienced byparticular groups of organisms (e.g.,Jablonski and Raup 1995, Marshall andWard 1996, Sheehan et al. 1996,MacLeod et al. 1997, d’Hondt et al. 1998,Jablonski 1998, Smith and Jeffrey 1998).With regard to the latter, biological groupswith more utilitarian fossil records (e.g.,planktonic foraminifera) or broad scientificand public appeal (e.g., dinosaurs) havereceived the most attention, whereas rela-tively little is currently known about extinc-tion patterns in many other groups,including bryozoans.

Bryozoans are a phylum of colonialmetazoans with a rich marine fossil recorddue to the readily fossilisable calcareousskeletons possessed by most species.Two clades of calcareous bryozoans arerepresented in the Cretaceous and Ceno-zoic, cyclostomes (Class Stenolaemata)and cheilostomes (Class Gymnolaemata).Both clades were diverse during the LateCretaceous; however, knowledge of theirsystematics is woefully inadequate—manyspecies have yet to be formally describedand others remain unrevised and are virtu-ally unrecognisable using the originaldescriptions published in the 19th Century.This lack of knowledge is compounded forthe cyclostomes which, in contrast with theskeletally more complex cheilostomeswhere a close correspondence has beendemonstrated between genetically andskeletally determined species (Jacksonand Cheetham 1990), have relatively sim-ple and easily confounded morphologies(McKinney and Jackson 1989; Håkanssonand Thomsen 1999). Ranges of species intime and space at all scales of resolution,from single stratigraphical sections to glo-bally, are poorly documented, and almostnothing is known about phylogenetic rela-tionships that might aid the interpretationof extinction patterns (e.g., Smith and Jef-

fery 1998, for echinoids). Despite theseproblems in documentation, the complete-ness of the fossil record apparently israther high for bryozoan genera, with anapproximately 70 percent probability of thepreservation of a genus in each strati-graphic stage throughout its range (Footeand Sepkoski 1999). With regard to globalpatterns, the finest level of analysis thatcan reasonably be attempted at presentfor bryozoan genera is at the level of thestratigraphical stage/age, as done, forexample, by Viskova (1980, 1997).

Alternative approaches to understand-ing the historical record of bryozoans havelooked at changes in species assemblagediversity and in relative skeletal biomassaround and across the K-T boundary (Lid-gard et al. 1993; McKinney et al. 1998, inpress). The only bed-by-bed study of bryo-zoan species distributions across the K-Tboundary is that of Håkansson and Thom-sen (1999) at Nye Kløv in Denmark. In thispaper, we track the history of originationsand extinctions of Late Cretaceousthrough Cenozoic bryozoans at the genuslevel. Therefore, we utilise primarily theglobal record of temporal distribution ofthe genera rather than local speciesassemblage diversities or skeletal biom-ass.

The existence of two distinct clades ofbryozoans crossing the K-T boundary pro-vides a replicate data-set of extinction andorigination patterns, thereby lesseningpotential problems caused by factors spe-cific to one clade. Cyclostomes date backin the fossil record to the Lower Ordovi-cian, cheilostomes to the Upper Jurassic(Taylor 1993). Each group is thought tohave acquired its mineralised skeletonindependently from a bryozoan of ctenos-tome-grade and to share a commonancestor no younger than Early Ordovi-cian (Todd 2000). They show importantdifferences in zooidal baupläne, whichapparently are linked with the greater rate

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of suspension feeding, growth rate, and –in tropical and temperate waters – abilityto compete for substrate space in cheilos-tomes (McKinney 1993, 1995; but seeBarnes and Dick 2000 for reversal of com-petitive interactions in high latitudewaters). Species belonging to the twoclades commonly co-exist and competewith one another in the same habitats, anda comparable range of colony forms isdeveloped in the two clades. Cyclostomesand cheilostomes, therefore, occupybroadly similar ‘ecospace’; however, somecheilostomes have invaded brackishwaters and a few others have evolvedfree-living colonies, while cyclostomeshave done neither. Other than these twocategories of exceptions, the two cladesmight be expected to show parallelresponses to the majority of environmentalchanges.

To put our consideration of extinctionat the K-T boundary into a broader evolu-tionary context for the phylum and to iden-tify other times of enhanced genericturnover during the past 100 millionyears—whether resulting from changes inextinction or origination rates - we analy-sed a new database of uppermost LowerCretaceous to Recent (Albian-Recent)bryozoans containing genus ranges atstage/age-level precision. The three prin-cipal questions we set out to address ini-tially were

1. Did generic extinction of Albian-Recent bryozoans peak in the Maastrich-tian, corresponding with the K-T event?

2. Are temporal patterns of genericextinction and origination intensities thesame for cheilostomes and cyclostomes?

3. Do generic origination rates supportVoigt's (1981) notion of the Danian as astage of low 'creativity'?

DATA AND METHODS

Stage-level ranges for Albian-Recentcheilostome and cyclostome bryozoan

genera were provided by J. J. Sepkoski,Jr. from his unpublished global genusdatabase. Accuracy of the database waschecked by us, resulting in various alter-ations to about 20 percent of the records,largely changes in ranges but also includ-ing elimination of some synonyms, addi-tion of some genera, and reassignment ofa few genera from cyclostomes to cheilos-tomes or vice versa. This proportion oferrors is consistent with the findings ofAdrain and Westrop (2000) for trilobites inSepkoski’s database, and like they, wefound that the error was randomly distrib-uted, so that results of analyses based onthe database did not differ greatly betweenthe original and corrected versions.

The analysed data comprised 808genera (545 cheilostomes; 263 cyclos-tomes), of which 24 percent are confinedto one stage. Origination and extinctionmetrics were calculated both with andwithout such stage-only genera. Error barsfor the origination and extinction metricswere calculated using the ‘PercentageError Bars’ program, freeware availablefrom Steve Holland at http://www.uga.edu/~strata/Software.html. The program isbased on a calculation procedure given inRaup (1991).

The Gradstein and Ogg (1996) times-cale was used for stage boundary dates.Numbers of appearances and disappear-ances, hereby referred to as originationsand extinctions respectively, per strati-graphic interval constitute the raw dataand must be calibrated in order to be ofmost use. The method of calibration, how-ever, has not been standardised, withextinctions and originations variouslybeing presented as (1) number per millionyears (N/myr); (2) proportion of standingdiversity (i.e., per capita rate; N/D); and (3)number per million years as a proportionof standing diversity (N/D/myr). In addition,one may include or exclude taxa that areconfined to the stratigraphic interval beingstudied (e.g., stage, series). Foote (1994)

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used Monte Carlo simulations to examinethe validity of extinction and originationmetrics. He concluded that normalisingper-taxon extinction rate by introducinguniform time intervals (e.g., per millionyears) potentially introduces bias, espe-cially for extinction metrics. Apparently, theproblem cannot be entirely avoided, but‘For comparing extinction intensity over asmall number of intervals, it may still besafest to check for concordance amongseveral metrics’ (Foote 1994, p. 442). Inthis paper, we present the three types ofmetrics listed above, both with and withouttaxa confined to a single stage, and exam-ine degree of concordance among them.

Recently, Foote (2000b) discussedproblems of bias in origination and extinc-tion rates due to incomplete knowledge oftemporal distribution of taxa, the effects ofvariable interval length (e.g., in the analy-sis here, stages vary over almost an orderof magnitude, from 1.6 to 13.3 myr), andpossible secular trends in probability ofpreservation. He reviewed the variousmeasures used to estimate origination andextinction rates and advocated use ofmeasures in which interval-only taxa (‘sin-gletons’) become irrelevant, because boththeir inclusion or exclusion can introduceerror. Such measures, therefore, arebased only on taxa that cross rangeboundaries. We have nonetheless usedthe more straightforward calculations oforigination and extinction rates asdescribed above. We have done so forthree reasons. First, we find no systematiceffect of increased stage duration on ratesof origination and extinction in our data(Figure 1). Secondly, exclusion and inclu-sion of stage-only genera produces onlyminimal differences in the rates plotted,and in some instances is of interest initself. Thirdly, the major points of interest inthe study (i.e., the anomalously highMaastrichtian and Danian extinction rates)are so far above background rates that

they should stand out in virtually anymethod of calculation of rates.

RESULTS

Table 1 summarises the data oncheilostome and cyclostome genericdiversity changes.Standing diversities

Following the end-Palaeozoic extinc-tion, cyclostome bryozoans reappear in

Figure 1. Relationship between stage duration andrates of origination and extinction. A. Origination rate(originations/standing diversity/myr) plotted againststage duration; r = 0.145. B. Extinction rate (origina-tions/standing diversity/myr) plotted against stage dura-tion; r = 0.173.

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the fossil record by the Carnian Stage ofthe Upper Triassic (Bizzarini and Braga1981). They diversified slowly through theLate Triassic and Early Jurassic but morerapidly during the Mid Jurassic and EarlyCretaceous. Sixty-three genera are known

from the latest Early Cretaceous (Albian),the oldest stage included in this study.During the Late Cretaceous, cyclostomessteadily increased in diversity to the 170genera known in Maastrichtian rocks (Fig-ure 2). They declined drastically from the

Table 1. Summary of data on cheilostome and cyclostome generic first and last records, genera confined to a singlestage, and standing diversity.

Cheilostome genera Cyclostome genera

stage Midpoint (myr)

duration (myr)

cheilolasts

cheilo firsts

stage only

standing cyclolasts

cyclo firsts

stage only

standing

Albian 105.6 13.3 3 4 1 10 2 3 0 63

Cenomanian 96.2 5.4 8 31 7 44 9 28 6 95

Turonian 91.3 4.5 4 14 2 45 2 11 0 91

Coniacian 87.4 3.2 8 30 5 74 2 18 1 108

Santonian 84.7 2.3 11 23 4 88 1 6 0 111

Campanian 77.4 12.2 21 47 6 126 14 22 3 135

Maastrichtian 68.2 6.3 55 60 26 185 61 34 18 170

Danian 63 4.1 33 31 13 148 26 6 3 100

Thanetian (& Seelandian)

57.9 6.1 20 19 4 125 7 4 0 75

Ypresian 51.9 5.8 5 29 3 133 1 5 0 73

Lutetian 45.2 7.7 12 49 8 182 3 2 0 74

Bartonian 39.2 4.3 6 36 3 201 2 2 1 74

Priabonian 35.4 3.3 24 29 4 225 10 5 3 79

Rupelian 31.1 5.2 13 10 1 208 2 5 0 71

Chattian 26.2 4.7 5 8 1 203 1 1 0 70

Aquitanian 22.2 3.3 6 14 5 216 1 0 0 69

Burdigalian 18.5 4.1 13 28 7 240 3 3 1 72

Langhian 15.6 1.6 6 9 5 234 1 2 0 70

Serravalian 13 3.6 13 18 9 250 4 4 2 75

Tortonian 9.2 4.1 6 10 2 240 5 0 0 69

Messinian 6.2 1.8 9 8 5 245 3 0 0 64

Zanclean 4.4 1.7 5 7 0 238 4 2 2 65

Piacenzian 2.7 1.8 6 9 3 245 6 3 2 64

Pleistocene 0.9 1.8 4 8 1 245 1 2 0 58

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Maastrichtian to the Thanetian and thenremained at an approximately constantdiversity level through the Cenozoic. (Notethat Figure 2 plots only fossil diversity;Holocene data are not plotted.)

Cheilostomes first appeared in theLate Jurassic (Taylor 1994) but diversified

very slowly during the Early Cretaceous,with only 10 genera known from theAlbian. During the Late Cretaceous,cheilostomes diversified rapidly to reach alevel of 185 known genera in the Maas-trichtian (Figure 2). Subsequently, theydeclined through the Palaeocene to aThanetian diversity of 125 genera. Afterthe Thanetian, they again diversifiedthrough much of the remaining Cenozoic,interrupted by a modest Oligocene rever-sal, apparently reaching a plateau of 240to 250 genera during the Neogene.Extinctions

The absolute number of extinctions forboth clades is highest for the Maastrich-tian (Figure 3). Sixty-one cyclostome gen-era that ranged through two or morestages have their last record in the Maas-trichtian, and 18 are known only from theMaastrichtian, making a total of 79 Maas-trichtian cyclostome genera that did notsurvive beyond the K-T boundary. Fifty-five long-ranged cheilostome genera havetheir last record in the Maastrichtian, and26 are known only from that stage, total-ling 81 Maastrichtian cheilostomes that did

Figure 2. Standing diversity of cyclostome and cheilos-tome bryozoans during the Late Cretaceous and Ceno-zoic. For this and other graphs displaying data throughtime, data are grouped by stage, and each point is plot-ted at mid-Stage.

Figure 3. Number of generic extinctions per stage. A. Including only genera known to range through two or morestages. B. All generic extinctions, including stage-only.

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not cross the K-T boundary. The second-highest number of extinctions occurredduring the Danian for both clades: 26 long-ranged plus 3 stage-only cyclostomes,and 33 long-ranged plus 13 stage-onlycheilostomes became extinct in theDanian. These Maastrichtian and Danianextinctions are much higher than extinc-tions in any other Late Cretaceous or Cen-ozoic stage. The next highest number ofextinctions for cyclostome generaoccurred during the Campanian (14 long-ranged plus 3 stage-only), and for cheilos-tomes during the Priabonian (24 long-ranged plus 4 stage-only).

Extinctions per million years (E/myr)were also high during the Maastrichtianand Danian both when the two clades areconsidered together (Figure 4A, B) andindividually (Figures 5A, B, 6A, B). Basedon genera not confined to a single stage,for cyclostomes Maastrichtian extinctionrate was 9.7 genera/myr and Danian rate6.3 genera/myr; for cheilostomes Maas-trichtian extinction rate was 8.7 genera/myr and Danian rate 8.0 genera/myr.Including stage-only genera, cyclostomeextinction rates were 12.5 genera/myr and7.1 genera/myr and cheilostome rateswere 9 genera/myr and 11.2 genera/myr,respectively. As with absolute numbers ofextinctions, these rate values are wellabove background levels (Figure 7A, B).The next highest rates for cyclostomes are3.3 genera/myr and 4.4 genera/myr(including stage-only genera) in thePiacenzian, and for cheilostomes 7.3 gen-era/myr and 8.5 genera/myr (includingstage-only genera) in the Priabonian.

Number of extinctions per standingdiversity (E/D) also peaked during theMaastrichtian and Danian (Figures 4C, D,5C, D, 6C, D). Cyclostome extinctionswere 0.38 genera/D (0.46 genera/Dincluding stage-only) for the Maastrichtian,and 0.26 genera/D (0.36 genera/D includ-ing stage-only) for the Danian. Values for

cheilostomes are 0.30 genera/D (0.44genera/D including stage-only) for theMaastrichtian, and 0.22 genera/D (0.33genera/D including stage-only) for theDanian. Again, these are well above back-ground levels (Figure 7C, D). Next highestvalues for cyclostomes are 0.13 genera/D(0.16 genera/D including stage-only) forthe Priabonian, and for cheilostomes 0.17genera/D (0.21 genera/D including stage-only) for the Campanian.

Finally, calibrating extinctions by bothstanding diversity and time (E/D/myr),Maastrichtian and Danian extinctions stillstand above background levels (Figures4E, F, 5E, F, 6E, F). Cyclostome extinc-tions were 0.06 genera/D/myr (0.07 gen-era/D/myr including stage-only) for theMaastrichtian, with the same values forthe Danian. Values for cheilostomes are0.05 genera/D/myr (0.07 genera/D/myrincluding stage-only) for the Maastrichtian,and 0.05 genera/D/myr (0.08 genera/D/myr including stage-only) for the Danian.While Maastrichtian and Danian extinc-tions per standing diversity per millionyears stand well above background level(Figure 7E, F), they are essentiallymatched in the Piacenzian for cyclos-tomes (0.05 genera/D/myr, and 0.07 gen-era/D/myr including stage-only), and in theSantonian for cheilostomes (0.05 genera/D/myr and 0.07 genera/D/myr includingstage-only).Originations

The absolute number of originationsfor both clades is highest for the Maas-trichtian (Figure 8). Thirty-four cyclostomegenera that ranged through two or morestages have their first record in the Maas-trichtian. Adding the 18 that are knownonly from the Maastrichtian brings the totalto 52 Maastrichtian cyclostome origina-tions. Sixty long-ranged cheilostome gen-era have their first record in theMaastrichtian. Adding the 26 that are

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Figure 4. Total bryozoan (cyclostome plus cheilostome) generic extinctions by stage. A, B. Extinctions per millionyears. C, D. Extinctions per standing diversity. E, F. Extinctions per standing diversities per million years. Graphs onthe left do not include genera known only from a single stage, and those on the right do include stage-only genera.Error bars represent 95% confidence intervals.


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Figure 5. Cyclostome generic extinctions by stage. See Figure 4 for explanation of layout.


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Figure 6. Cheilostome generic extinctions by stage. See Figure 4 for explanation of layout.


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Figure 7. Stage-level extinction intensities (without stage-only genera) arranged in ascending order.Extinctions per million years; A, cyclostomes, B, cheilostomes. C, D. Extinctions per standing diversity; C,cyclostomes, D, cheilostomes. Extinctions per standing diversities per million years; E, cyclostomes, F,cheilostomes.


known only from that stage brings totalMaastrichtian cheilostome originations to86. The second-highest number of cyclos-tome originations was during the Cenoma-nian when 28 long-ranged and six stage-only (making 34 in total) cyclostome gen-era appeared. The second-highest num-ber of cheilostome originations is found inthe Lutetian, which has the earliestrecords of 49 long-ranged and 8 stage-only genera (57 total).

Originations per million years (O/Ma)were also high near the transition fromCretaceous to Cenozoic (Figures 9A, B,10A, B, 11A, B). Maastrichtian cyclostomeoriginations were 5.4 genera/myr for long-ranged genera and 8.3 genera/myr includ-ing stage-only genera. However, cyclos-tome originations/myr were not abovebackground levels during the Danian (Fig-ure 12A). Instead, the Cenomanian hadoriginations/myr almost equal to the Maas-trichtian (5.2 genera/myr without and 6.3genera/myr with stage-only genera).Cheilostome originations/myr were highduring both stages: 9.5 genera/myr with-out and 13.7 genera/myr including stage-only genera for the Maastrichtian, and 7.6genera/myr and 10.7 genera/myr, respec-

tively, for the Danian. However, theseMaastrichtian and Danian values forcheilostome originations/myr scarcely dif-fer from those for the Coniacian, Santo-nian, Bartonian, and Priabonian (Figures11A, B, 12B).

Number of genera originating perstanding diversity (O/D) was high forcyclostomes during the Maastrichtian(0.20 genera/D for long-ranged and 0.33genera/D including stage-only genera),but these values are exceeded by thosefor the Cenomanian (Figures 10C, D, 12C)and are not much above those for theConiacian and Campanian. The value ofO/D for the Danian is not above back-ground levels. Cheilostome O/D for theMaastrichtian (0.32 genera/D for long-ranged and 0.46 genera/D includingstage-only genera) are exceeded by orapproximately equal all other Late Creta-ceous stages and were almost equalled byLutetian O/D values. Danian cheilostomegeneric O/D values are only slightly abovethe median value for all stages (Figures11C, D, 12D).

Originations calibrated by both stand-ing diversity and time (O/D/myr) for theMaastrichtian and Danian are even closer

Figure 8. Number of generic originations per stage. A. Including only genera known to range through two or morestages. B. All generic extinctions, including stage-only.

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Figure 9. Total bryozoan (cyclostome plus cheilostome) generic originations by stage. A, B. Originations per mil-lion years. C, D. Originations per standing diversity. E, F. Originations per standing diversities per million years.Graphs on the left do not include genera known only from a single stage, and those on the right do includestage-only genera. Error bars represent 95% confidence intervals.


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Figure 10. Cyclostome generic originations by stage. See Figure 9 for explanation of layout.


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Figure 11. Cheilostome generic originations by stage. See Figure 9 for explanation of layout.


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Figure 12. Stage-level originations (without stage-only genera) arranged in ascending order. Origina-tions per million years; A, cyclostomes, B, cheilostomes. C, D. Originations per standing diversity; C,cyclostomes, D, cheilostomes. Originations per standing diversities per million years; E, cyclostomes, F,cheilostomes.


to the norm for Late Cretaceous and Cen-ozoic stages (Figures 9E, F – 12E, F).Maastrichtian cyclostome values (0.03genera/D/myr for long-ranged genera and0.05 genera/D/myr including stage-only)are far exceeded by Cenomanian andConiacian values, and the Danian valuesare near the median for all stages.Cheilostome generic originations/D/myrfor both Maastrichtian and Danian are onlyslightly above typical values for the Ceno-zoic and are exceeded minimally by Turo-nian and substantially by Cenomanian,Coniacian, and Santonian values; i.e.,Maastrichtian and Danian cheilostome O/D/myr are below the norm of Late Creta-ceous stages but high relative to Cenozoicstages.

DISCUSSION

Potential error

Potential error (represented by bars inFigures 4-6, 9-11) in determining extinc-tion and origination intensities is higher forsmall sample sizes than for larger sam-ples. Standing diversity of cyclostomeswas relatively low in the Albian and in allpost-Danian Cenozoic stages, and stand-ing diversity of cheilostomes was very lowin the Albian, Cenomanian and Turonian(Figure 2). Consequently, error bars forthese are longer than for any other stages.

For the times of lowest diversity enu-merated above, any source of error – suchas how completely the fossil record isknown and random events in ‘background’extinctions and originations – has a pro-portionally greater influence on calculatedextinction and origination rates than duringtimes of higher diversity. Consequently, inthe discussion and interpretations that fol-low, we de-emphasise the earliest (Albian-Turonian) record of cheilostomes.

Extinctions

Maastrichtian/Danian. By virtually allmeasures, generic extinction in the Maas-trichtian was greater for both cyclostomesand cheilostomes than in any other stageduring the past 100 million years. How-ever, it is almost equalled or evenexceeded (Figures 4E, F – 6E, F, except-ing 5F) by bryozoan generic extinction inthe Danian. Error bars for all Maastrichtianand Danian extinction measures overlap,apart from measures of total bryozoan andcyclostome generic extinctions per stand-ing diversity when stage-only genera areincluded (Figures 4D, 5D). The proportionof stage-only genera for both cyclostomes(11 percent) and cheilostomes (14 per-cent) was much higher for the Maastrich-tian than for any other stage; in theDanian, the 3 percent cyclostome stage-only genera is at ‘background’ level, butthe 9 percent cheilostome stage-only gen-era is much higher than the norm of 2 to 3percent. The greater difference in stage-only genera between Maastrichtian andDanian for cyclostomes apparentlyresulted in the higher Maastrichtian thanDanian extinction per standing diversityper million years when stage-only generawere included. It also contributed to lack ofoverlap of error bars for this measure forMaastrichtian and Danian cyclostomes(Figure 5D), as well as for bryozoans as awhole (Figure 4D).

Bryozoans experienced essentiallyidentical generic extinction intensities inthe Maastrichtian and Danian, except thatthe Maastrichtian extinction appears tohave been somewhat more intense thanthe Danian extinction for cyclostomes.Including stage-only genera, extinctionsper standing diversity were slightly higherfor cyclostomes than for cheilostomes inthe Maastrichtian, resulting in a smallerabsolute diversity of cyclostomes relativeto cheilostomes during the Danian. There

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was only a slight decline in within-faunacyclostome species richness from theMaastrichtian into the Danian, part of alonger-term trend (Lidgard et al. 1993).Conversely, there was an abrupt transitionacross the Maastrichtian-Danian boundaryfrom cheilostome to cyclostome domi-nance of assemblage biomass as mea-sured by relative skeletal mass(Håkansson and Thomsen 1979, 1999;McKinney et al. 1998). Therefore, thegeneric extinction pattern stands in sharpcontrast with the abundance patterns.

High generic extinction rates of bryo-zoans at the end of the Cretaceous havebeen noted previously by Viskova (1980,1997), McKinney et al. (1998), and Sepko-ski et al. (2000). This concentration of bry-ozoan extinctions is consistent with a K-Tmass extinction, now generally attributedto impact of an extraterrestrial bolide(Alvarez et al. 1980, and many paperssince). However, our data lack the preci-sion necessary to determine whether bryo-zoan extinctions occurred at the end of theMaastrichtian rather than being distributedmore widely through that stage.

The equally high bryozoan extinctionrates for the Danian must be explained byother cause(s). They apparently correlatewith the loss of carbonate shelf environ-ments across northern Europe, whichhosted a high proportion of bryozoan taxaknown in the Danian fossil record(Håkansson and Thomsen 1999). Thewidespread ‘chalk’-depositing environ-ments were established during the Cen-omanian Stage of the mid-Cretaceous(e.g., Rawson 1992; Gale 2000; Gale etal. 2000) and lasted through to the end ofthe Danian (e.g., Smith and Jeffery 2000).Although local bryozoan diversity andabundance were reduced essentially tozero immediately above the K-T boundaryin the few complete sections studied indetail, both abundance and diversity re-built within a few decimetres of the base of

the Danian section in northern Europe(Håkansson and Thomsen 1979, 1999).The subsequent disappearance of thechalk environments by the end of theDanian and correlated bryozoan extinctionmay possibly be explained by (1) long-term fall in sea-level (Haq et al. 1987) to alevel that shut off oceanic circulation ontothe shelf (e.g., Gale et al. 2000); and/or (2)development or increase of cyclonic circu-lation across the opening Atlantic (Parrishand Curtis 1982).Background extinctions

Background intensities of cheilostomeextinctions, calculated as extinctions permillion years (Figure 6A, B), are similar forthe Upper Cretaceous and Cenozoic,whereas Maastrichtian and Danian extinc-tion rates are substantially greater(although their error bars overlap appre-ciably with those of several other stages).However, Maastrichtian and notablyDanian extinction rates group with thehighly variable earlier Cretaceous extinc-tions in plots of extinctions per standingdiversity (Figure 6C, D) and also withextinctions per standing diversity per mil-lion years (Figure 6E, F). In contrast, forcyclostomes the measures of extinctionrate are much lower for virtually all otherstages than for the Maastrichtian andDanian, especially extinctions per stand-ing diversity (Figure 5C, D). The low pre-Maastrichtian and post-Danian extinctionrates likely are a good reflection of back-ground extinction, which are more con-stant over time than are origination rates(e.g. Van Valen 1985; Gilinsky and Bam-bach 1987).

Extinction rates of cheilostomes andcyclostomes during the past 100 myr havebeen remarkably similar, with a median(‘background’) E/D/myr of 0.009 forcyclostomes and 0.013 for cheilostomes.An arithmetic plot of cyclostome versuscheilostome extinction rates (Figure 13A)

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shows low correlation (r = 0.487) if allUpper Cretaceous and Cenozoic stagesare considered together. However, ifstages are separated into the two majortime intervals, low correlation (r = 0.429) isseen for paired Upper Cretaceous extinc-tion rates, but Cenozoic extinction ratescorrelate well with one another (r = 0.742).The poor correlation in the Upper Creta-

ceous is due largely to high variation inextinction rate of low-diversity, pre-Cam-panian cheilostomes, but not of cyclos-tomes.

Sepkoski et al. (2000) determinedbackground extinction rates for cyclos-tomes and cheilostomes by counting fre-quency of longevity of genera, groupingthem into ‘bins’ of 5-million-year multiples,and taking the slope of log-linear regres-sion for bins other than the shortest (0 to 5million years). Their estimates were 0.31genus/genus-million years for cyclostomesand 0.48 genus/genus-million years forcheilostomes. Background extinction rateof cyclostomes by their calculations is,therefore, 65 percent that of cheilostomes.Our results (previous paragraph) for back-ground extinction rate calculated in a verydifferent way—extinctions per standingdiversity per million years—is remarkablysimilar: cyclostome extinction rate is 69percent that of cheilostomes.Priabonian

Among post-Danian cheilostome andcyclostome extinction rates, the Priabon-ian (latest Eocene) stands anomalouslyhigh in all measures except for cheilos-tome extinctions per standing diversityinclusive of stage-only genera. This isprobably part of the widely recognisedEocene/Oligocene extinction associatedwith the world change from greenhouse toicehouse conditions (Prothero 1994). Wecannot resolve extinction rates in bryozo-ans to zone as has been done for someother taxa affected during the mid- to lateEocene extinction. However, the extinctionof bryozoans appears different from thedetailed extinction patterns documentedfor coccolithophores (Aubrey 1992) andforaminiferans (Boersma et al. 1987).While extinction patterns for these groupsare collectively complex, their respectivetimes and places of most profound extinc-tion and displacement occurred either

Figure 13. Cheilostome versus cyclostome extinctions(A) and originations(B) per stage, plotted as rates perstanding diversity per million years. Blue fields repre-sent Mesozoic, yellow Cenozoic.

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early or late in the middle Eocene and canbe related to successive stages in thelong-term cooling. Eocene extinction ofechinoids also occurred in multiplephases, with the maximum diversity in theLutetian, followed by moderate extinctionat the Lutetian/Bartonian boundary andmaximum extinction during the Priabonian(M. L. McKinney et al. 1992). However,extinction rates of bryozoans in the earlyto middle Eocene (Ypresian – Bartonian)were not above background levels butinstead were intense during the Priabon-ian at a time when extinction rates of othertaxa were declining. A possible reason forthis delayed extinction of bryozoans duringan extended period of global cooling isthat their peak abundance occurs in shelf-depth temperate rather than tropicalwaters (Taylor and Allison 1998). Theorganisms that had been affected in theearlier phase of the extended Eoceneextinction were predominantly tropical anddeep-water.Neogene

Cyclostome extinction rates seem toincrease through the Miocene andPliocene, culminating in a late Pliocenepeak. This apparent increase in cyclos-tome extinctions through the Neogene, ifreal, finds a parallel in coral and molluscextinctions documented in the westernAtlantic and Caribbean (Stanley andCampbell 1981; Petuch 1995; Allmon etal. 1996; Jackson et al. 1993; Budd et al.1996; Jackson and Johnson 2000). Theseextinctions have been attributed to a vari-ety of environmental causes related to theclosure of the Isthmus of Panama andlong-distance effects of intensified glacia-tion.Growth habits

A broad range of colony growth habitshas developed in both cyclostomes andcheilostomes (Lagaaij and Gautier 1965;

McKinney and Jackson 1989; Hageman etal. 1998), most of which can be categor-ised as either encrusting or erect (a minor-ity are free-living or have morphologiesthat are difficult to place, and these are notconsidered here). As a first step towardsanalysis of the ecological history of bryo-zoan extinctions, we examined the extinc-tion rate of encrusting and erect generaover the past 100 million years. Somegenera include both encrusting and erectcolonies, and we assigned a value of 0.5for each such genus to the tally forencrusters and also for erect forms.

The most notable patterns for cyclos-tomes (Figure 14A) are that (1) erectforms went extinct at twice the rate ofencrusters during both the Maastrichtianand Danian; and (2) the Priabonian extinc-tion eliminated only erect genera. Indeedthe Priabonian cyclostome extinction canbe viewed as an intensification of the pat-tern seen for the Thanetian through Chat-tian (i.e., almost the entire Palaeogene)during which no encrusting cyclostomesare known to have gone extinct. Theabsence of encrusting cyclostome extinc-tions during the post-Danian Palaeogeneand its concentration in the Neogene may,however, be a taxonomic artefact giventhat encrusting cyclostome genera arepoorly defined.

Extinction rates of encrusting anderect cheilostomes were similar during theMaastrichtian and Danian (Figure 14B),followed by disproportionally higher peri-ods of extinctions of erect cheilostomesduring the Thanetian and the Priabonian;at other times, encrusting and erectcheilostomes exhibited similar patterns ofextinction rate. The substantial Palaeo-gene to Neogene decline in erect speciesfrom approximately 50 percent to approxi-mately 25 percent of the bryozoan fauna(McKinney and Jackson 1989) may bedue, at least in part, to the Priabonianextinction.

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Our data suggest contrasting extinc-tion patterns of erect and encrustingcheilostome genera in the Pliocene andPleistocene (Figure 14B), with high extinc-tion rates of erect cheilostomes in the

Pliocene followed by low extinction rate inthe Pleistocene, and the opposite patternin encrusting genera. These patterns forgenera parallel the strong Neogenedecline of erect cheilostome species in theCaribbean described by Cheetham andJackson (1996). They noted that thedecline in proportion of erect cheilostomesis in part due to more vigorous speciationof encrusting species but is largely due topreferential extinction of species in erectgenera.Originations

Origination rates for bryozoan genera(Figure 9) do not show the Maastrichtianand Danian anomalies that characteriseextinction rates. In general, originationrates were higher and more variable dur-ing the Late Cretaceous than during theCenozoic and were the cause of the steeprise in overall bryozoan diversity throughthe Late Cretaceous (Figure 2).Cyclostomes

Cyclostome originations were highthroughout the Late Cretaceous (Figures8, 10). Maastrichtian originations are thehighest among these only in three of thesix measures (Figure 10B-D), suggestingthat Maastrichtian originations are part ofthe continuum of high originations duringthe most active period of cyclostomediversification. Following the K-T extinc-tion, however, cyclostome originationsremained very low throughout the Ceno-zoic by most measures, although theremay have been a slight increase in origi-nations during the Neogene (Figure 10E,F). This possible Neogene increase didnot result in an increase in cyclostomediversity (Figure 2) because it wasmatched by a slight increase in extinctions(Figure 5E, F).

Figure 14. Extinctions per standing diversity per millionyears for encrusting and erect (A) cyclostomes and (B)cheilostomes. Standing diversities of erect cyclostomesand of encrusting cheilostomes were relatively largethroughout, but standing diversities of encrustingcyclostomes and of erect cheilostomes were relativelylow.

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Cheilostomes

Cheilostome generic originationsshow an overall pattern of decreasethrough the Late Cretaceous and Ceno-zoic (Figures 8, 11). The decline incheilostome generic origination rate mayreflect the general temporal decline inorigination rates of higher taxa as a pro-gressively greater proportion of new spe-cies are established within previouslyestablished higher level clades (cf. Flessaand Jablonski 1985), or it may mark near-saturation of the ecosystem as suggestedby Sepkoski et al. (2000).

Cheilostome originations during theMaastrichtian and Danian are remarkableonly for the fidelity with which they fitwithin the long-term trend. There are threestages for which originations fall substan-tially below the long-term trend-line (e.g.Figure 11E, F): Upper Palaeocene(Thanetian) and both stages of the Oli-gocene (Rupelian, Chattian). Generic orig-ination rates do not support Voigt's (1981)notion of the Danian as a stage of low 'cre-ativity'. For the Cenozoic, the Danian wascharacterised by high origination rates,even though many of the bryozoan generathought of as typical of the Cenozoic (e.g.,Sertella, Schizoporella, Microporella) didnot appear until later in the Palaeogene.The general taxonomic composition ofDanian cheilostome faunas has greatersimilarity to Late Cretaceous faunas thanto later Cenozoic faunas. This is becausenumerous genera that originated in theCretaceous survived into the Danianbefore becoming extinct, not because ofanomalously few generic originations. Cenozoic contrasts in origination rates

In contrast with the similarity inmedian extinction rates of cyclostomesand cheilostomes, median originationrates (O/D/myr) for cyclostomes are 0.013and for cheilostomes are 0.028. OverallLate Cretaceous through Cenozoic origi-

nation rates of the two clades (Figure 13B)correlate better (r = 0.786) than do overallextinction rates. However, the correlationis almost entirely due to correspondenceof rates during the Cretaceous (r = 0.838)when both clades were vigorously diversi-fying, whereas the rates are almost inde-pendent of one another (r = 0.101) duringthe Cenozoic. The low correlation in theCenozoic is due to the Eocene rebound inorigination rates of cheilostomes, while thecyclostomes had no correspondingrebound.

Our analysis of extinction and origina-tion of post-Palaeozoic bryozoans corrob-orates the inference by Sepkoski et al.(2000) that the essentially flat diversity ofcyclostomes following the K-T extinctionwas due to sustained low origination ratesrather than an increase in extinction rates.Sepkoski et al. (2000) were comparingmid-Mesozoic through Cenozoic diversi-ties of cyclostome and cheilosotme bryo-zoans with coupled-logistic curves inwhich standing diversity of each cladesuppresses origination rate (but has noeffect on extinction rate) of the other.(Parameterization of variables in the cal-culation of the model was based on esti-mates of background extinction rates,equilibrium diversity, and the initial diversi-fication rates only of the bryozoan clades.)The model, perturbed by a sudden diver-sity reduction simulating the K-T extinc-tion, closely matched the actual diversityhistories of cyclostomes and cheilos-tomes. Sepkoski et al. (2000), therefore,concluded that actual diversity history ofcyclostomes and cheilostomes is consis-tent with competitive interference betweenthem, which suppresses origination rates.Our analysis of origination and extinctionof cyclostomes and cheilostomes broadlysupports the assumptions of the Sepkoskiet al. model, although, like Sepkoski et al.,we note that while the history of post-Palaeozoic bryozoan diversity is consis-

22


tent with a model based on competitiveinterference, other biological – or physical– factors may have been influential.

CONCLUSIONS

The diversity histories of cyclostomeand cheilostome bryozoans have followeddifferent trajectories during the past 100million years, although both clades haveexperienced (apparently) simultaneousperiods of anomalously high extinctionwhen data are resolved to stage-leveloccurrences. (At present, they cannot bedifferentiated into finer-scale stratigraphicunits.) The highest, essentially equivalentextinction rates occurred during or at theends of the latest Cretaceous (Maastrich-tian) and earliest Palaeogene (Danian);the latest Eocene (Priabonian) also was atime of high extinction rates for the twoclades.

The Maastrichtian and Priabonianextinctions appear to be parts of well-doc-umented global extinctions that affectedboth terrestrial and marine ecosystems.The Maastrichtian extinction was one ofthe four or five major extinctions of thePhanerozoic (Raup and Sepkoski 1982),whereas the mid- to Late Eocene extinc-tion was in the second tier (Raup and Sep-koski 1984, 1986). The relative scale ofbryozoan extinctions at these two times isproportional to the intensity of the twoextinctions for the biosphere as a whole.Of the bryozoan genera alive at the begin-ning of the Maastrichtian, approximately46 percent were extinct by its end,whereas only 13 percent went extinct dur-ing the Priabonian.

The scale of the Danian extinction ofbryozoans has previously been under-appreciated, but it was almost as intenseas the Maastrichtian extinction, with 30percent of genera alive at the beginning ofthe Danian going extinct. The Danian isnot recognised as a time of major global,

pan-ecosystem extinction. The demise ofso many bryozoan genera appears to bethe result of the end-Danian disappear-ance of the broad carbonate (‘chalk’) seathat had covered northern Europe andparts of Asia since the Cenomanian. Themajority of Danian bryozoan genera areknown from northern Europe, and thosethat went extinct likely were endemic tochalk sea environments. The combinedMaastrichtian and Danian extinction pat-tern for bryozoans is generally similar tothat for echinoids, which showed 36 per-cent and 26 percent extinction of genus-level clades in the Maastrichtian andDanian, respectively (Smith and Jeffery1998). Ending of widespread shallow-water carbonates was suggested by Smithand Jeffery as the probable cause of thehigh rate of Danian extinctions.

The earlier suggestion (Voigt 1981)that the Danian was a time of low ‘creativ-ity’ for cheilostomes is not supported byour data on originations. The Danian hadthe highest Cenozoic rate of O/D/myr forcheilostomes. The Cretaceous affinity ofits faunas is due to the large proportion ofgenera that originated during the Creta-ceous and ranged into the Danian beforegoing extinct; it is not due to anomalouslylow origination rate of new genera.

There is some indication of increasingextinction rate of cyclostomes during theNeogene, although extensive overlap ofthe 95 percent error bars makes the trendequivocal. A simultaneous, similarly equiv-ocal increase in origination rates almostcancels the possible increase in extinctionrate, so that total cyclostome diversitydeclines only slightly during the Neogene.

Cheilostome and cyclostome origina-tion rates correlate in both the Late Creta-ceous and Cenozoic, but origination ratescorrelate only in the Late Cretaceous. Dur-ing the Cenozoic, cyclostomes maintainedlow rates of origination while cheilostomerates were much more variable. This pro-

23


nounced difference in Cenozoic origina-tion rates appears to be the basic causefor the contrasts in diversity histories of thetwo clades and is consistent with the pre-diction of the coupled-logistic curves ofSepkoski et al. (2000) that simulated bryo-zoan diversity based on competitive inter-action between members of the twoclades. This difference in origination ratesduring the Cenozoic also bears on Foote’s(2000a) findings that the post-Palaeozoicdiversity history of gymnolaemates (mostlycheilostomes) is weakly driven more byoriginations than by extinctions, while thepost-Palaeozoic history of stenolaemates(mostly cyclostomes) is driven more byextinctions than by originations. Indeed,stenolaemates have the most stronglyextinction-driven diversity history of allpost-Palaeozoic clades.

ACKNOWLEDGEMENTS

We thank the late J. J. Sepkoski, Jr.for generously providing his database onbryozoan generic ranges. A portion of thispaper was given orally in the Paleontologi-cal Society Sepkoski memorial sympo-sium held at the 1999 Geological Societyof America Annual Meeting, Boulder, Colo-rado (Taylor and McKinney 1999).

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